UBC Theses and Dissertations

UBC Theses Logo

UBC Theses and Dissertations

Exploring the nature of postural sway Murnaghan, Chantelle Dawn 2013

Your browser doesn't seem to have a PDF viewer, please download the PDF to view this item.

Item Metadata

Download

Media
24-ubc_2013_spring_murnaghan_chantelle.pdf [ 2.35MB ]
Metadata
JSON: 24-1.0073647.json
JSON-LD: 24-1.0073647-ld.json
RDF/XML (Pretty): 24-1.0073647-rdf.xml
RDF/JSON: 24-1.0073647-rdf.json
Turtle: 24-1.0073647-turtle.txt
N-Triples: 24-1.0073647-rdf-ntriples.txt
Original Record: 24-1.0073647-source.json
Full Text
24-1.0073647-fulltext.txt
Citation
24-1.0073647.ris

Full Text

EXPLORING THE NATURE OF POSTURAL SWAY by Chantelle Dawn Murnaghan M.Sc., Simon Fraser University, 2008 B.Sc. Hon., Dalhousie University, 2004 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF Doctor of Philosophy in THE FACULTY OF GRADUATE STUDIES (Kinesiology)  THE UNIVERSITY OF BRITISH COLUMBIA (Vancouver)  March, 2013  © Chantelle Dawn Murnaghan, 2013  Abstract Humans are unable to stand still, but rather experience continuous oscillations of the body known as postural sway. While the origins of postural sway are largely unknown, theories suggest that postural sway originates from the interaction between movements of the body (centre of mass, COM) and forces beneath the feet (centre of pressure, COP). The COP is commonly assumed to control or correct for deviations of the body from equilibrium, and delays or errors in control result in postural sway. In a sequence of 5 studies, this thesis used a novel experimental paradigm to investigate how postural sway is controlled or used by the central nervous system.  The first of five experiments tested whether COP displacements would be reduced when the body was externally stabilized, as traditional theories would predict. Contrary to our hypothesis, COP displacements actually increased, suggesting an exploratory role for postural sway. Using the same experimental protocol, Study 2 provided participants with visual feedback of the COM or COP to determine if increases in COP displacements could be the result of sensory illusions or motor drift. Study 3 provided participants with an explicit verbal cue indicating how and when COM stabilization would occur to determine whether increases in COP displacements reflect an attempt to adapt the internal model of the body during stance. Study 4 examined whether increases in COP displacements could be the result of increases in oscillatory cortical drive. Using an upper limb postural task, the fifth and final study extended the findings from Studies 1-4 to determine whether exploratory behaviour may be a more global phenomenon and observed in other postural tasks that do not involve whole body stability. ii  Individually, the results of Studies 1-4 provide evidence which challenges traditional theories of postural control. In addition, they provide evidence against alternative explanations for increases in COP displacements and suggest that this behaviour may be a more global phenomenon and observed in any postural task (Study 5). Collectively, they provide evidence supporting a potential exploratory role of postural sway and question the basis of current clinical practices designed to deal with balance control deficits due to age or disease.  iii  Preface All data contained in this thesis was collected by Chantelle Murnaghan in the Neural Control of Posture and Movement Laboratory within the School of Kinesiology at the University of British Columbia, Vancouver, Canada. All methodologies were approved by the University of British Columbia’s Behavioural Research Ethics Board (ID # H08-02327).  Chapter 2 has been published in Neuroscience [Carpenter MG, Murnaghan CD, & Inglis JT (2010). Shifting the balance: evidence of an exploratory role for postural sway. Neuroscience, 171(1): 196-204]. Carpenter MG was the supervisory author on the project and was involved in concept formation and manuscript composition. Murnaghan CD was the lead investigator and performed all data collection and analysis, and contributed to the study design and manuscript composition. Inglis JT was a supervisory author and was involved throughout the project in concept formation and manuscript composition.  Chapter 3 has been published in Neuroscience [Murnaghan CD, Horslen BC, Inglis JT, & Carpenter MG. (2011). Exploratory behaviour during stance persists with visual feedback. Neuroscience, 195: 54-59]. Murnaghan CD was the lead investigator on the project, responsible for concept formation, data collection and analysis, as well as manuscript composition. Horslen BC was involved in data collection and contributed to revisions of the manuscript. Inglis JT and Carpenter MG were supervisory authors and were involved throughout the project in concept formation and manuscript composition.  iv  Chapter 4 has been published in Gait and Posture [Murnaghan CD, Squair J, Chua R, Inglis JT, & Carpenter MG. Are increases in COP variability observed when participants are provided explicit verbal cues prior to COM stabilization? Gait & Posture, In Press (GAIPOS-D-12-00580R1)]. Murnaghan CD was the lead investigator on the project, responsible for concept formation, data collection and analysis, as well as manuscript composition. Squair J was involved in data collection and contributed to revisions of the manuscript. Chua R was involved throughout the project in concept formation and contributed to revisions of the manuscript. Inglis JT and Carpenter MG were supervisory authors and were involved throughout the project in concept formation and manuscript composition.  The study described in Chapter 5 was submitted and reviewed [Murnaghan CD, Squair J, Chua R, Inglis JT, & Carpenter MG. Does the cortex contribute to exploratory postural sway?]. Murnaghan CD was the lead investigator on the project, responsible for concept formation, data collection and analysis, as well as manuscript composition. Squair J was involved in data collection and contributed to revisions of the manuscript. Chua R was involved in concept formation, technical aspects of the electroencephalographic recordings and contributed to revisions of the manuscript. Inglis JT and Carpenter MG were supervisory authors and were involved throughout the project in concept formation and manuscript composition.  The study described in Chapter 6 will be submitted to a peer-reviewed journal [Murnaghan CD, Chua R, Inglis JT, & Carpenter MG]. Murnaghan CD was the lead v  investigator on the project, responsible for concept formation, data collection and analysis, as well as manuscript composition. Chua R was involved in concept formation, technical aspects of data collection and analysis, and contributed to revisions. Inglis JT and Carpenter MG were supervisory authors and were involved throughout the project in concept formation and manuscript composition.  vi  Table of Contents Abstract .................................................................................................................................... ii Preface ..................................................................................................................................... iv Table of Contents .................................................................................................................. vii List of Figures .......................................................................................................................... x List of Abbreviations and Definitions ................................................................................. xv Chapter 1: General introduction and literature review ...................................................... 1 1.1  Overall goal and specific aims .............................................................................................. 1  1.2  Literature review ................................................................................................................... 4  1.3  Mechanics of human quiet stance and inverted pendulum model ........................................ 7  1.4  Afferent contributions to postural control ........................................................................... 11  1.5  Neural control of posture .................................................................................................... 15  1.6  Theories of postural sway ................................................................................................... 21  1.7  Conclusion .......................................................................................................................... 27  Chapter 2: Shifting the balance: Evidence of an exploratory role of postural sway ...... 29 2.1  Introduction ......................................................................................................................... 29  2.2  Experimental procedures..................................................................................................... 31  2.2.1  Participants ..................................................................................................................... 31  2.2.2  Apparatus ........................................................................................................................ 31  2.2.3  Experimental protocol .................................................................................................... 32  2.2.4  Measurements ................................................................................................................. 33  2.2.5  Statistical analysis........................................................................................................... 35  2.3  Results ................................................................................................................................. 36  2.3.1  Experiment 1................................................................................................................... 36  2.3.2  Experiment 2................................................................................................................... 37  2.4  Discussion ........................................................................................................................... 38  Chapter 3: Exploratory behaviour during stance persists with visual feedback ............ 49 3.1  Introduction ......................................................................................................................... 49  3.2  Methods............................................................................................................................... 51  3.2.1  Participants ..................................................................................................................... 51 vii  3.2.2  Apparatus ........................................................................................................................ 52  3.2.3  Experimental protocol .................................................................................................... 52  3.2.5  Measurements ................................................................................................................. 53  3.2.6  Statistical analysis........................................................................................................... 54  3.3  Results ................................................................................................................................. 54  3.4  Discussion ........................................................................................................................... 56  Chapter 4: Are increases in COP variability observed when participants are provided explicit verbal cues prior to COM stabilization? ............................................................... 63 4.1  Introduction ......................................................................................................................... 63  4.2  Methods............................................................................................................................... 65  4.2.1  Participants ..................................................................................................................... 65  4.2.2  Apparatus ........................................................................................................................ 65  4.2.3  Experimental protocol .................................................................................................... 66  4.2.4  Measurements ................................................................................................................. 66  4.2.5  Statistics .......................................................................................................................... 67  4.3  Results ................................................................................................................................. 67  4.4  Discussion ........................................................................................................................... 68  Chapter 5: Does the cortex contribute to exploratory postural sway? ............................ 76 5.1  Introduction ......................................................................................................................... 76  5.2  Methods............................................................................................................................... 78  5.2.1  Participants ..................................................................................................................... 78  5.2.2  Apparatus ........................................................................................................................ 79  5.2.3  Experimental protocol .................................................................................................... 79  5.2.4  Measurements ................................................................................................................. 80  5.2.5  Statistics .......................................................................................................................... 83  5.3  Results ................................................................................................................................. 83  5.4  Discussion ........................................................................................................................... 85  Chapter 6: Is exploratory behaviour observed in other postural tasks that do not involve whole body stability? ............................................................................................... 96 6.1  Methods............................................................................................................................... 99  6.1.1  Participants ..................................................................................................................... 99  6.1.2  Apparatus ........................................................................................................................ 99  6.1.3  Experimental protocol .................................................................................................. 100 viii  6.1.4  Measurements ............................................................................................................... 100  6.2  Statistics ............................................................................................................................ 103  6.3  Results ............................................................................................................................... 103  6.4  Discussion ......................................................................................................................... 105  Chapter 7: General discussion ........................................................................................... 114 7.1  Summary of results from the thesis ................................................................................... 114  7.2  Thesis contributions to our understanding of the origins of postural sway....................... 117  7.3  Thesis contributions to our understanding of how postural sway is controlled or used by  the CNS .......................................................................................................................................... 119 7.4  Evidence of exploratory behaviour in other tasks/systems ............................................... 123  7.5  Clinical Implications of an exploratory role of postural sway .......................................... 126  7.6  Future directions ............................................................................................................... 128  7.7  Conclusion ........................................................................................................................ 130  References ............................................................................................................................ 131  ix  List of Figures Figure 1-1  Schematic of the inverted pendulum model of the body during stance. Adapted from Murnaghan et al. (2009), the model assumes that the articulated body acts as a rigid segment. The weight of the body (mass*gravity) acts at the centre of mass (COM) and is located at ~2/3 of the participant’s height (L). The body adopts a slight anterior lean (θ) from vertical and rotates about the ankle joint which has a stiffness k. ........................................................... 10  Figure 2-1  Illustration of apparatus and experimental procedures: (A) sagittal and transverse views of the apparatus used to minimize or “lock” AP movements of the COM without the subject’s awareness; (B) raw traces of the AP-COM angular displacement (top trace) and AP-COP displacements (bottom trace) from a representative subject in the Eyes Open group. Dashed vertical lines indicate the boundaries between quiet standing (QS-which was used to calculate the threshold for locking), Unlocked-1, Locked, and Unlocked-2 conditions. Grey boxes indicate the 60 s time periods used for data analysis. Zero on the y-axis represents the mean COP and COM position calculated during the initial 30 s quiet stance period. ...................................................... 46  Figure 2-2  (A) Group means and standard error bars illustrate the significant main effects of condition (pooled across vision) for AP-COM Range (left panel) and APCOP RMS (right panel); (B) x-y plots of AP and ML COP displacements from a representative subject in the Eyes Open group during the Unlocked-1, Locked and Unlocked-2 conditions. Zero represents the mean COP position calculated during the initial 30 s quiet stance period and positive values indicate displacements in the forward and rightward directions. ................... 47  Figure 2-3  Individual AP-COP displacements recorded during the Unlocked-1 condition (grey lines) and Locked condition (black lines) plotted together for each of the 19 subjects in the Eyes Open group. ............................................................... 48  Figure 3-1  Mean changes from Unlocked to Locked for all 16 subjects in each of the three feedback conditions. Top panels illustrate the magnitude of the decrease in RMS of COM angular displacement (deg) for all subjects when Locked x  compared to Unlocked in each of the three feedback conditions (NOFB, COPFB, and COMFB). Bottom panels illustrate the concurrent changes in RMS of COP displacements (mm) for all subjects when Locked compared to Unlocked in each of the feedback conditions. Black lines represent subjects who showed increases in COP displacements, while grey lines represent subjects who showed decreases in COP displacements, when movement of the COM was minimized. ..................................................................................... 61 Figure 3-2  Individual subject traces in each of the three feedback conditions. Upper panels illustrate the COM angular displacements (deg) over the 60s periods used for data analysis in the Unlocked (grey) and Locked (black lines) conditions. Bottom panels illustrate the corresponding COP displacements over the 60s period used for data analysis in the Unlocked (grey) and Locked (black lines) conditions. .................................................................................. 62  Figure 4-1  Mean RMS of anterior-posterior COP displacements for all subjects in the no cue (top panel) and cued (bottom panel) conditions. Grey boxes represent the Unlocked condition, while black boxes represent the Locked condition. ...... 74  Figure 5-1  Illustration of experimental procedures used to screen participants for inclusion in the study. (A) Participants performed two two-minute seated trials. In the first trial, participants were completely relaxed, and in the second trial they maintained a low-level voluntary contraction of the plantar flexor musculature against a load (~30% MVC). (B) To be included in the study, participants were required to achieve significant magnitudes of coherence (>95% confidence interval) in the 15-30 Hz range in at least one muscle during the voluntary contraction (top panel, solid line). In addition, the magnitude of coherence had to be significantly greater than that achieved during the seated relaxed trial (top panel, dashed line). Significant differences were determined using a difference of coherence (DOC) test (bottom panel), and having the DOC exceed the 95% confidence intervals. If the DOC exceeded the lower interval, the magnitude of coherence during the voluntary contraction was statistically larger than the coherence estimated in the relaxed condition. ........................................................................................................ 91 xi  Figure 5-2  Sagittal plane view of the apparatus used to stabilize the COM without participants’ knowledge. During the trial, participants were firmly braced with their back against a rigid board with adjustable straps tightened firmly around the shoulders, chest, waist, hips/upper thighs, and upper shank, to prevent movement at any joint except the ankle. The board was attached to a closedloop pulley system that allowed “normal postural sway‟ at the ankle joint unless the experimenter applied a brake that discretely locked the board (and thus COM) in place in the sagittal plane. Participants wore earplugs to eliminate any auditory cues, and blinders designed to occlude both horizontal and vertical peripheral vision, while maintaining full visual input anteriorly. In all conditions, participants stood with their arms crossed and feet shoulder width apart on a forceplate, and we measured EEG and bilateral surface EMG from lateral and medial gastrocnemius and soleus muscles. .......................... 92  Figure 5-3  Average COM (top panel) and COP displacements (bottom panel) in the Unlocked (grey boxes) and Locked (black boxes) conditions. Across all 12 participants, COM RMS was significantly reduced in the Locked compared to Unlocked condition. Stabilizing the COM resulted in a significant increase in COP displacements in 9 of 12 participants. .................................................... 93  Figure 5-4  Estimates of coherence between EEG (Cz) and EMG (left MGAS) from a representative subject. (A) During a seated low level voluntary contraction, the participant achieved significant levels of coherence (top panel, solid black line). The difference of coherence test (bottom panel) illustrated that the magnitude of coherence during the voluntary contraction (top panel, solid line) was significantly larger than during the relaxed condition (top panel, dashed line). (B) When standing in the apparatus, there was little to no coherence in the Unlocked condition (top panel, grey line). The magnitude of coherence did not increase and also showed little to no coherence in the Locked condition (top panel, black line). The difference of coherence test confirmed that there was no significant difference in coherence between the Unlocked and Locked conditions (bottom panel). .......................................... 94  xii  Figure 5-5  Estimates of coherence pooled across the 9 participants who showed an increase in COP displacements following COM stabilization. (A) There were significant magnitudes of coherence in the seated voluntary contraction (top panel, solid lines) in the 15-30 Hz frequency range across all muscles recorded (LGAS-red, MGAS-blue, and SOL-green), and the DOC (bottom panel) illustrated that this magnitude was significantly greater than the magnitude of coherence in the seated relaxed trial (top panel, dashed line). (B) When standing in the apparatus, there was little to no coherence in the Unlocked condition (top panel, dashed lines). The magnitude of coherence did not increase and also showed little to no coherence in the Locked condition (top panel, solid lines). The difference of coherence test confirmed that there was no significant difference in coherence between the Unlocked and Locked conditions (bottom panel). .............................................................................. 95  .Figure 6-1  Schematic of the setup used for the upper limb postural task. Participants were asked to lie in a supine position on a solid support surface with the arm pointing vertically and the palm facing medially. Any flexion or extension at the wrist and/or elbow was prevented by splinting both joints, forcing all movement to occur about the shoulder. At the level of the wrist, the splint was attached to a closed-loop pulley system that allowed normal displacements of the arm unless the experimenter applied a brake that discretely locked the arm in place in the sagittal plane. Forces in the sagittal plane were measured using a force transducer that was embedded in the splint and connected in series with the cable. ............................................................................................... 110  Figure 6-2  Diagram illustrating how angular accelerations that would be expected to occur if the arm were freely moving were calculated. Time-varying torque at the shoulder (Tshoulder) was calculated in the Locked condition. These measures of torque were then used to estimate the accelerations of the arm that would be expected if the arm was Unlocked and could move freely. Moment of inertia (Ishoulder) was calculated using anthropometrics as described in the text, and used to estimate the angular acceleration of the arm (α). ............................. 111  xiii  Figure 6-3  Accelerations and power spectra from a representative participant during a visual feedback trial in the Unlocked (left panels) and Locked (right panels) conditions. Plots of acceleration (top panels) illustrate the increased accelerations in the Locked compared to Unlocked condition. Plots of power spectra illustrate the shift to dominant lower frequency components (~2.5 Hz) in the Locked compared to Unlocked condition. Y-axes on graphs of power spectra have been optimized for visual purposes. ......................................... 112  Figure 6-4  Mean ± SE for the range of cable displacements (top graph), RMS (middle graph) and MPF (bottom graph) of accelerations in the Unlocked (grey bars) and Locked (black bars) conditions when participants performed the trials with eyes closed and with visual feedback of arm angular displacements. There was a significant main effect of locking on the range of cable displacements (top panel) and MPF of accelerations (bottom panel), and a significant interaction between lock and vision on the RMS of accelerations (middle panel). .............................................................................................. 113  xiv  List of Abbreviations and Definitions Abbreviations:   Central nervous system (CNS)    Centre of mass (COM)    Centre of pressure (COP)    Electromyography (EMG)    Electroencephalography (EEG)    Corticomuscular coherence (CMC)  Operational Definitions:   Central Nervous System: one of the two major divisions of the nervous system containing the brain and spinal cord.    Afferent: Carrying toward. An afferent nerve carries impulses toward the CNS.    Efferent: Carrying away. An efferent nerve carries impulses away from the CNS.    Stiffness: Ankle joint rotation results in elongation of the series contractile tissue (muscle) and in changes in tension of the muscle tendon unit (Loram, Lakie et al. 2009). This stiffness, or resistance to angular displacement, is often measured as the slope or the torque vs. angular displacement trace. The slope provides a measure of the overall ankle joint stiffness and is due to a variety of mechanisms, including any voluntary motor commands, segmental reflexes, and the passive force–deflection and force–velocity properties of the muscles, tendons, and ligaments spanning the ankles (Murnaghan, Elston et al. 2009).    Postural Equilibrium: The state in which the sum of all the forces and moments acting on the body are balanced such that the body tends to stay in the desired position and orientation (static equilibrium), or is able to progress through an intended movement without losing balance (dynamic equilibrium).    Stability: The body can stray from its point of equilibrium but be maintained within an area that does not allow a fall to occur. Specifically, during quiet standing, a person is said to be in a stable posture as long as the line of action of the person's COG passes through (within) his or her base of support. Stability is often described in relative terms and is a continuum based on the magnitude or area of postural sway. xv    Exploratory Behaviour: Movement of a body or limb arising from passive and/or active mechanisms that serves to stimulate perceptual systems (Gibson, 1962; Riley, Mitra, Stoffregen, & Turvey, 1997).  xvi  1 Chapter: General introduction and literature review 1.1 Overall goal and specific aims During quiet standing we can never stand perfectly still. We constantly experience small, involuntary oscillations of the body known as postural sway that cannot be suppressed even during concentrated efforts. There is little consensus on the origins or role of postural sway during stance. Postural sway is typically described as the result of noise or errors in the postural control system, providing little to no relevant information. However, some have suggested that postural sway may provide valuable information to the postural control system. Therefore, the overall goal of this thesis was to investigate how postural sway is controlled or used by the CNS.  To address this goal, this thesis investigated five specific aims. Aim 1 was to determine experimentally whether the postural control system operates in a pure negative feedback manner, where ground reaction forces beneath the feet (centre of pressure – COP) are used to minimize movements of the body (centre of mass – COM) during stance. It was hypothesized that COP displacements would be minimized following an external stabilization (“locking”) of the body during stance. Contrary to the original hypothesis, the results showed that increases in COP variability persisted when movement of the body was stabilized without subjects’ knowledge, suggesting that postural sway under normal stance conditions may be used as an exploratory means of acquiring sensory information.  1  Based on the results obtained from aim 1, aim 2 was to try and replicate our previous results and to determine whether the effects of COM stabilization (“locking”) on COP displacements could be attributed to alternative mechanisms such as sensory illusions or motor drift. To address this aim, participants were provided visual feedback of the COP beneath the feet (COP) or movement of the body (COM) throughout the trial. If there was an influence of sensory illusions, this thesis hypothesized that the change in COP displacements from Unlocked to Locked would be significantly reduced when participants were provided definitive visual confirmation that the COM had been stabilized. If there was an influence of motor drift, it was hypothesized that the change in COP displacement from Unlocked to Locked would be significantly reduced when participants were provided visual feedback of the COP and thus were aware of, and able to confirm, its position throughout the trial. Results showed that increases in COP displacements persisted, and actually increased further with visual feedback, again providing support for an exploratory role of postural sway.  Aim 3 was to determine whether increases in COP variability observed following COM stabilization, could be explained by an attempt to adapt or create a new internal model of the body during stance. To address this aim, participants were provided an explicit verbal cue indicating how and when displacements of the COM would be minimized by the experimenter. This thesis hypothesized that if increases in COP displacement were the result of an attempt to adapt an internal model of the body during stance, there would be a significant interaction. More specifically, COP displacements would decrease from Unlocked to Locked when participants were provided an explicit verbal cue, and increase when no cue was provided. The results showed that COP displacements increased similarly in the non2  cued and cued conditions, suggesting that increases in COP displacements with locking were not the result of an attempt to adapt an internal model of the body, and providing further support for an exploratory role of postural sway.  Aim 4 was to determine whether the origin of increases in COP displacements observed following COM stabilization may be explained by increases in cortical drive to muscles of the lower leg. To address this aim, the linear relationship between oscillatory activities in the cortex (measured using electroencephalography -EEG) was estimated using a statistical measure known as corticomuscular coherence. Based on previous studies, it was hypothesized that, in the majority of participants, there would be an increase in COP displacements with locking. Since corticomuscular coherence may provide an indication of greater cortical drive to the muscles, it was further hypothesized that, in those participants whose COP increases with locking, significant increases in coherence at frequencies in the range of 15-30 Hz would also be observed. The results replicated previous results and showed that when displacements of the COM were minimized by the experimenter without participants’ knowledge, COP displacements increased in 75% of participants. Although it was hypothesized that increases in COP would be associated with increases in CMC, little to no CMC was found in both the Unlocked and Locked conditions, suggesting that increases in COP were not the result of increases in cortical drive.  Finally, aim 5 was to determine whether increases in variability would be observed with locking in an upper limb postural task does not involve whole body stability. To address this aim, participants were placed in a supine position with the arm pointing vertically and 3  the arm attached to the closed-loop pulley system used in Studies 1-4. During the upper limb postural task, it was hypothesized that, following an external stabilization of the arm, fluctuations in horizontal forces would predict arm angular accelerations that exceeded those measured in the Unlocked condition. The results showed that the forces recorded following arm stabilization predicted arm angular accelerations that were larger than those recorded when the arm was freely moving. The evidence from this study suggests that exploratory behaviour may be a more global phenomenon, and observed in any task that requires the maintenance of a static position of the body or a limb.  1.2 Literature review  Postural control is generally defined as the ability of the central nervous system (CNS) to maintain the basic body posture, which for humans is an upright standing position (Deliagina, Orlovsky, Zelenin, & Beloozerova, 2006). Although standing in humans appears to be a simple and innate task, it is actually a very complex motor behaviour. In general, the postural control system has two main functions: (1) to build up posture against gravity and ensure that balance is maintained; and (2) to fix the orientation and position of the segments that serve as a reference frame for perception and action with respect to the external world (Massion, 1992). There are various contexts in which the postural control system carries out these functions. For example, we require precise and context-appropriate control when holding postural configurations (i.e. quiet standing). In addition, the postural control system must act in a compensatory manner to regain an upright posture when we experience an external perturbation. Furthermore, we must stabilize the body in an anticipatory manner when performing a voluntary movement or experiencing an internal perturbation to balance. 4  In the past 50 years, a great deal of research has been performed in all three areas, however there is still little consensus on the mechanisms underlying postural control (Gatev, Thomas, Kepple, & Hallett, 1999; Nashner, 1976; Prieto, Myklebust, Hoffmann, Lovett, & Myklebust, 1996; van der Kooij, van Asseldonk, & van der Helm, 2005; Winter, Patla, Prince, Ishac, & Gielo-Perczak, 1998).  The study of quiet standing in humans or “station” dates back many years with the first reported “recordings” of man standing at rest by Vierordt in 1860 (Fearing, 1924). In clinical settings, time to maintain a given posture was frequently documented, however many studies used a measure of body movement or sway to investigate the performance of the postural control system (Winter et al., 1998). According to Fearing (1924), measures of body sway in these original studies (mostly from the late 1800s) measured anterior-posterior (AP) and medial-lateral (ML) oscillations of the body using a variety of crude measurement tools including feathers and chalk, cardboard placed on top of the subjects head, and a novel invention called the ataxiameter. Fearing, Miles and others at this time investigated everything from how training could improve postural control to the effects of height, weight, respiration, menstrual cycles and gender. The implicit underlying assumption in the measurement of body sway is that it is the body or centre of mass of the upright body (COM) that is controlled in the gravitational environment during stance (Winter et al., 1998). However, as is still the case today, what it is that sway represents is largely unknown.  With technological advancements came the development of the first force platform in France in the 1950s (Gagey, 1992). This instrument allowed for more objective measures of 5  quiet standing in man. The forceplate enabled measurement of the centre of pressure (COP), or the resultant ground reaction forces acting on the feet. Further technological advancements included optical motion capture systems, which allowed precise measures of very small movements of the body. Using these measures, accurate estimations of the body’s centre of mass (COM) could be calculated. Now the study of postural sway had two main variables that could capture the characteristics of this seemingly simple but complex action in humans: movement of the body or COM, and displacements of the COP beneath the feet. Researchers agreed that there was a relationship between these two variables, and many erroneously used one synonymously with the other as a measure of “sway” (F. Horak & MacPherson, 1996; Winter, Patla, & Frank, 1990; Winter et al., 1998). However, how they worked together and what the “link” was between these two variables was the topic of many debates during this time at the International Society of Posturography (now the International Society of Posture and Gait Research) (Gagey, 1992). We now have a better understanding of the relationship between COP and COM because of theoretical studies (Gurfinkel, 1973), spectral property studies, as well as measures of both variables at the same time during stance (Gage, Winter, Frank, & Adkin, 2004; Winter et al., 1998). We now know that COP displacements are of higher frequency and larger amplitude, and track movements of the lower frequency, lower amplitude COM. COP is believed to represent the net neuromuscular control at the ankle and is controlled by plantar/dorsi flexor torque in the anterior-posterior plane, and hip torque in the medial-lateral plane (Winter et al., 1998). COP is often labeled as the controlling variable which regulates or controls displacements of the body or COM (Winter et al., 1998).  6  1.3 Mechanics of human quiet stance and inverted pendulum model  To comprehend the particular complexity of maintaining an upright posture in humans requires an understanding of the mechanics of bipedal standing. During human standing, many articulated body segments are aligned such that ~2/3 of our total body mass is positioned at ~2/3 of our height above the ground (Winter et al., 1990; Winter, 1995). This mass is then supported by the two legs and feet, which provide the only source of contact with the ground, creating the base of support (BOS) (Winter et al., 1990).  The behaviour of the body during stance is typically represented by the centre of mass (COM), the point equivalent of the total body mass in the global reference system. The whole body COM is the weighted average of the COM of each body segment in threedimensional space. The vertical projection of the COM toward the ground is called the centre of gravity (COG) (Winter & Eng, 1995). We often portray natural stance in humans as having each body segment perfectly positioned on top of another, with the COG projecting through the ankle joint, or point of rotation in the anterior-posterior plane. However, it is well known that humans adopt a slight anterior lean, where the COG is positioned midway along the anterior-posterior length of the foot (F. A. &. F. Hellebrandt E.B., 1943; Thomas & Whitney, 1959). In this slight anterior position we are particularly exposed to the effects of gravity. The gravitational force acts approximately at the COM, creating a toppling torque that pushes the body toward the ground. To remain upright, this torque must be countered with equal and opposite forces to maintain the mass of the body in an upright position (Gurfinkel & Osovets, 1972; Loram, Kelly, & Lakie, 2001; Smith, 1957; Winter et al., 1998). 7  Although a slight anterior lean always places the COG anterior to the ankle joint during quiet standing, its position is not always constant. Closer observation reveals that we are in constant motion. The body undergoes small and seemingly random oscillations during stance, which persist even with conscious attempts to minimize such movement (Thomas & Whitney, 1959). This movement is what I have described above and is known as postural sway. Initial “recordings” of this behaviour by Karl von Vierordt, illustrate that this sway occurs primarily in the anterior-posterior plane, with relatively smaller displacement in the medial-lateral plane (Fearing, 1924). The mean frequency of postural sway is 0.27-0.45 Hz (Carpenter, Frank, Winter, & Peysar, 2001), and these small oscillations are associated with sagittal plane angular changes of approximately 1.0-1.5 degrees at the ankle, knee and hip joints (Gage et al., 2004; Gatev et al., 1999), and COM horizontal displacements ranging from 4-18 mm (Gatev et al., 1999; Winter et al., 1998).  Postural sway of the human body during stance is commonly modeled as an inverted pendulum (Figure 1-1) (Gage et al., 2004; Gurfinkel & Osovets, 1972; Smith, 1957; Winter et al., 1998). In this model, the body above the ankle is assumed to act as a single rigid segment, supporting a single point mass (the COM), which rotates about the ankle joint (Winter et al., 1998). When the pendulum sways forward, a proportionally greater amount of torque at the ankle is required to prevent the body from toppling due to the effects of gravity. In contrast, as the body sways backward, and angular displacement from vertical is minimized and proportionally less ankle torque is required to prevent the body from toppling. Therefore, the gravitational torque acting at the COM increases linearly with ankle angle, and this is referred to as the toppling torque or toppling torque per unit angle (Loram and Lakie 8  2002). While some have argued that we cannot assume the multi-articulated body acts as a rigid segment, the inverted pendulum model of stance has been validated as an appropriate representation of the overall behaviour of the body in the sagittal and frontal planes using kinematic, kinetic, and electromyographic (EMG) analyses (Gage et al., 2004; Gatev et al., 1999; Winter, Prince, Frank, Powell, & Zabjek, 1996; Winter et al., 1998). The advantage of representing the body in this manner is that the model reduces the system to a single degree of freedom, focusing on the ankle joint, where the destabilizing effects of gravity largely exhibit their influence.  9  Figure 1-1  Schematic of the inverted pendulum model of the body during stance. Adapted from Murnaghan et al. (2009), the model assumes that the articulated body acts as a rigid segment. The weight of the body (mass*gravity) acts at the centre of mass (COM) and is located at ~2/3 of the participant’s height (L). The body adopts a slight anterior lean (θ) from vertical and rotates about the ankle joint which has a stiffness k.  10  The COM of the inverted pendulum is thought to be controlled through the development of ground-reaction forces, which can be recorded using the forceplate. The vector sum of all of the ground-reaction forces under the feet is used to calculate the centre of pressure (COP), which is comprised of two different components: (1) the gravitational projection of the COM (COG); and (2) torques generated at the ankle joint (dorsiflexion/plantar-flexion) in the anterior–posterior (AP) plane and the hip joint (abduction/adduction) in the medial–lateral (ML) plane (Winter et al., 1996).  1.4 Afferent contributions to postural control  The postural control system requires information concerning its own state and that of its surroundings. This information is transferred from sensory receptors located in the periphery to the central nervous system via afferent pathways (Enoka, 1994). According to Gagey (1992), in 1837 keen interest concerning the source of this afferent information developed with Charles Bell asking “How does a man maintain a standing or bending posture against the wind that blows against him? He obviously has a sense through which he knows his body’s degree of bending and he has the ability to readjust it and to rectify any deviation from the vertical. What sense is that?” These perceptive questions illustrated an awareness of external forces acting on the body, and that afferent information provided by an unknown source must be forming a coherent interpretation of the body’s orientation in space.  During this era, it was believed that there was one organ providing one sense. As such, researchers pursued discovery of the “sense of equilibrium,” the sense which provided information on the body’s orientation. A host of various organs were discovered and 11  identified as the contributor to our sense of equilibrium: the eye (Romberg, 1853), the vestibule (Flourens P., 1829), cervical muscles (Longet R.A., 1845), the foot (Heyd, cited by von Vierordt K., 1860) and even the oculomotor muscles (de Cyon E., 1911) (all c.f. (Gagey, 1992)). However, it was Karl von Vierordt in 1860 who suggested that perhaps all of these organs could work together and participate in the same function.  Our current understanding is that there are three major sensory systems contributing to postural control: the somatosensory, vestibular, and visual systems. Many experiments have been published illustrating the contributions of each of these subsystems to postural control (Dietz, 1992; F. Horak & MacPherson, 1996; Winter, 1995). In humans, these experiments typically assess the role of a particular source of sensory input in healthy populations by removing, reducing, or distorting the information it provides during standing. Alternatively, patients with disorders affecting particular sources of afferent information have been used to investigate whether there is a change in postural control associated with a loss of information. Reliance on a particular source of sensory information is typically confirmed with changes in postural sway.  The somatosensory system is the most complex afferent system and provides sensation from many types of receptors located throughout the entire body. These include receptors in skin (touch or cutaneous receptors), muscles (muscle spindles), tendons (golgi tendon organs), and joints (joint receptors), all of which provide critical information about postural orientation and equilibrium (Dietz, 1992; F. Horak & MacPherson, 1996). More specifically, receptors located in muscles, joints (and some would argue skin (D. F. Collins, 12  Refshauge, Todd, & Gandevia, 2005)), transduce information about the relative configuration of body segments, while skin receptors in the foot sole transduce information about the pressure and contact forces between the feet and the ground. Investigations into the role of various somatosensory receptors in quiet standing typically manipulate the sensitivity (i.e. cooling the feet to reduce sensitivity of cutaneous receptors in the foot) (Asai et al., 1992; Orma, 1957), or distort (i.e. vibration to stimulate muscle spindles) available input from various receptors (Roll, Vedel, & Roll, 1989). Alternatively, studies use patients who exhibit peripheral nerve damage (i.e. individuals with peripheral neuropathy) (Nardone et al., 2000). These methods have shown that postural sway increases when subjects have reduced or inaccurate somatosensory information available to them (Dietz, 1992; F. Horak & MacPherson, 1996; Jeka, Kiemel, Creath, Horak, & Peterka, 2004).  The stabilizing effects of vision on posture have been established since clinical observations in the 1800’s (Dietz, 1992). In the complete absence of visual input (eye closure), Romberg documented that there is a 30% increase postural sway (Lanska and Goetz 2000). Even with the eyes open, body sway becomes progressively greater as visual acuity decreases (Paulus, Straube, & Brandt, 1984). Increases in postural sway are also observed as the distance between the eye and a stationary target is increased, or the characteristics of a stationary visual surround are altered (F. B. Horak, 1996; F. Horak & MacPherson, 1996; Paulus et al., 1984; Straube, Krafczyk, Paulus, & Brandt, 1994). Interestingly, visual cues may also provide illusory sensations of self-motion. Linear motion of a visual surround can create the sensation that the body, rather than the surround, is in motion, eliciting compensatory sway behaviour (Dietz, Schubert, & Trippel, 1992; Lee, 1980). 13  The role of the vestibular system in quiet standing is somewhat more controversial. The system is comprised of two types of specialized receptors located bilaterally within the inner ear (labyrinth). The first receptors are the otoliths, which transduce information about the head orientation in the gravitational field, as well as linear acceleration of the head. The second type of receptor is the semicircular canals, which transduce information on angular acceleration of the head (Kandel, Schwartz, & Jessell, 2000). Vestibular input alone cannot lead to conscious perception of movement during quiet standing (R. Fitzpatrick & McCloskey, 1994), however it does appear to be used subconsciously in the control of posture, with some referring to it as the “silent sense” (Day & Fitzpatrick, 2005). The role of the vestibular system becomes apparent when other sensory inputs are made unavailable or inaccurate. For example, patients with bilateral vestibular loss can exhibit sway similar to that observed in healthy controls when all sensory information is available (Dietz, 1992; Yoneda & Tokumasu, 1986), as well as when one of the two remaining sensory inputs (somatosensory and vision) is removed. Yet, when required to rely on accurate input supplied only by the vestibular system, they will fall when standing quietly (R. C. Fitzpatrick, Taylor, & McCloskey, 1992; Nashner, Black, & Wall, 1982). This is strong evidence for a role for vestibular input during quiet standing.  While it has been shown that all three sensory systems contribute to postural control, there is ongoing debate as to how and where this afferent information is integrated to provide a representation of the body’s orientation, as well as whether one system is more vital than another (R. Fitzpatrick & McCloskey, 1994; F. Horak & MacPherson, 1996). We do know that movement of the body during stance, known as postural sway, is smallest when all 14  sensory inputs are available (R. C. Fitzpatrick et al., 1992). The many channels of available sensory information lead to redundancies, which help to resolve any ambiguities and to accurately interpret sensory information that is relevant to standing. While it is optimal to have sensory information from all sources available, all inputs are not required. This is because humans are very adept at compensating for a loss of information from one or more sources. However, it is important to note, that we may not be able to compensate for a complete loss of somatosensory information. Patients with complete proprioceptive loss are not able to stand without highly concentrated effort (which is not required for natural standing) (Cole & Sedgwick, 1992). This illustrates that the postural control system can be quite proficient despite a loss of vestibular or visual information, yet be ineffective when deprived of somatosensory information.  1.5 Neural control of posture  Maintaining an upright position during stance and throughout dynamic activities largely does not require conscious, volitional control. Rather, the fundamental neural mechanisms underlying this control seem to be innate and automatic (Deliagina et al., 2006; Massion, 1998). Although the ease with which we maintain balance may suggest a straightforward and simple postural control system, the sheer number of studies which have tried to elucidate the neural mechanisms responsible for controlling posture, suggests that it is a much more complicated system than perhaps was initially postulated (Gatev et al., 1999; Loram & Lakie, 2002; Loram, Maganaris, & Lakie, 2004; van der Kooij et al., 2005; Winter et al., 1998).  15  Most of our erect, anti-gravity posture is maintained by means of passive stiffness in connective tissue within and around muscle (Thomas & Whitney, 1959; Winter et al., 1998). This passive stiffness can be supplemented in some body segments with low-level background (tonic) muscle activation which acts to increase the stiffness further, and resist displacement of the body, which is under the constant force of gravity (F. Horak & MacPherson, 1996). Although tonic muscle activity plays a significant role in maintaining an erect posture, it is limited to only a few muscles including the soleus (calf muscle), iliopsoas (hip flexor), and occasionally neck muscles (Joseph & Nightingale, 1952; Thomas & Whitney, 1959). Tonic activation is primarily observed in the soleus muscle due to the anterior position of the COM, and even in this muscle, the mean level of contraction amounts only to 15-20% of the available contractile force (F. A. &. F. Hellebrandt E.B., 1943; Joseph & Nightingale, 1952; Smith, 1954).  Original theories on the control of posture in humans supported a stretch reflex control of posture. Passive stiffness and low-level tonic activation were believed to maintain a static position of the body when minimal torque was required to maintain balance. However, Hellebrandt and Brogdon (1938) recognized that upright stance is associated with degrees of postural sway which must “markedly alter the tone demanded of the antigravity muscles” to maintain balance. As such, they suggested that as we sway forward, the muscles and muscle spindles of the triceps surae stretch, increasing the firing rate of Ia afferents. Consequently, this spindle afferent information initiates a reflexive response, which generates a contraction in homonymous muscle, and acts to move the body back to vertical. Therefore, he suggested that posture was controlled via a stretch reflex strategy or ‘geotropic 16  reflex’ strategy. However, many have since argued that stretch reflexes are not responsible for generating the plantar flexor torque necessary for controlling movements of the COM. This is based on findings of insufficient stretch of the calf muscles (Kelton & Wright, 1949), and absence of stretch reflexes observed when participants experienced tiny rotations of the support surface (Gurfinkel, Lipshits, & Popov, 1974) . Over the years, the theoretical framework for posture has generally changed to a central organization of posture that does not regulate the ankle angle or muscle length, but a more global parameter such as the position of the COM (Dietz, 1992; Gatev et al., 1999; F. Horak & MacPherson, 1996). While there is no sensory receptor that can directly monitor the position of the COM, it is most likely estimated through integration of sensory information from various sources including visual, vestibular and somatosensory (F. Horak & MacPherson, 1996).  Under the assumption that COM is the controlled variable during stance, Winter et al. (1998), proposed that humans maintain balance via stiffness control. However, he did not believe that sensory thresholds are exceeded or necessary to control movement of the body during quiet standing. He suggested that no active intervention is required to oppose the natural displacement of the COM during stance. Instead, the central nervous system is able to set the tone of calf musculature in order to increase the stiffness to a level that is sufficient to support the load of the body. In this model, the combination of passive stiffness and tonic muscle activation acts instantaneously to increase force and generate adequate torque to oppose forward sway of the body before a peripherally or centrally driven signal could dynamically change muscle activation (Horak and MacPherson 1996; Winter, Patla et al. 1998). Action of the muscle-tendon complex in this mechanism is analogous to an elastic 17  band, which stretches, thereby increasing tension when the body sways forward, and recoils to bring the body back to vertical.  More recently, others have argued that active modulation is required to supplement stiffness control of posture (Loram & Lakie, 2002; Loram, Maganaris, & Lakie, 2005; Loram, Gawthrop, & Lakie, 2006; Loram, Lakie, Di Giulio, & Maganaris, 2009; Morasso & Schieppati, 1999; Morasso & Sanguineti, 2002). Stiffness control of posture requires that the level of torque created by the combination of passive stiffness and muscle tone exceed a critical threshold to counter the gravitational forces, which create the toppling torque. This critical threshold is determined by properties of the standing body (mass, height of COM, gravitational forces, and the angle of the body from vertical). If the ankle joint stiffness is less than the critical threshold, active neural modulation is required. Several reports have suggested that the stiffness of the ankle joint is at most 91% of the critical threshold (Loram & Lakie, 2002), emphasizing the necessity of additional active modulation. While the mechanical stiffness of the activated muscle itself could be sufficiently stiff to support the body, the intrinsic stiffness of the whole ankle, including the tendon and foot, is determined by the weakest link in the entire series elastic component. However, because a neural delay exists between changes in muscle activity (EMG) and changes in torque, Loram and Lakie (2002) proposed a postural control system that uses ankle joint stiffness supplemented with feedforward or anticipatory neural control of ankle torque. This feedforward control of torque is based on accurate predictions of COM movement from available sources of sensory information. This theory is corroborated by changes in EMG which occur in advance of COM or COP displacements(Gatev et al., 1999). 18  Rather than simply predicting COM displacements, some theorists and modellers have proposed much more complex control schemes. One prominent theoretical concept in motor control, which has more recently been applied to the control of posture, is that complex computations are simplified by building internal models within the CNS (Morasso, Baratto, Capra, & Spada, 1999; Wolpert, Ghahramani, & Jordan, 1995). Internal models are the neural representations of the expected behaviour of an object or system (i.e. the whole body during stance) in response to a given neural command, and therefore describe the input/output relationships of the system (Wolpert et al., 1995). Feedback control alone would be insufficient, given the delays in sensory feedback described above (Kawato, 1999). Therefore, internal models can resolve this issue since they can be used to estimate appropriate motor commands or predict sensory consequences of these commands (Wolpert et al., 1995). According to Wolpert and Kawato (1998a), the motor system is able to use multiple internal models, or adapt the current model, to the dynamics of the object or system. For example, the CNS can use a forward model to predict the sensory consequences of their motor commands. Based on the comparison between the predicted and actual sensory consequences, on-line corrections can be made and a more appropriate model can be selected, or the current one can be adapted (Wolpert & Kawato, 1998b; Wolpert & Ghahramani, 2000).  The majority of neural control mechanisms described above assume that as the body sways forward, the tonically active calf muscles stretch. If intrinsic ankle stiffness is insufficient to support the body, afferent information provided by length sensitive muscle 19  receptors (spindles), can signal the generation of spinal or central reflex pathways. However, Loram et al.(2004), argued that perhaps an alternative control mechanism was taking place when intrinsic stiffness is too low to support the body. They suggested, based on ultrasound measures that, as the body sways forward, the ankle torque required increases, and tension in the series elastic component (calf muscles, tendon and connective tissue of the foot) increases. However, the tension does not result from the lengthening of all series elastic components. Instead, the tendon lengthens and the muscle is actively shortened. This active shortening of the muscle then produces additional elongation, and therefore tension, in the tendon. As such, they suggested a slight variation in the active component of the control mechanism, one that incorporates anticipatory control of muscle length as opposed to anticipatory control of stiffness, and further advocate for the anticipatory control of posture.  While there are some more recent models of postural control based on more complex engineering control models, the majority have integrated various aspects of the theories described above. For example, some have expanded on the notion that there is active modulation of posture, suggesting that we use intermittent (Bottaro, Casadio, Morasso, & Sanguineti, 2005; Nomura, Oshikawa, Suzuki, Kiyono, & Morasso) or continuous feedback control (Kiemel, Zhang, & Jeka, 2011; Maurer & Peterka, 2005; Vette, Masani, Nakazawa, & Popovic, 2010). Others have applied various system identification approaches to the study of postural control, applying small perturbations or choosing certain parameters to investigate the input/output relationships used in the control of posture (van der Kooij et al., 2005). Interestingly, these and many other current theories of postural control reported in the  20  literature are based on the notion that posture is controlled in a reactive manner, where the goal is to stabilize or control movements of the body or COM.  1.6 Theories of postural sway  Although postural sway is experienced by all humans when standing quietly, the origin of sway is and has been a subject of debate for many years. Theories on the causes of postural sway can generally be lumped into a few categories that act in isolation or may be considered to act together and result in sway behaviour. These include suggestions that postural sway arises from (1) various internal and external forces that act on the body and displace the COM; (2) noise in the postural control system from a variety of sources; and (3) errors or delays in generating motor output that corrects or prevents movement of the COM.  One theory regarding why we sway during standing is that it results from internal perturbations, which act to displace the COM during stance. The majority of theories suggesting internal perturbations as the source of postural sway are based on frequencies of the perturbation, which are detected in spectral analyses of postural sway. One source of internal perturbation is respiration (Hunter and Kearney 1981; Jeong 1991; Hodges, Gurfinkel et al. 2002; Caron, Fontanari et al. 2004). When calculating the power spectra on measures of postural sway, Soames and Atha (1982) found that 72% of subjects had a peak frequency within a range of 0.30-0.45 Hz in the anterior-posterior direction, and 67% had this same peak frequency in the medial-lateral direction. This frequency corresponds to a breathing rate of 18-27 breaths per minute, therefore it was suggested that respiration is a significant component of postural sway. This was also confirmed in voluntarily paced 21  breathing efforts, where the frequency of voluntary breathing was reflected in the power spectrum of sway (Hunter and Kearney 1981). Finally, it was found that breath holding tends to reduce postural sway (Caron, Fontanari et al. 2004). This evidence was thought to provide further support for the theory that respiration underlies postural sway behaviour during stance.  Another source of internal perturbation that has been suggested to generate postural sway is the mechanical beating of the heart. Similar to the evidence for respiration, links between postural sway and heartbeats have been identified using spectral properties of postural sway measures. Soames and Atha (1982) also identified peak frequencies between 1.05-1.35 Hz in 34% of participants in the anterior-posterior direction, and 21% of participants in the medial-lateral direction. This range of frequencies is the same as heart rates between 63-81 beats per min. Therefore, through association, the authors suggested that this component of postural sway originated from the involuntary beating of the heart during stance. This suggestion is supported by Sturm et al. (1980), who reported that the distinct cardiac characteristics were observed in the vertical component of “microvibrations of the body.”  Involuntary muscle contractions during quiet standing have also been coupled to postural sway. Observations of muscle activity in the calf muscles during stance have suggested that the level of tonic activation during stance is very low. Periodic bursts of activity were observed; however, these bursts did not correspond at all to changes in ankle position. Rather, these bursts occurred randomly. As such, the authors suggested that the 22  bursting behaviour simply acted to “awaken” or influence the stretch mechanism (Soames and Atha 1981). Others have postulated that muscular contractions create a venous muscle pump to facilitate venous return from the lower extremities to the heart during quiet stance (Murray, Seireg et al. 1975). While little evidence has been provided, negative correlations have been observed between those with poor orthostatic tolerance and the magnitude of postural sway (Claydon & Hainsworth, 2005).  Theories on the contributions of internal perturbations to postural sway are largely based on the spectral properties of the COP signals recorded by the forceplate (and sometimes the COM). In the 70s and 80s there was a large movement away from characterizing postural sway in the time domain, to characterizing it in the frequency domain. The flood of research in this area was most likely based on the suggestion by Njiokiktjien and de Rijke (1972), who said that one of the most discriminating features separating “normals” and “pathologics” lay in their sway frequency patterns (Soames and Atha 1982). The limited impact of the work in this area is the result of data collection times that were too short. Short timescales used in these analyses do not allow for proper identification of the true frequencies of the COP during postural sway, where 90% is below 0.5 Hz (Carpenter, Frank et al. 2001).  Another theory regarding why we sway during stance is that it is the product of general noise in the postural control system. To my knowledge there is no empirical evidence indicating the sole sources of this noise, however some have suggested that it originates from intrinsic stochasticity (noisiness) of perceptual-motor processes (Slifkin & Newell, 1999), 23  and it has been implicated in many postural control studies, particularly in those that have tried to model the behaviour of the body during stance. For example, Ishida and Miyazaki (1987) in their maximum likelihood model of postural control suggested that measures of postural sway do not provide any insight into the mechanisms underlying postural control, since sway is simply the resultant sum of internal noise in the postural control system. Similarly, Morasso and Schieppati (1999) suggested that it is a combination of white noise and quasi-periodic spike noise, which keeps the body away from its natural equilibrium position.  Rather than general noise in the system, some theories have suggested that postural sway may result from errors or delays in the attempt to maintain the body in a perfectly balanced or equilibrium position. In these theories, it is assumed that movement of the body or COM away from equilibrium during stance requires active mechanisms to return the body back to vertical. Any errors in the magnitude of ankle torque, or delays in initiating these mechanisms, will result is continuous over and undershooting of the equilibrium position, which over time will result in continuous postural sway of the body (Horak and MacPherson 1996; Loram and Lakie 2002; Maurer and Peterka 2005).  The majority of theories described above assume that the goal of the CNS is to maintain an equilibrium position of the body or COM. However, the body is constantly exposed to various internal and external forces that constantly challenge this position. Any deviation from equilibrium is detected by the visual, vestibular and somatosensory systems, and in turn, corrective ground-reaction forces are generated to return the body to a vertical 24  position. Therefore, it is often assumed that the postural control system operates in a negative feedback manner where displacements of the COP control the COM, and errors or delays in this control lead to the development of sway. An alternative theory is that postural sway may function to gather and obtain sensory information during stance and function to explore the environment. Theoretically, if the body were to remain perfectly still in an equilibrium position, stimulation of the underlying sensory receptors would be limited or entirely absent. In contrast, with continuous motion of the body, there would be continuous receptor stimulation from a variety of sources, which could potentially provide a constant flow of sensory information to the CNS.  There is a limited amount of empirical evidence supporting an exploratory role of postural sway that functions to gather or obtain sensory information during stance. However, this theory regarding the behaviour of the body during stance has been proposed frequently in the field of ecological psychology (Gibson, 1962; Riccio, 1993; Riley et al., 1997; Riley & Turvey, 2002; Stoffregen & Riccio, 1988). Additional support for this theory may exist if we change the conceptual framework through which we describe our results. For example, postural sway is smallest when sensory information from the three sources of sensory information is available (Fitzpatrick, Taylor et al. 1992). When afferent input from one or more sensory systems is removed or distorted, the magnitude of postural sway increases (Nashner 1985; Simoneau 1995; Horak and MacPherson 1996), and this increase is thought to be indicative of a loss of control by the postural system. Similarly, with ageing and neurological disease, increases in postural sway are also observed, and are thought to be indicative of a failing postural control system. However, it could be argued that when one or 25  more sources of sensory information are removed, the changes in the magnitude and structure of postural sway may be functional (Riley & Clark, 2003) and act to maintain a critical level of incoming sensory information from the remaining sensory systems.  Another way in which the postural control system could acquire additional sensory information is from other sources of sensory information that are typically not used in the maintenance of upright stance. Jeka and Lackner (1994) supported this theory in a study where participants stood with their eyes closed, in a difficult position (tandem stance), while lightly touching (<1N) a bar which was not able to provide mechanical support. In this condition, postural sway was significantly reduced. Applied fingertip forces also preceded postural sway, suggesting that sensory information from the fingertip provided information regarding the position of the body. In this study, it could be interpreted that decreases in postural sway resulted from an increase in proprioceptive information supplied by cutaneous receptors in the fingertip, and that this sensory information decreased the need for proprioceptive information arising from beneath the feet.  The view that movement or variability is necessary to stimulate sensory receptors and acquire a certain quantity and quality of sensory information is abundant in literature pertaining to other systems. In the human visual system, with voluntary fixation of the eye, we can observe small, involuntary movements known as microsaccades (Engbert and Kliegl 2004; Martinez-Conde, Macknik et al. 2006). Without these small movements we would lose perception and the image projecting onto the retina would disappear. Similarly in the olfactory system, a sniff is accurately and rapidly modulated with sensory content. Therefore, 26  as the concentration of an odorant is reduced, sniffing increases to accommodate olfaction (Sobel, Thomason et al. 2001; Johnson, Mainland et al. 2003). A final example is the act of “whisking” in rats. The rat uses its whiskers to acquire tactile sensory information by sweeping them in a coordinated, rhythmic fashion, and these movements can be modulated in amplitude and frequency. These examples support Berg and Kleinfeld (2003), who stated that “most processes of sensation involve the active repositioning of the underlying sensors. Therefore, an understanding of sensation involves the need to decode the motor control of the sensory organs as well as the sensory input per se.” Collectively, the behaviours in these systems require a dynamic (as opposed to static/tonic) input to facilitate the delivery of afferent information. If adequate afferent information is not received, the system must modify behaviours (i.e. by increasing saccades or sniffing frequency) to ensure dynamic afferent input is maintained.  1.7 Conclusion  In summary, although standing seems to be a very simplistic task, it is actually a very complex motor behaviour. Afferent information supplied by the visual, vestibular, and somatosensory systems provides critical information on the gravitational orientation of the body, while neuromuscular control mechanisms activate muscles very precisely to remain in an upright position. However, we are never able to maintain a perfect balanced position of the body in space. We are constantly moving, and even if we try to stand still, we cannot prevent the small oscillations of the body known as postural sway. This behaviour of the body during stance has traditionally been viewed as noise or error in the postural control system, and is generally associated with performance decrements and pathology. However, 27  there is some evidence to suggest that movement observed during postural control and in a variety of other motor behaviours may be exploratory and serve as a means of acquiring a certain quantity and quality of sensory information. The studies completed in the following 5 chapters experimentally tested how postural sway is controlled and/or used by the CNS.  28  2 Chapter: Shifting the balance: Evidence of an exploratory role of postural sway1 2.1 Introduction  Postural sway, the seemingly random oscillation of a body during stance, is a common characteristic among bipedal and quadrupedal species, including humans, dogs, cats, and horses (Brookhart, Parmeggiani, Petersen, & Stone, 1965; Clayton, Bialski, Lanovaz, & Mullineaux, 2003; Thomson, Inglis, Schor, & Macpherson, 1991; Winter et al., 1998). Postural sway is observable primarily during periods of quiet stance and persists despite concentrated efforts to minimize such movement (Vuillerme & Nafati, 2007). However, the exact cause or purpose of postural sway is currently unknown. Balance is maintained during stance if the gravitational line through the body’s centre of mass (COM) stays within the base of support. Human balance is typically modeled as an inverted pendulum, where the body is controlled as a single rigid segment, supporting a single point mass (i.e. the COM), which rotates about the ankle joint (Winter, Patla et al. 1998). The inverted pendulum is controlled through the development of ground-reaction forces which can be recorded using a forceplate. The vector sum of all of the ground-reaction forces under the feet is called the centre of pressure (COP), which is comprised of two different components: (1) the gravitational projection of the COM; and (2) torques generated at the ankle joint (dorsi-flexion/plantar-flexion) in the anterior–posterior (AP) plane and the hip joint (abduction/adduction) in the medial–lateral (ML) plane(Winter et al., 1996). As a result,  1  The following chapter has been published in Neuroscience, An International Journal under the editorial  direction of the International Brain Research Organization. 29  displacements of the COM and COP can be viewed as a game of cat and mouse where the movements of one are chased or tracked by movements of the other. The majority of currently-held theories assume that the goal of the central nervous system (CNS) is to maintain equilibrium of the COM around a set-point; a goal which is under constant challenge by continuous perturbations to the COM caused by factors such as breathing, heartrate, and muscle activity(Jeong, 1991; Soames & Atha, 1981; Soames & Atha, 1982). Thus, the COP is considered to be constantly reacting to the estimated position of the COM, via feedback from multiple sources of sensory information(Ishida & Miyazaki, 1987; Johansson, Magnusson, & Akesson, 1988; Peterka, 2000), and the residual sway that persists is due, in part, to inherent delays or errors within the feedback control system. Assuming that such theories are correct, and balance is controlled using corrective ground reaction forces (COP) to minimize movement of the COM, we hypothesized that an artificial stabilization of the COM would lead to a decrease in the displacements of the COP. To test this hypothesis, we have devised a unique apparatus (Figure 2-1A) to minimize or “lock” movements of the COM in the sagittal plane and compare the resultant changes in COP displacements during the Locked and Unlocked conditions. The unique aspect of this apparatus is that COM can be locked and unlocked without the subject being aware that sway in the sagittal plane has been artificially minimized. Since COM displacements in the sagittal and frontal planes are known to be controlled by the CNS independently (Winter et al., 1996), we further hypothesized that any changes in COP displacements due to locking the COM would be restricted to the sagittal plane. Subjects performed the experiment with their eyes open or closed, to test the hypothesis that the effects of locking the COM on COP displacements would be independent of vision. 30  2.2 Experimental procedures  2.2.1  Participants  47 healthy young adults volunteered to participate in the study and were randomly assigned to one of three groups: the Eyes Open group (19 subjects (7 males, 12 females); mean±sd for age=24.5±2.8 years; height=170.9±8.2 cm; weight=66.1±9.9 kg), the Eyes Closed group (18 subjects (6 males, 12 females); age=25.1±3.8 years; height=172.6±11.7 cm; weight=70.1±11.9 kg) and the Control group (10 subjects (3 males, 7 females), age=21.3±2.7 years; height=167.8±7.4 cm; weight=60.7±6.7 kg). Each participant provided informed written consent, and the experimental protocol was approved by the Behavioural Research Ethics Board at The University of British Columbia. All subjects were completely naive to the goals of the experiment and the intended effect of the apparatus on postural sway.  2.2.2  Apparatus  In all conditions (except the Control condition-see section Experiment 2 under Experimental protocol) subjects were firmly braced with their back against a rigid board with adjustable straps tightened firmly around the head, both shoulders, chest, waist, hips, and lower legs. The board was used to ensure that sway was controlled as an inverted pendulum by allowing sway in the sagittal plane to occur only about the ankle joints. The board was 1.66 m high (including head rest) Χ 0.61 m wide and had a total mass of 12.5 kg. Despite the 31  added mass, the average total body mass (including the mass of the board) for all subjects was 78.1 kg, which is still within a normal range for subjects of this age and height. The board (not the person) was attached to a closed-loop pulley system that allowed the subject to stand and experience “normal postural sway” about the ankle joint unless the experimenter applied a brake, which would discretely lock the board (and thus COM) in place in the sagittal plane without the subject’s knowledge (Figure 2-1A). To eliminate any chance that the participant could receive auditory cues to indicate that they had been locked, all participants wore headphones that reduced any noise within the testing area. Subjects also wore blinders that occluded both horizontal and vertical peripheral vision to eliminate any visual cues from the apparatus. In all conditions, subjects stood with their arms crossed and feet shoulder width apart on a forceplate (#K00407, Bertec, USA).  2.2.3  Experimental protocol  Experiment 1. All subjects were fitted into the apparatus and instructed to stand as still as possible, for a total of ~5–6 minutes of upright stance. The first 30 seconds (s) of stance was used to allow the transient component of sway to stabilize (Carroll and Freedman 1993). As shown in Figure 2-1B, the next 30 s of quiet stance was used to calculate the mean AP-COP position used to establish the threshold for “locking”. Immediately after, subjects stood for ~75 s with the apparatus unlocked allowing for normal sway movement (“Unlocked-1” condition). After the Unlocked-1 condition, the apparatus was locked in place (without the subjects’ knowledge) when the COP was within 2 standard deviations of the calculated mean COP and maintained during a further stance period of ~75 s (“Locked” 32  condition). The Locked condition was then followed by a second Unlocked condition in which the brake was released and the subject/apparatus was again free to move, for a subsequent ~75 s of stance (“Unlocked-2” condition). Subjects in the Eyes Open group performed each standing trial with their eyes open and gaze focused on a target placed at eye level ~6 m in front of them. Subjects in the Eyes Closed group were instructed at the beginning of each standing trial to close their eyes and keep them closed over the duration of the standing trial.  Experiment 2. To examine the potential effects of the apparatus itself on postural sway, the Control group performed an initial standing trial (“Control”), in which they were instructed to stand as still as possible for 120 s on the forceplate (arms crossed, feet shoulder width apart, eyes open while wearing the blinders) without any contact with the apparatus. They were then placed into the apparatus and asked to undergo the same procedures as the Eyes Open group in Experiment 1, (see the above section, with the exception of the Unlocked-2 condition).  2.2.4  Measurements  Experiment 1. Ground reaction forces and moments were sampled at 100 Hz and low-pass filtered offline using a 5 Hz dual-pass Butterworth filter before calculating COP in the AP and ML directions. Prior to calculating summary measures, linear trends in the AP and ML COP signals were removed to eliminate any effects of bias on measures of variability. From these unbiased signals, two summary measures were recorded to characterize different aspects of postural sway. Mean position and Root Mean Square (RMS) 33  amplitude of COP displacements (“COP RMS”) were calculated in the AP and ML directions over a 60 s period within each condition. For the Unlocked-1 and Locked conditions the 60 s measurement period began 75 s prior to the beginning, and end, of the braking period respectively. For the Unlocked-2 condition the 60 s measurement period began 15 s after the brake was released (see Figure 2-1B). Kinematics were sampled at 100 Hz for the duration of each trial using an Optotrak three dimensional optical motion analysis system (Northern Digital Inc., Waterloo, Ontario, Canada) with infrared light emitting diodes placed on the cable, ankle joint and the back of the board at a level that approximated the height of the COM. Kinematic data were filtered at 5 Hz with a dual-pass Butterworth filter and used to calculate the range of the angular displacement of the COM in the sagittal plane (AP-COM Range) for each 60 s measurement period.  Experiment 2. In addition to the COP and COM measures described for Experiment 1 (see the above section), subjects in the Control group had electromyographic (EMG) activity recorded from gastrocnemius, soleus and tibialis anterior muscles of the right leg, using surface electrodes (Telemyo 2400R G2, Noraxon, USA) collected with a sampling rate of 1000 Hz, band-pass filtered between 10 and 500 Hz, and used to calculate RMS amplitudes over three 60 s measurement periods from the Control, Unlocked-1, and Locked conditions as a measure of tonic muscle activation. Control subjects also had additional infrared light emitting diodes placed on the fifth metatarsal and heel to allow for the calculation of the mean ankle torque using the following procedure. We combined synchronous measures of force and motion to estimate the time-varying ankle torque as: TA(t)= Fz(t)x(t)-Fx(t)z(t)Wfxf(t), where FZ is the resultant vertical force acting on the foot (defined positive if upward), 34  x is the horizontal distance in the sagittal plane from the COP to the ankle joint (defined positive if anterior to the ankle), FX is the resultant horizontal force in the sagittal plane acting on the foot (defined positive if directed posteriorly), z is the vertical height of the ankle joint above the ground, Wf is the weight of the foot (estimated as 0.0145Χbody weight (Winter 2004), and xf is the horizontal distance from the ankle joint to the centre-of-mass of the foot (Winter 2004). From these measures, the mean ankle torque was calculated for each subject during the Control and Unlocked-1 condition.  2.2.5  Statistical analysis  In Experiment 1, AP- and ML-COP RMS and AP-COM Range were analyzed using a 3Χ2 within and between subject analysis of variance (ANOVA) with condition (Unlocked-1, Locked, Unlocked-2) as the within subject variable and vision (Eyes open, Eyes closed) as the between subjects variable. In cases where Mauchly’s test of sphericity was significant, degrees of freedom were corrected using Greenhouse–Geisser estimates of sphericity. Post-hoc analysis of significant condition effects were performed using paired t-tests. Preplanned comparisons for dependent measures in Experiment 2 were analyzed using paired ttests. In all cases, alpha level was set at 0.05.  35  2.3 Results  2.3.1  Experiment 1  As shown in Figure 2-1B, the apparatus was highly effective in accomplishing the goal of stabilizing the COM in the sagittal plane during the Locked compared to Unlocked-1 condition. AP-COM Range was influenced by a significant main effect of condition (F(1.62,56.74)=60.56, P<0.001, η2=0.634). As shown in Figure 2-2A, there was a significant decrease in AP-COM Range in the Locked, compared to the Unlocked-1 (P=0.001) and Unlocked-2 (P=0.001) conditions. Significantly higher AP-COM Range was observed in the Unlocked-2 compared to Unlocked-1 condition (P=0.004). Post-test questionnaires confirmed that all participants were unaware of any manipulation of the COM displacement during the entire experiment. The results of stabilizing the COM had the opposite effect on the COP than originally hypothesized. As shown in Figure 2-1B, the COP amplitude of a representative subject drastically increased in amplitude during the Locked compared to the Unlocked conditions. As shown in Figure 2-3, most subjects demonstrated the same pattern of larger amplitude AP-COP displacements in the Locked compared to Unlocked-1 condition. Individually, 14 of the 19 subjects in the Eyes Open group and 11 out of 18 subjects in the Eyes Closed group were found to have larger AP-COP RMS values measured in the Locked compared to Unlocked-1 condition. These individual observations were confirmed statistically with a significant main effect of condition found for AP-COP RMS (F(1.12,39.06)=7.45, P=0.008, η2=0.176). As shown in Figure 2-2A, there was a significant increase in AP-COP RMS amplitude during the Locked compared to the Unlocked-1 36  (P=0.002) and Unlocked-2 condition (P=0.04). The Unlocked-2 condition had significantly larger AP-COP RMS compared to the Unlocked-1 condition (P=0.002). While the largest magnitude of COP changes within the Locked condition were found in the AP direction (see Figure 2-2B) there was a small, but significant, main effect of condition also found for MLCOP RMS (F(1.29,45.05)=4.05, P=0.041, η2=0.104). Post-hoc tests revealed significantly larger ML-COP RMS in the Locked (0.675±0.075 mm) compared to Unlocked-1 (0.546±0.034 mm) condition (P=0.046), and Unlocked-2 (0.667±0.038 mm) compared to Unlocked-1 conditions (P<0.001). There were no significant main effects of vision, or visionΧcondition interactions observed for any COP or COM measures (all P’s<0.05).  2.3.2  Experiment 2  Data from the Control group confirmed that the apparatus itself had an influence on postural sway. There was a significant decrease in AP-COP RMS amplitude (t(9)=4.88, P=0.001) when standing in the Unlocked-1 condition compared to the Control condition (0.981±0.217 mm vs. 3.03±0.391 mm, respectively). However, because the weight of the board is distributed along the entire length of the body, and fixed to the subject using straps at seven different locations, we would argue that the change in AP-COP RMS is not likely due to a change in the position of the COM, but rather the increased mass (and inertia) of the body (Loram, Gawthrop et al. 2006; Blaszczyk, Cieslinska-Swider et al. 2009). This argument was supported by the lack of significant differences observed between Control and Unlocked-1 conditions for mean ankle torque (t(9)=0.053, P=0.959), and tonic muscle activity in tibialis anterior (t(9)=1.552, P=0.155), soleus (t(9)=1.136, P=0.285) and 37  gastrocnemius (t(9)=0.717, P=0.492), that would otherwise be expected if the mean COM location was shifted due to the board. The ML-COP RMS was also significantly reduced (t(9)=4.43, P=0.002) when standing in the Unlocked-1 condition (0.391±0.036 mm) compared to the Control condition (0.991±0.127 mm), although this reduction is likely due to the board’s restriction of movements around the hip joint (with straps around the waist, pelvis, and legs) as much as adding mass (inertia) to the body.  Control data also confirmed that in the Locked condition, subjects continued to maintain their normal posture, and support themselves in the vertical direction (i.e. against gravity), despite having their COM stabilized in the horizontal direction by the apparatus. For example, there was no difference between the Locked and Unlocked-1 condition observed in the vertical ground reaction force (averaged 729.41±22.4 vs. 729.38±22.4 N, respectively; P=0.944), or tonic EMG measured from tibialis anterior (0.014±0.008 vs. 0.007±0.000 mV; P=0.335), gastrocnemius (0.015±0.003 vs. 0.015±0.003 mV; P=0.953), or soleus (0.014±0.003 vs. 0.015±0.004 mV, P=0.873) muscles.  2.4 Discussion  The common element within the majority of traditional theories on the mechanisms of postural sway is the assumption that the COM is unstable, and the COP is used as a means to control, or to correct for, deviations in the COM from a desired position or point of equilibrium (Ishida and Miyazaki 1987; Johansson, Magnusson et al. 1988; Peterka 2000). In the current experiment, the displacement of the COM was largely reduced in the sagittal 38  plane in the Locked condition. Therefore, based on traditional theories we hypothesized that the amplitude of AP-COP displacements should also dramatically decrease when AP movements of the COM are artificially minimized. However, in the majority of participants, we observed a significant increase in the amplitude of AP-COP displacement when AP movements of the COM were minimized. Stabilizing the COM in the AP direction also increased ML-COP displacements, although to a far lesser degree than increases observed in AP-COP. These results firmly reject our primary hypotheses, and provide support for a possible exploratory role of postural sway. Other studies investigating the role of postural sway have postulated that sway variability may reflect the characteristics of an exploratory behaviour (Riccio 1993; Riley, Mitra et al. 1997; van Emmerik and van Wegen 2002; van Wegen, van Emmerik et al. 2002; Mochizuki, Duarte et al. 2006). In this regard, postural sway is not viewed as error or noise in the postural control system, but rather, as part of a perceptual-action strategy that allows an animal to gain essential information about its interaction with the environment (Riccio 1993). This information may be essential to track the position of the body relative to its limits of stability (Riley, Wong et al. 1997; van Wegen, van Emmerik et al. 2002). Alternatively, the information gained through exploratory behaviour may ensure that there is a certain quality and volume of sensory information received by the CNS. From a neurophysiological standpoint, it is reasonable to assume that the CNS would encourage movement variability even during static posture tasks. First, movement variability will ensure a greater variety of sensory receptors are stimulated, since all sensory receptors respond to dynamic change (at least to some degree), yet not all respond to static states (i.e. rapidly-adapting receptors) (Johansson and Vallbo 1983; Gandevia 1996). Second, due to the limited receptive and/or operating ranges of individual receptors, 39  movement variability ensures a greater number of receptors within a population will be stimulated, thereby increasing the ensemble code (Cordo, Flores-Vieira et al. 2002; Kennedy and Inglis 2002). Third, movement variability will ensure converging information is provided by multiple sensory systems to allow for reliable integration (Horak and MacPherson 1996).  In this regard, we feel that the exploratory hypothesis provides a unique perspective to understand why the removal or degradation of sensory information leads to an increase in postural sway during quiet stance. For example, sway increases when the eyes are closed (Teasdale, Stelmach et al. 1991), when proprioceptive inputs are altered through cooling (Asai, Fujiwara et al. 1992), or ischemic block (Mauritz and Dietz 1980), and when vestibular inputs are made unreliable through head-tilting (Brandt, Buchele et al. 1996). Traditional theories would argue that sway amplitude increases in such conditions because there is insufficient sensory information available to accurately and rapidly detect the errors in the estimated COM position to provide optimal control through adjustments of COP. However, based on the exploratory hypothesis, it could be argued that the COP displacement is increased purposefully by the CNS in order to ensure a certain quality or quantity of sensory information is received by the CNS from the remaining intact sensory systems. Only the latter hypothesis is supported by our observations that COP increases when COM movement is minimized.  Evidence for an exploratory role of motor variability can also be found from other types of motor control tasks. For example, Burgess (1989) observed force fluctuations in the hands of subjects trying to stabilize a load in a static position in a low friction environment. 40  However, when the friction was unexpectedly increased to the point that any movement cues were eliminated, the force generated by the hand was observed to “wander” and increased in amplitude to levels that would have translated into excessive movements if the friction had been lower. Likewise, microsaccades observed during static positioning of the eye, have also been proposed as a method to generate sensory feedback, since stabilizing the eye in a fixed position leads to peripheral blindness (Martinez-Conde, Macknik et al. 2006). Evidence of micro-slips or micro-exploration during purposeful hand-movements have also been described as a possible means of the CNS to derive sensory information during a manual reaching task (Sasaki, Mishima et al. 1995).  In addition to increasing sensory information, increased variability during static positioning tasks could also have other positive effects on motor performance. For example, Goodman and Kelso (1983), have provided clear evidence that physiological tremor can be incorporated into the generation of a voluntary task; results of their experiment demonstrated that the initiation of a reactive or self-initiated finger movement coincided with the point of maximum momentum induced by the physiological tremor in the direction of the intended movement.  While we feel that our results provide strong evidence in support of an exploratory role of postural sway, we recognize that there are a number of alternate explanations that warrant consideration. The first is that our observations in Locked compared to Unlocked conditions may be attributed to sensory illusions. For example, there is the possibility that the sensation of a change in force between the board and the body during the Locked condition, 41  may provide the subjects with the illusion that they are being pushed or pulled, and thus elicit reactive COP responses. However, our participants were tightly strapped into the board with seven different straps around the body, and previous studies using a similar apparatus have argued that there would be minimal pressure changes on the trunk for such small disturbances due to the large surface area of the back and long lever arm of the rigid board when compared with the size and length of the feet (Fitzpatrick, Taylor et al. 1992). Furthermore, if the results were due to an illusion effect, we would expect that the illusionary effects would be enhanced by the removal of visual information, as found in most other studies involving proprioceptive illusions (Eklund 1973; Lackner and Taublieb 1984). However, no significant interactions between vision and locking conditions were observed for any variable, confirming that the effects of locking the COM on COP RMS amplitude were independent of any effects of vision, and therefore unlikely to be attributable to an illusionary effect. Alternatively, it could be argued that locking the COM may create a sensory-deprivation state, in which the COP may drift in a similar fashion to the motor drift observed in static hold tasks performed by patients with total proprioceptive loss (Rothwell, Traub et al. 1982). However, this explanation does not apply to our results, as the mean range of COM angular displacement observed in the Locked condition falls within the perceptual sensory thresholds for stance estimated by Fitzpatrick and McCloskey (1994). In fact, six of the seven subjects that had COM angular ranges during the Locked condition that exceeded even the upper bounds of known perceptual thresholds for stance (0.12 degrees), also had increased COP RMS amplitude during the Locked compared to Unlocked-1 condition. Finally, it could be argued that at least some of the COP variation observed during the Locked condition could be attributed to uncontrolled fluctuations of motor output from leg 42  muscles (De Luca, LeFever et al. 1982), although it seems unlikely that this would account for the current observations of increased COP amplitudes that far exceed those recorded during normal postural sway.  While the majority of subjects, individually, and as a group, on average, showed increases in AP-COP RMS in the Locked compared to the Unlocked-1 condition, there were some subjects (12 out of 37 in both the Eyes open and Eyes closed groups) that did not follow this same pattern of change. While explanations for such individual differences are beyond the scope of the current paper, it is extremely important to highlight that even in these subjects that showed decreases in the AP-COP RMS in the Locked compared to the Unlocked-1 condition, the magnitude of the AP-COP RMS change (36% decrease on average) was by no means congruent with the reduction in the AP-COM Range (94% decrease on average). Therefore, we would argue that in all cases, the changes in AP-COP observed during the Locked condition (whether increased or decreased to a far lesser extent than that of the AP-COM) provides evidence that postural sway, or at least some proportion thereof, may be exploratory in nature.  There are a number of possible explanations for the larger amplitudes of COP and COM displacement observed in the Unlocked-2 compared to Unlocked-1 condition. For example, the changes may reflect fatigue that developed from standing within the apparatus for an extended period of time (Vuillerme and Nafati 2007). However, even if this were the case, its effect will have little bearing on the changes observed in the Locked condition, which preceded, and yet, still elicited significantly larger AP-COP RMS amplitudes than the 43  Unlocked-2 condition. Alternatively, the larger amplitudes of AP-COP and COM observed in Unlocked-2, could reflect a persistence of exploratory behaviour that carried over from the preceding Locked condition. However, the simplest, and therefore most likely, explanation is that the release of the brake caused an unexpected postural disturbance, and as a consequence, increased postural sway during the Unlocked-2 condition. The acceleration of the COM is known to be negatively correlated to the difference in COP–COM (Winter et al., 1998). Therefore, at the time the brake was released at the end of the Locked condition, any difference in instantaneous AP-COP position (which is undergoing larger displacements when locked) and AP-COM position (which is minimized when locked) will induce an unexpected acceleration of the COM, and resulting period of instability until equilibrium is re-established. Although there was a 15 s delay between the release of the brake and start of the Unlocked-2 measurement period, this may still have been an insufficient amount of time for sway characteristics to return to normal levels. Therefore, future studies will need to ensure that differences in the COP and COM position are minimized prior to releasing the brake at the end of the Locked period, if the potential carry-over effects of exploratory behaviour are to be further investigated.  The exploratory hypothesis of postural sway has the potential to shift current beliefs about balance in humans and animals and could be used to directly challenge the basis of current clinical practices for treating balance deficits associated with age and disease. For example, increased postural sway observed in older adults (Overstall, Exton-Smith et al. 1977; Colledge, Cantley et al. 1994) is commonly attributed to increased thresholds of peripheral sensory receptors, as well as brain functions responsible for integrating and 44  processing this sensory information (Goble, Coxon et al. 2009), and interpreted as a negative outcome of the unreliable or delayed sensory feedback within the postural control system which leads to further instability (Isaacs 1978). However, if, as our results suggest, postural sway is controlled by the CNS to generate a certain quality or volume of sensory information, then it could be argued that increased postural sway in older adults may represent a natural correction of the CNS to account for the age-related increases in sensory thresholds or reduced integration capacity. In such cases, increased postural sway may be viewed as a positive adaptation to age-related decline which is generated to ensure that the input to the peripheral sensory receptors exceeds the thresholds for detection and enhance the sensory information available to the CNS (Patla, Frank et al. 1990). If this is the case, treatments designed to reduce postural sway may, in fact, oppose the natural adaptations made by the CNS. Therefore, it may be necessary to reconsider the theoretical basis behind current rehabilitation strategies for dealing with balance control deficits due to age, or disease (van Emmerik and van Wegen 2002).  45  Figure 2-1  Illustration of apparatus and experimental procedures: (A) sagittal and transverse views of the apparatus used to minimize or “lock” AP movements of the COM without the subject’s awareness; (B) raw traces of the AP-COM angular displacement (top trace) and AP-COP displacements (bottom trace) from a representative subject in the Eyes Open group. Dashed vertical lines indicate the boundaries between quiet standing (QSwhich was used to calculate the threshold for locking), Unlocked-1, Locked, and Unlocked-2 conditions. Grey boxes indicate the 60 s time periods used for data analysis. Zero on the y-axis represents the mean COP and COM position calculated during the initial 30 s quiet stance period.  46  Figure 2-2  (A) Group means and standard error bars illustrate the significant main effects of condition (pooled across vision) for AP-COM Range (left panel) and AP-COP RMS (right panel); (B) x-y plots of AP and ML COP displacements from a representative subject in the Eyes Open group during the Unlocked-1, Locked and Unlocked-2 conditions. Zero represents the mean COP position calculated during the initial 30 s quiet stance period and positive values indicate displacements in the forward and rightward directions.  47  Figure 2-3  Individual AP-COP displacements recorded during the Unlocked-1 condition (grey lines) and Locked condition (black lines) plotted together for each of the 19 subjects in the Eyes Open group. 48  3 Chapter: Exploratory behaviour during stance persists with visual feedback2 3.1 Introduction  Postural sway is experienced by all humans when standing quietly, however, the origins of postural sway are unknown. The continuous and random nature of postural sway is commonly thought to result from the interplay between movements of the body or centre of mass (COM), and ground-reaction forces acting beneath the feet (centre of pressure (COP)), where the COP controls, or corrects for, deviations of the COM from a desired position or point of equilibrium. Therefore, it is assumed that errors or delays in this control system lead to continuous movement or sway of the body during stance. From this perspective, increases in the amplitude of postural sway are commonly considered to be indicative of poor postural control.  However, recent evidence has begun to challenge the view that postural sway is a consequence of an unstable balance system or errors in feedback control. By using a novel method to minimize or “lock” COM displacements in the anterior-posterior plane during stance without subject awareness, we have demonstrated that COP amplitude increased compared to when the COM swayed freely (Carpenter, Murnaghan, & Inglis, 2010). Since locking stabilized movements of the COM, the increase in COP amplitude could not be attributed to increases in movement of the COM. Therefore, it was interpreted that COP  2  The following chapter has been published in Neuroscience, An International Journal under the editorial  direction of the International Brain Research Organization. 49  displacements may be actively driven by the central nervous system (CNS), potentially as an exploratory means to acquire sensory information.  While the conclusions of Carpenter et al. (2010) were consistent with other evidence of exploratory behaviour (Burgess 1989; Sasaki, Mishima et al. 1995; Martinez-Conde, Macknik et al. 2006), at least two potential alternative hypotheses had to be acknowledged. The first hypothesis was that sensory illusions may have emerged during locking, consequently eliciting reactive COP displacements. Such illusions may have arisen from a mismatch between the actual displacement of the body, and afferent feedback from cutaneous and/or musculo-tendinous force feedback receptors. However, in Carpenter et al. (2010) we argued that the effects of sensory illusions would be amplified when vision was removed (Eklund 1973; Lackner and Taublieb 1984); yet we observed that increases in COP displacement during locking were comparable when vision was available or removed. A second alternative hypothesis was that increases in COP amplitude were the result of a drift in motor output; a phenomenon thought to result from a deprivation of sensory information, and most often observed in individuals with total proprioceptive loss during static hold tasks (Rothwell, Traub et al. 1982). While our manipulation significantly reduced COM displacement during locking, participants were not likely in a sensory deprived state since body displacements still exceeded known perceptual thresholds for stance (Fitzpatrick and McCloskey 1994). However, despite these arguments, we were unable to conclusively rule out these alternative hypotheses without more direct evidence.  50  Therefore, the aim of the current study was to try and replicate our previous results and determine whether the effects of COM stabilization on COP displacements can be attributed to sensory illusions or motor drift. During the experiment, we asked participants to stand as still as possible in an apparatus that allowed movements of the COM to be minimized or “locked” in the sagittal plane without subject awareness (Carpenter, Murnaghan et al. 2010). The potential role of sensory illusions and motor drift was investigated by providing subjects with real-time visual feedback of the COM or COP, throughout the trial. If there was an influence of sensory illusions, we hypothesized that the change in COP displacements from Unlocked to Locked would be significantly reduced when participants were provided definitive visual confirmation that the COM had been stabilized. If there was an influence of motor drift, we hypothesized that the change in COP displacement from Unlocked to Locked would be significantly reduced when participants were provided visual feedback of the COP and thus were aware of, and able to confirm, its position throughout the trial.  3.2 Methods 3.2.1  Participants  Sixteen healthy young adults (8 females; mean ± sd for age = 22.9 ± 3.9 years; height = 174.3 ± 9.7 cm; weight = 67.0 ± 9.8 kg) volunteered in the study. Each participant provided informed written consent, and the experimental protocol was approved by the Behavioural Research Ethics board at the University of British Columbia. All subjects were completely  51  naïve to the goals of the experiment and the intended effect of the apparatus on postural sway.  3.2.2  Apparatus  During all experimental trials, participants were firmly braced with their back against a rigid board with adjustable straps tightened firmly around the head, shoulders, chest, waist, hips/upper thighs, and upper shank, to prevent movement at any joint except the ankle. The board was 1.66 m high (including head rest) x 0.61 m wide and had total mass of 12.5 kg. The board was attached to a closed-loop pulley system that allowed ‘normal postural sway’ at the ankle joint unless the experimenter applied a brake that would discretely lock the board (and thus COM) in place in the sagittal plane without participants’ knowledge (Figure 2-1A). To eliminate any chance that the participant could receive auditory cues to indicate that they had been locked, all participants wore headphones that reduced any noise within the testing area. Participants also wore blinders designed to occlude both horizontal and vertical peripheral vision. In all conditions, subjects stood with their arms crossed and feet shoulder width apart on a forceplate (#K00407, Bertec, USA).  3.2.3 Experimental protocol  All subjects were fitted into the apparatus and asked to stand as still as possible in four trials. First, participants performed a two-minute trial where they were asked to stand as still as possible and to focus on a target located at eye-level two meters in front of them (CONTROL). This trial was used to calculate the mean and peak-to-peak amplitude of 52  anterior-posterior (AP) COP and COM displacements. Three additional feedback trials, each with a minimum duration of 3.5 minutes, were randomized and varied in the type of feedback participants received. In one trial, participants received instructions identical to those in the CONTROL trial (no feedback condition - NOFB). In the remaining two trials, participants received real-time COP (COP feedback condition – COPFB), or real-time COM (COM feedback condition – COMFB) feedback on a screen located at eye-level two meters in front of them. The COP visual feedback was smoothed using a low pass digital filter with a time constant of 0.2s to ensure that participants did not respond to very high frequency components within the signal. After being familiarized with how to control their COP (or COM), participants were asked to maintain their COP (or COM) between boundaries positioned at their mean ± 1 peak-to-peak amplitude of COP (or COM) displacement recorded during the CONTROL trial. In all feedback conditions (NOFB, COPFB and COMFB), the first 30s of each trial was used to allow the transient component of sway to stabilize (Carroll & Freedman, 1993), and the following 30s was used to calculate the mean COP position to be used as the threshold for “locking.” Following the initial 60s, participants stood freely in the “Unlocked” condition for a minimum of 75s (Unlocked) and then the board was locked when the COP was within 2 standard deviations of the calculated mean COP, for a further minimum 75s (Locked).  3.2.5  Measurements  Ground reaction forces and moments were sampled at 100 Hz and low-pass filtered offline using a 5 Hz dual-pass Butterworth filter before calculating COP in the anterior– posterior (AP) direction. From these signals, the Root Mean Square (COP RMS) of the AP 53  COP displacements was calculated. Kinematics were sampled at 100 Hz for the duration of each trial using an Optotrak three dimensional optical motion analysis system (Northern Digital Inc., Waterloo, Ontario, Canada) with infrared light emitting diodes (IRED) placed on the cable, ankle joint, and back of the board at a level that approximated the height of the COM. Kinematic data were filtered at 5 Hz with a dual-pass Butterworth filter and used to calculate the angular displacements of the COM in the sagittal plane. From this signal, the range and RMS of AP COM angular displacements (COM RMS) were calculated. All dependent variables were calculated for each trial over a 60s period when participants were Unlocked and Locked. The 60s measurement periods began 75s prior to the beginning, and end, of the braking period respectively.  3.2.6  Statistical analysis  To ensure the effectiveness of the apparatus was consistent across conditions, we used one-way repeated measures ANOVA. To test the influence of sensory illusions (hypothesis 1), we compared the change in COP RMS from Unlocked to Locked across NOFB and COMFB conditions using a paired t-test. To test the influence of motor drift (hypothesis 2), we compared the change in COP RMS from Unlocked to Locked across NOFB and COPFB conditions using a paired t-test. In both cases, alpha level was set at 0.05.  3.3 Results  The apparatus was effective in minimizing movement of the COM during locking in all 3 feedback conditions (Figures 3-1 and 3-2, upper panels). When participants were 54  locked, there was no significant difference in the RMS amplitude of cable displacements between the NOFB (0.05 ± 0.01 mm), COPFB (0.07 ± 0.01 mm) and COMFB (0.06 ± 0.01 mm) condition. Across all three conditions, locking the cable was related to an average RMS and range of COM angular displacements of 0.02 ± 0.00 deg and 0.09 ± 0.02 deg respectively.  In the NOFB condition, 9 of 16 participants had the same or larger COP RMS during the Locked compared to Unlocked condition (Figures 3-1 and 3-2, bottom panels), with average COP RMS amplitude of 3.37 ± 0.65 mm and 2.47 ± 0.35 in the Locked and Unlocked condition, respectively. In contrast, with COM feedback available, 13 of 16 participants had larger COP RMS during the Locked compared to Unlocked condition (figures 3-1 and 3-2, bottom panels), with average COP RMS displacements of 4.36 ± 0.88 mm and 1.78 ± 0.17 mm, respectively. Although, the percent change between Locked and Unlocked conditions was larger in the COM feedback (183% increase), compared to the no feedback condition (94.7% increase), the differences were not found to be statistically significant between feedback conditions (P=0.19).  In the COPFB condition, 15 of 16 participants had larger COP RMS during the Locked compared to the Unlocked condition (Figures 3-1 and 3-2, bottom panels), with average displacements of 5.56 ±0.83 mm and 1.56 ±0.11 mm in the Locked and Unlocked conditions respectively. With COPFB, the percent change between the Locked and Unlocked condition was 286%, which was significantly greater (P=0.03) than the increase observed in the no feedback condition (86% increase). 55  3.4 Discussion  Traditional theories suggest that the COP controls, or corrects for, deviations of the COM from a desired position or point of equilibrium. Based on these theories, minimizing or locking COM displacements without participants’ knowledge would be expected to result in a concurrent decrease in COP displacements. Contrary to these theories, the results of the current study converged with prior evidence, and showed that the COP actually increases when participants are Locked compared to when they are Unlocked and swaying freely. In the present study, we observed increases in RMS of COP displacement in the Locked (3.37 mm) compared to Unlocked (2.47 mm) condition without visual feedback (NOFB). Likewise, Carpenter et al. (2010) also showed that the RMS of COP displacements increased in the Locked (3.25 mm) compared to Unlocked (1.74 mm) conditions, respectively. While these results together suggest a possible exploratory role of postural sway, we still need to rule out whether the increases in COP displacements, observed when the COM was stabilized, could potentially be the result of sensory illusions or motor drift.  Therefore, the current study was designed to investigate whether illusory motion of the stationary body during locking may have elicited reactive COP displacements. Based on the configuration of the participant within the apparatus (Figure 2-1A), sensory illusions may have emerged during locking from a mismatch between a sensation of a change in pressure/force between the body and the board, or afferent feedback from other sources (i.e. cutaneous or force feedback), and the actual displacements of the body, eliciting reactive COP responses. While proprioceptive illusions have strong influences on our perception of movement, providing accurate visual input can significantly reduce these illusions (Lackner 56  and Taublieb 1984; Izumizaki, Tsuge et al. 2010). Therefore, if there was an influence of sensory illusions, we hypothesized that the change in COP displacements from Unlocked to Locked would be significantly reduced when participants were provided visual confirmation that the COM had been stabilized. In the current study, we tested this argument, by providing direct visual feedback of COM displacements to provide clear evidence to the subject that the COM was in fact stable. Despite this visual confirmation, no significant differences were observed in the change in COP displacements from Unlocked to Locked, suggesting that sensory illusions did not lead to the observed increases in COP displacements during locking. In addition, the work of Carpenter et al. (2010) and others have argued that the likelihood that there are small pressure changes between the body and the apparatus would be unlikely to be sufficient to generate illusions. This is because we would expect minimal pressure changes on the trunk for such small disturbances that occur in the current experiment, due to the large surface area of the back of the board and long lever arm of the rigid board when compared to the size and length of the feet (Fitzpatrick, Taylor et al. 1992).  In the current paradigm, we also had to consider that increases in the amplitude of COP displacements during locking may have simply reflected a drift in motor output. Motor drift is a phenomenon that occurs in de-afferented individuals during tasks requiring either constant position or constant force output. In these individuals, over time, the motor output tends to drift either in a specific or random direction, depending on the goal of the task (Rothwell, Traub et al. 1982; Sanes and Evarts 1984). Ensuring that motor drift was not contributing to our results was important because our interpretation of exploratory behaviour is based on increases in variability (as measured using RMS) observed when movement of 57  the COM is minimized. In addition, COP displacements in our previous study were detrended, implying that any linear trends (which may be indicative of motor drift) were removed from the data during data processing. As such, we were unable to rule out motor drift effects with confidence. To eliminate the possibility of motor drift, we provided participants with real time visual feedback of the COP throughout the trial and asked them to maintain a mean position. In addition, data were analyzed without prior detrending. If there was an influence of motor drift, we hypothesized that the change in COP displacements from Unlocked to Locked would be significantly reduced when participants were provided visual feedback of the COP and were able to visually control and attempt to maintain its position throughout the trial. Rather than finding a decrease in the change in COP displacements from Unlocked to Locked, increases in COP displacements were even greater when COP feedback was provided. This finding provides evidence against any contribution of motor drift. A further argument against the potential for motor drift to confound our results, is that angular displacements of the COM during locking in the current (average COM angular range across conditions of 0.09 ± 0.02 deg) and previous study (Carpenter, Murnaghan et al. 2010), were still within perceptual ranges, ruling out a state of sensory deprivation.  The suggestion that there may be an exploratory role for motor variability has been described in a variety of motor control tasks. For example, when fixating the eyes on a visual target, rapid, involuntary eye movements known as microsaccades play a fundamental role in visual perception by ensuring continuous motion of the image projected onto the retina. Without this continuous motion, the visual environment rapidly fades from view (MartinezConde, Macknik et al. 2006; Rolfs 2009). Therefore, microsaccades ensure constant change 58  in visual input, which is ideal since our nervous system has evolved to detect changes more readily than static stimuli. Similarly in postural control, postural sway is commonly viewed as error or noise in the system (Riccio 1993; Riley, Mitra et al. 1997; van Emmerik and van Wegen 2002; Blaszczyk, Cieslinska-Swider et al. 2009). However, some studies have theorized that sway variability may represent a perception-action strategy that allows one to acquire essential information about the interaction with the environment (Riccio 1993; Riley, Mitra et al. 1997). As described previously (Carpenter, Murnaghan et al. 2010), this action may serve as a means to acquire a certain quality and quantity of sensory information. In fact, during development, arguments to this effect have been applied to the larger sway observed in younger children during development, which is thought to facilitate the formation of “a reliable and stable sensorimotor relationship for postural control” (Chen, Metcalfe et al. 2008). In these children, postural sway may act as a means of gathering and experiencing a variety of sensory interactions during stance, in order to improve the development of a proficient postural control system. Given that larger sway in children may represent the CNS’s attempt to couple sensori-motor action during stance, it is conceivable that smaller amounts of controlled sway may continue to be used by the CNS throughout life as a means to ensure a constant flow of sensory inputs. Likewise, a return to larger sway in older adults may represent a means for the CNS to generate more sensory information to compensate for the decreased speed and sensitivity of sensory systems in this population. As opposed to a negative consequence of a failing postural control system, the increased magnitude of sway in these populations may be an adaptation of similar origin to the larger sway observed in young children, and be reflective of the CNS’s attempt to re-establish or strengthen sensorimotor control. 59  There are important clinical implications from the results of the current study. Our findings of increased COP displacements, observed despite providing convincing feedback to the subjects, provides further support for an exploratory role of postural sway. In contrast to this view, larger magnitudes of postural sway in populations with balance deficits due to age or disease are considered to be indicative of instability and greater fall risk. Therefore, they are often treated with rehabilitation and preventative strategies aimed at decreasing sway. However, if postural sway is in fact exploratory, and beneficial in acquiring sensory information to develop a better representation of where the body is in space, attempting to decrease sway may oppose the natural adaptations of the CNS that are required to maintain the integrity of the postural control system. Based on conflicting interpretations of increases in postural sway in these populations, it is imperative that we first develop an improved understanding of the origins of postural sway in general. If, as our results suggest, there is support for an exploratory role of postural sway, a serious re-evaluation of current clinical practices designed to deal with balance control deficits due to age or disease may be warranted.  60  COP Feedback  COM Feedback  COM angle RMS (deg)  No Feedback  Locked  Unlocked  Unlocked  Locked  Unlocked  Locked  Unlocked  Locked  Unlocked  Locked  COP RMS (mm)  Unlocked  Figure 3-1  Locked  Mean changes from Unlocked to Locked for all 16 subjects in each of the three feedback conditions. Top panels illustrate the magnitude of the decrease in RMS of COM angular displacement (deg) for all subjects when Locked compared to Unlocked in each of the three feedback conditions (NOFB, COPFB, and COMFB). Bottom panels illustrate the concurrent changes in RMS of COP displacements (mm) for all subjects when Locked compared to Unlocked in each of the feedback conditions. Black lines represent subjects who showed increases in COP displacements, while grey lines represent subjects who showed decreases in COP displacements, when movement of the COM was minimized.  61  No Feedback  COP Feedback  COM Feedback Unlocked  COM angular displacement (deg)  Locked ooLocke  COP displacement (mm)  d  time (s)  Figure 3-2  time (s)  time (s)  Individual subject traces in each of the three feedback conditions. Upper panels illustrate the COM angular displacements (deg) over the 60s periods used for data analysis in the Unlocked (grey) and Locked (black lines) conditions. Bottom panels illustrate the corresponding COP displacements over the 60s period used for data analysis in the Unlocked (grey) and Locked (black lines) conditions.  62  4 Chapter: Are increases in COP variability observed when participants are provided explicit verbal cues prior to COM stabilization?3 4.1 Introduction  Postural sway is commonly thought to result from the interplay between movements of the body or center of mass (COM), and ground-reaction forces acting beneath the feet (center of pressure (COP)), where the COP controls, or corrects for, deviations of the COM from a desired position or point of equilibrium. However, some researchers have begun to challenge this assumption, suggesting that the natural displacements of the body associated with postural sway may be used as an exploratory means of acquiring sensory information (Gatev et al., 1999; Riccio, 1993; Riley et al., 1997; Riley & Turvey, 2002; Stoffregen & Riccio, 1988). Using a novel method to minimize or “lock” COM displacements in the anterior-posterior plane during stance without subject awareness, Carpenter et al. (2010) and Murnaghan et al. (2011) demonstrated that COP amplitude increased when the COM was locked, compared to when the COM swayed freely, even when participants were provided visual confirmation of COM stabilization. Since locking stabilized movements of the COM, the increase in COP amplitude could not be attributed to increased movement of the COM. Therefore, it was concluded that the central nervous system (CNS) may actively drive COP displacements in an attempt to move the body and regain afferent input (Carpenter et al., 2010; Murnaghan et al., 2011), which otherwise would have been acquired from normal postural sway.  3  The following chapter has been published in Gait & Posture, An International Journal under the  editorial direction of the International Society for Posture and Gait Research. 63  Alternatively, it could be argued that the increases in COP displacements were not a function of exploratory behavior, but rather a result of the CNS adapting to novel postural conditions. This interpretation is based on the perspective that the CNS regulates posture through the use of an internal model (Lestienne & Gurfinkel, 1988; Massion, 1992; Massion, 1994; Massion, 1998; Mittelstaedt, 1983) which allows the generation of appropriate motor commands based on the predicted dynamics of the task and the anticipated response of the system (Chew, Gandevia, & Fitzpatrick, 2008; Gottlieb, 1994; Johansson et al., 1988; Kawato, 1999; Neilson, Neilson, & O'Dwyer, 1988; Shadmehr & Mussa-Ivaldi, 1994; Wolpert et al., 1995). Specifically, it could be argued that the unexpected stabilization of the COM used by Carpenter et al. (2010) and Murnaghan et al. (2011) changed the dynamics of upright standing unexpectedly, forcing participants to update the internal model used to control stance, leading to movement errors (Eun Jung Hwang and,Reza Shadmehr, 2005) expressed as increases in COP displacement. If this is the case, Imamizu et al. (2007) have suggested, based on experimental and computational data during a targeted reaching task, that explicit contextual cues can selectively decrease the errors by improving our ability to predict the specific motor commands that are required for the new dynamics of the task.  The aim of the current study was to determine whether increases in COP variability observed when the COM is stabilized, could be explained as an attempt by the CNS to adapt to novel sensorimotor conditions that necessitated an update to the internal model used to control stance. To address this aim, participants were given a verbal cue that provided them with explicit knowledge that movements of the COM would be minimized by the experimenter. In this condition, any erroneous COP displacements that arise as the CNS 64  attempts to adapt to the novel postural conditions should be reduced (Imamizu et al., 2007). Therefore, if increases in COP displacement were the result of an adaptive attempt to update an internal model, we hypothesized that increases in COP displacements would be reduced from unlocked to locked when participants were provided an explicit verbal cue compared to when no cue was provided.  4.2  Methods  4.2.1  Participants  Eighteen healthy young adults (9 females; mean ± sd for age=22.5 ± 2.8 years; height=171.3 ± 7.1 cm; weight=67.7 ± 11.7 kg) volunteered in the study. Each participant provided informed written consent, and the experimental protocol was approved by the Clinical Research Ethics board at the University of British Columbia.  4.2.2  Apparatus  The apparatus used was similar to that used in previous studies (Figure 4-1A) (Carpenter et al., 2010; Murnaghan et al., 2011). Briefly, in all trials, participants stood on a forceplate and were firmly braced against a rigid board. The board was attached to a closedloop pulley system that allowed “normal postural sway” at the ankle joint unless the experimenter applied a brake that discretely locked the board (and thus COM) in place in the sagittal plane.  65  4.2.3  Experimental protocol  All participants were asked to stand as still as possible in two trials. In both trials, the initial 30s period was used to allow the transient component of sway to stabilize (Carroll & Freedman, 1993), and the following 30s was used to calculate the mean COP position to be used as the threshold for “locking” (“Mean” in Figure 4-1B). Following the initial 60s, participants stood freely in the “Unlocked” condition for a minimum of 135s (Unlocked) and then the board was locked without participant knowledge when the COP was within 2 standard deviations of the calculated mean COP. Subjects stood in the locked condition for a minimum of 135s (Locked). In the second “cue” trial, participants were provided with an explicit verbal cue immediately prior to locking (Figure 4-1B). To ensure participants understood the implications of the verbal cue, participants were provided with a detailed description of what it meant to be “locked” prior to initiating the trial, indicating that the lock would be applied and thus, COM displacements would be stabilized. During the trial, the experimenter informed participants of when locking would occur by providing them with a three second countdown. The “no cue” condition was always performed before the “cue” condition to minimize any carry-over effects from having knowledge of locking.  4.2.4  Measurements  Ground reaction forces and moments (#K00407, Bertec, USA) and kinematic data (Optotrak Certus, Northern Digital Inc., Canada) were sampled at 2000 Hz and 500 Hz, respectively. Data were processed as described in previous studies (Carpenter et al., 2010; Murnaghan et al., 2011), and used to calculate the Root Mean Square of anterior-posterior 66  (AP-COP RMS) and medial-lateral (ML-COP RMS) COP displacements, as well as the range of COM angular displacements over a 120 s period in each trial when participants were unlocked and locked. The 120 s measurement periods began 135 s prior to the beginning, and end, of the locking period respectively.  4.2.5  Statistics  To test whether any changes observed from unlocked to locked depended on the presence of an explicit verbal cue, a 2 (lock) x 2 (cue) repeated measures ANOVA was used to analyze the range of COM displacements, AP-COP RMS and ML-COP RMS. Post-hoc comparisons were corrected for multiple comparisons using a Bonferroni correction, and significance was assumed at an alpha level of 0.05.  4.3 Results  The results showed that the apparatus was effective in minimizing displacements of the COM in the locked condition. Across the eighteen participants, there was a significant main effect of locking on the range of COM angular displacements (F(1,17)=63.85, P<0.01). COM angular displacements decreased from 1.400 deg (SE=0.16) to 0.114 deg (SE=0.014). There was no main effect of cueing (F(1,17)=1.483, P=0.240), or interaction between locking and cueing (F(1,17)=1.905, P=0.185) (Figures 4-2 and 4-3).  The results also showed that following an external stabilization of the COM, there were changes in the RMS of AP but not ML COP displacements (Figure 4-3). In the AP 67  direction, there was a significant main effect of locking (F(1,17)=10.55,P<0.01) with COP displacements increasing from 3.90 mm (SE=0.43) to 8.30 mm (SE=1.30). There was no main effect of cueing (F(1,17)=0.056,P =0.816), or interaction between locking and cueing (F(1,17)=0.256, P=0.620) (Figures 4-2 and 4-3). In the ML direction, there were no significant main effects of locking (F(1,17)=0.198,P=0.662) or cueing (F(1,17)=0.088,P=0.816).  4.4 Discussion  Internal models are an important theoretical concept used to understand how complex neural computations are simplified within the CNS (Wolpert et al., 1995; Wolpert & Kawato, 1998b). Typically used to describe voluntary reaching behaviour, internal models are the neural representations of the expected behaviour of an object or system in response to a given neural command. Therefore, internal models describe the input/output relationships of the system (Kawato, 1999; Wolpert et al., 1995). If the input/output relationships are suddenly altered, movement errors are known to arise (Eun Jung Hwang and,Reza Shadmehr, 2005; Imamizu et al., 2007), and individuals must adapt the internal model (or create a new internal model) to recalibrate the motor commands to match the new dynamics of the task. In this context, the increase in errors is thought to be caused by “contamination of motor commands from the internal model used in the previous block” (Imamizu et al., 2007). However, Imamizu et al. (2007) have suggested, based on experimental and computational data during a target pointing task, that explicit contextual cues selectively decrease errors by improving our ability to predict the specific motor commands that are required for the new dynamics of the task.  68  Although internal models have been an important theoretical concept applied to understand voluntary motor control tasks for some time, they have more recently been used to understand how posture is controlled (Morasso et al., 1999). It is believed that the CNS builds internal models, which are used to carry out the necessary and complex computations that allow posture to be controlled in such a simple and automatic manner (Chew et al., 2008; Kawato, 1999; Morasso et al., 1999; Wolpert et al., 1995). Because humans have experience standing in a gravitational environment from the time we begin to stand, we have a complex representation of the body during stance that is partly innate and most likely strengthened with experience. This representation includes knowledge of verticality based on vestibular, visual and somatosensory inputs, and a perception of the trunk axis. It also includes a representation of the body’s geometry as well as its dynamics (Massion, 1992). Based on this representation, it is thought that we use internal models to predict a future state of the body based on information about its current state and knowledge of motor commands. Alternatively, we can determine what motor commands are appropriate to achieve a desired state of the body (Wolpert et al., 1995). In the novel paradigm used throughout the current and previous experiments (Carpenter et al., 2010; Murnaghan et al., 2011), although participants are not consciously aware of any change, stabilizing the COM alters the context under which we normally stand. Therefore, this manipulation may distort the input/output relationships we are familiar with during quiet standing leading to errors (Wolpert & Kawato, 1998b), which are expressed as increases in COP displacements. In our study, COP displacements increased when displacements of the COM were minimized externally by the experimenter without participants’ knowledge (no cue condition). Even when participants were provided an explicit verbal cue indicating how and when stabilization would occur (cue 69  condition), COP displacements still increased, and the magnitude of the increase was similar to that observed when they were unaware of COM stabilization. Therefore, the results of the current study do not support the hypothesis that increases in COP displacements observed following COM stabilization are a by-product of adapting the internal model used during upright stance.  Although increases in COP displacements occurred in both the cue and no cue conditions, it could be argued that participants may not have been able to use the explicit cue to consciously and quickly adapt the internal model to reduce any errors that may be expressed as COP displacements. However, the results of Imamizu et al. (2007) would suggest that explicit contextual information can be used to very quickly modify the response, as they observed significant decreases in errors immediately following a change in the dynamics of the task (first 1-40 trials following the change). Given their observations, it would seem plausible that the explicit information provided in the current study could also be used quickly to reduce errors. However, we must acknowledge that there may be differences in our ability to use explicit information in a voluntary targeting task (Imamizu et al., 2007) compared to a whole body postural task used in the current study. In addition, some authors have suggested that while explicit information may reduce initial errors, it cannot override the natural time course of implicit adaptation processes (Mazzoni & Krakauer).  While the results of this and previous studies (Carpenter et al., 2010; Murnaghan et al., 2011) do not provide conclusive evidence of an exploratory role of postural sway under normal conditions, they have challenged alternative explanations such as sensory illusions, 70  motor drift, or an attempt to adapt an internal model of the body during stance. In addition, the results challenge a number of theories that are proposed in the literature and used to explain the control or use of postural sway.  One theory described in the literature assumes that posture is controlled in a negative feedback manner. In this theory, it is suggested that afferent information arising from the displacements of the body that are associated with postural sway, is used in a feedback manner to generate corrective ground reaction forces (COP) that return the body to its equilibrium position (F. Horak & MacPherson, 1996; Prieto, Myklebust, & Myklebust, 1993). Based on this description, it is assumed that the goal of the CNS is always to maintain an equilibrium position of the body during stance and to minimize any deflections from this ideal position. Observations of increases in COP displacements in this and previous studies argue against the notion that posture is controlled in this manner. If COP displacements were used only to correct or control for displacements of the body or COM, an equivalent reduction in COP displacements should have been observed following stabilization. However, the fact that increases in COP displacements were observed consistently across this and previous studies (Carpenter et al., 2010; Murnaghan et al., 2011) confirm that posture is not controlled in a pure negative feedback manner.  Other theories suggest that, rather than using afferent information in a negative feedback manner, the afferent information acquired from postural sway is received by the CNS, but ignored until the postural control system must implement feedback mechanisms (i.e. when the COG reaches the limits of stability) (J. J. Collins & De Luca, 1993). However, 71  if, as suggested by Collins and Deluca (1993), afferent information associated with displacements of the body or COM was ignored until it reached a critical threshold, then the decreased COM displacements caused by external stabilization should not require any corrective COP displacements. In contrast, increases in COP displacements were consistently observed in this and previous studies (Carpenter et al., 2010; Murnaghan et al., 2011), providing evidence against the proposal that afferent information is ignored. Therefore, increases in COP displacements following stabilization suggest that afferent information may be monitored and used to provide the CNS with afferent information indicating where the body is positioned in space.  By providing evidence against alternative explanations for increases in COP displacements, and challenging other theories that are proposed in the literature and used to explain the control or use of postural sway, the results of the current study provide further support for an exploratory role of postural sway (Riccio, 1993; Riley et al., 1997; Riley & Turvey, 2002; Riley & Clark, 2003; Stoffregen & Riccio, 1988). According to this theory, the central nervous system takes advantage of the natural oscillations of the body arising from internal or external forces (Hunter & Kearney, 1981; Soames & Atha, 1982) and/or centrally-generated muscle activity (Gatev et al., 1999), to ensure constant stimulation of a variety of receptors from the visual, vestibular and proprioceptive systems. This continuous stimulation would ensure that the central nervous system is consistently afforded a broad array of sensory information and that an accurate sense of body orientation in space can be maintained. The idea that motion is required to maintain afferent inflow has been proposed for decades in a variety of sensory systems. For example, in regards to cutaneous receptors, 72  Nafe and Wagoner (1941) (c.f. (Gibson, 1962)) have suggested that if there were absolutely no motion, these receptors would cease firing and essentially become completely ineffective. Similarly, in the visual system, if small involuntary eye movements known as microsaccades are suppressed experimentally leaving only constant retinal input, the image fades within a few seconds (Ditchburn & Ginsborg, 1952; Engbert & Kliegl, 2004; Riggs, Ratliff, Cornsweet, & Cornsweet, 1953). Interestingly, Gibson (1962) suggested that under normal conditions, afferent receptors would rarely be subjected to no or precisely constant stimulation, simply because humans always experience movements in various forms such as tremor when attempting to hold a limb in a static position, or in the form of continuous postural sway of the body during stance. Therefore, the observation of increased COP displacements in the locked condition with or without verbal or visual feedback (Murnaghan et al., 2011) may represent an attempt of the CNS to increase torques to generate normal sway lost through unexpected stabilization of the COM, thereby re-stimulating afferent receptors.  73  No Cue  Cue  Unlocked  Figure 4-1  Locked  Mean RMS of anterior-posterior COP displacements for all subjects in the no cue (top panel) and cued (bottom panel) conditions. Grey boxes represent the Unlocked condition, while black boxes represent the Locked condition.  74  Figure 4-2  COM angular displacements (top panel) and AP COP displacements (bottom panel) from a single representative subject in the no cue (left panel) and cued (right panel) conditions over the 120s periods used for data analysis in the Unlocked (grey lines) and Locked (black lines) conditions.  75  5 Chapter: Does the cortex contribute to exploratory postural sway? 4 5.1 Introduction  Traditional theories of postural control suggest that corrective ground reaction forces acting beneath the feet (centre of pressure (COP)), correct or control for displacements of the body or centre of mass (COM). In this view, larger and therefore unstable COM displacements require larger COP displacements, whereas smaller COM displacements require smaller COP displacements. Using a novel paradigm to stabilize or “lock” the COM, it has been shown that, rather than decrease as traditional theories would predict (Ishida & Miyazaki, 1987; Johansson et al., 1988; Peterka, 2000), COP displacements actually increased. This increase in COP displacement persisted with changes in visual conditions (Eyes open and eyes closed) (Carpenter et al., 2010), when participants were provided visual confirmation of COM stabilization (Murnaghan et al., 2011) and with explicit knowledge of stabilization (Murnaghan, Squair, Chua, Inglis, & Carpenter, In Press). Therefore, it was interpreted that COP displacements may reflect the central nervous system’s attempt to reestablish movement of the body so as to acquire a critical level of incoming sensory information, which is otherwise acquired through natural postural sway.  While increases in the variability of COP displacements have been observed consistently across the majority of subjects during conditions of restricted sway, the origin of this increase remains unknown. Under normal sway conditions, it is suggested that the movement associated with postural sway may ensure that a large number, and variety, of  4  The following chapter was submitted and reviewed. 76  sensory receptors from multiple sensory systems are stimulated. This sway may be the result of internal or external forces acting on the body or COM (Hunter & Kearney, 1981; Soames & Atha, 1982), or be centrally-generated in a feed-forward manner (Gatev et al., 1999). When the COM is externally stabilized without participant awareness, the amount or gain of available sensory information is most likely significantly reduced. As such, although participants may be unaware of any change, they may actively generate displacements of the COP in an attempt to move the body and regain a level of afferent input that provides critical information regarding the position of the body in space.  One way to investigate whether increases in COP displacements are actively generated, either during normal or restricted sway conditions, is to use coherence analysis between measures of cortical (electroencephalography – EEG) and muscle activities (electromyography - EMG). Corticomuscular coherence (CMC) is thought to provide evidence of a change in the strength of association between oscillatory activity in the cortex and the muscle, and has a spectral maximum in humans between ~15-30 Hz (Gerloff et al., 2006; Mima & Hallett, 1999). Based on estimations of corticomuscular conduction times, coherence within the beta range (15-30 Hz) is thought to reflect oscillatory behaviour of the direct corticospinal pathway (Mima & Hallett, 1999).  Some have suggested that corticomuscular coherence in the 15-30 Hz range during quiet stance is low (Luu, 2010), or even absent (Masakado et al., 2008), compared to equivalent voluntary muscle activations (Luu, 2010). Furthermore, it has been proposed that motor cortical areas do not become functionally involved until disturbances greater than 77  natural sway occur (Slobounov, Hallett, Stanhope, & Shibasaki, 2005; Taube et al., 2006), or when the cortex is engaged in voluntary effort to generate the amount of torque associated with normal postural sway (Luu, 2010). However, if there is insufficient incoming sensory information, as may be the case when the COM is externally restricted, as in prior studies, cortical areas may play a greater role in order to drive an increase in variability of COP displacements. As such, the objective of the current study was to determine whether changes in corticomuscular coherence accompanied increases in COP displacements when a participant’s COM is stabilized (“Locked”) compared to when they swayed freely (“Unlocked”). Based on previous studies, we hypothesized that, in the majority of participants, there would be an increase in COP displacements when the COM was stabilized during quiet stance. Since corticomuscular coherence may provide an indication of greater cortical drive to the muscles, it was further hypothesized that, in those participants whose COP displacements increased with locking, significant increases in coherence at frequencies in the range of 15-30 Hz would also be observed.  5.2 Methods 5.2.1  Participants  Twelve healthy young adults (8 females; mean ± sd for age = 23.8 ± 3.9 years; height = 173.3 ± 7.0 cm; weight = 67.8 ± 11.3 kg) participated in the study. Each participant provided informed written consent, and the experimental protocol was approved by the Behavioural Research Ethics board at the University of British Columbia. All participants  78  were completely naïve to the goals of the experiment and the intended effect of the apparatus on postural sway.  5.2.2  Apparatus  The apparatus used in the study was the same as that described in Carpenter et al. (2010) and Murnaghan et al. (2011). During all experimental trials, participants were firmly braced with their back against a rigid board with adjustable straps tightened firmly around the head, shoulders, chest, waist, hips/upper thighs, and upper shank, to prevent movement at any joint except the ankle. The board was 1.66 m high (including head rest) x 0.61 m wide and had a total mass of 12.5 kg. The board was attached to a closed-loop pulley system that allowed “normal postural sway‟ at the ankle joint unless the experimenter applied a brake that discretely locked the board (and thus COM) in place in the sagittal plane. To eliminate any chance that the participants could receive auditory cues indicating that they were being locked, all participants wore earplugs that reduced any noise within the testing area. Participants also wore blinders designed to occlude both horizontal and vertical peripheral vision, while maintaining full visual input anteriorly. In all conditions, participants stood with their arms crossed and feet shoulder width apart on a forceplate (#K00407, Bertec, USA).  5.2.3  Experimental protocol  The study required measurable levels of corticomuscular coherence between electroencephalographic (EEG) and electromyographic (EMG) activities during voluntary 79  muscle contraction. This cannot be obtained in all participants and is reported to occur in approximately 50-75% of individuals (Masakado et al., 2008; Perez, Soteropoulos, & Baker, 2012). As such, participants were initially screened to ensure that they showed significant corticomuscular coherence with at least one muscle of the lower leg (Lateral and Medial Gastrocnemius, Soleus) during a 2-minute seated low-level contraction (~30% MVC), and that this magnitude of coherence was significantly larger than that recorded during a 2minute seated relaxed trial (Figure 5-1A and 5-1B). Twelve participants showed measurable levels of corticomuscular coherence. Each of the twelve participants were fitted into the apparatus and asked to stand as still as possible in one trial of ~6 minutes standing duration (Figure 5-2). The first 30s of the trial was used to allow the transient component of sway to stabilize (Carroll & Freedman, 1993), and the following 30s was used to calculate the mean COP position to be used as the threshold for “locking.” Following the initial 60s, participants stood freely in the “unlocked” condition for a minimum of 135s (unlocked) and then the board was locked without participant knowledge when the COP was within 2 standard deviations of the calculated mean COP, for a minimum of 135s (locked). One hundred thirtyfive second periods were used to ensure two minutes of time could be analysed in each of the Unlocked and Locked conditions.  5.2.4  Measurements  In order to characterize the oscillatory interactions between motor cortical areas and motor neuron pools of muscles using coherence analysis, we collected synchronous measures of electromyographic (EMG) and electroencephalographic (EEG) activities. Surface EMG activity was sampled bilaterally from lateral and medial gastrocnemius (LGAS and MGAS), 80  and soleus (SOL) muscles using bipolar Ag/AgCl surface electrodes placed ~2cm apart on each muscle belly. EMG data were sampled at 2048 Hz, band-pass filtered between 30 and 500 Hz, and full-wave rectified to capture the temporal pattern of grouped motor unit firing regardless of its shape, which can vary with the relative position of active and reference electrodes (D. M. Halliday et al., 1995; Mima & Hallett, 1999). EEG was collected using a 32 channel electrode configuration based on the International 10-20 standard (CAPANTWG32, Advanced Neuro Technology, The Netherlands), with the vertex (Cz) positioned halfway between the Nasion and Inion, and the reference electrode positioned anteriorly to the vertex at AFz. EEG data were sampled at 2048 Hz and, band-pass filtered between 1 and 500 Hz. We focused primarily on recordings over the leg area of the sensorimotor cortex (vertex-Cz), where coherence between leg muscle EMG and the cortex is strongest (Salenius, Portin, Kajola, Salmelin, & Hari, 1997). During all EEG recordings participants were instructed to limit any blinking, jaw clenching, or facial expressions that could introduce artefacts into the EEG signal. EEG and rectified EMG data from each trial were then segmented into 120s periods of Unlocked and Locked data. The 120s measurement periods began 135s prior to when participants were initially locked, and 135s prior to when the lock was removed, respectively.  Coherence analysis was based on the theoretical framework described by Halliday et al. (1995) and Rosenberg et al. (1989) and calculated by modifying publicly available Matlab scripts (Neurospec 2.0 (Dakin, Luu, van den Doel, Inglis, & Blouin, 2010; D. M. Halliday et al., 1995; Rosenberg et al., 1989)). The first part of the analysis was performed on individual records from each participant, using frequency domain measures of correlation between EEG 81  and rectified EMG in both the Unlocked and Locked conditions, with EEG as the reference signal and EMG as the output signal. The second part of the analysis required further concatenation across all participants who showed an increase in COP displacements with COM stabilization to create a single pooled data array for each condition. Because the amplitudes of data records being pooled may vary across participants, the records from each participant were normalized by dividing by the standard deviation prior to estimating pooled parameters as suggested by Baker (2000) and Halliday and Rosenberg (2000). In both the individual and pooled analyses, data from each condition were analyzed using segments of 1024 points (0.5 s), giving a frequency resolution of 2 Hz. Coherence estimates are unitless and bounded between 0 and 1 and enable the identification of correlated frequencies between the two signals, where 1 indicates a perfect relationship and 0 indicates independence. Any coherence was deemed significant at a particular frequency when it surpassed the 95% confidence interval, which was calculated according to the number of segments (D. M. Halliday et al., 1995). Differences in coherence between conditions were then calculated using a Difference of Coherence (DOC) test (Amjad, Breeze, Conway, Halliday, & Rosenberg, 1989).  Ground reaction forces and moments were sampled at 1000 Hz and low-pass filtered offline using a 5 Hz dual-pass Butterworth filter before calculating COP in the anterior– posterior (AP) and medial-lateral (ML) directions. From these signals, the Root Mean Square (COP RMS) was calculated. Kinematics were sampled at 500 Hz for the duration of each trial using an Optotrak three-dimensional optical motion analysis system (Northern Digital Inc., Waterloo, Ontario, Canada) with infrared light emitting diodes (IRED) placed on the 82  cable, ankle joint, and back of the board at a level that approximated the height of the COM. Kinematic data were filtered at 5 Hz with a dual-pass Butterworth filter and used to calculate linear displacements of the COM in the sagittal plane. From this signal, the RMS of AP COM displacements (COM RMS) were calculated. Finally, the magnitude of EMG from LGAS, MGAS and SOL was calculated as an integrated area of the processed and rectified EMG averaged across the left and right sides. All dependent variables were calculated over the same 120s Unlocked and Locked periods.  5.2.5  Statistics  In addition to the statistical tests described above which were used to compare estimates of coherence, we tested whether there were significant differences in all other dependent variables across Unlocked and Locked conditions using dependent t-tests. Significance was assumed at an alpha level of 0.05 and was corrected for multiple comparisons using a Bonferroni correction.  5.3 Results  In the current study, the apparatus was effective in minimizing displacements of the COM without participant awareness. Across all 12 participants, COMRMS was significantly reduced in the Locked (0.55 mm) compared to Unlocked (5.92 mm) condition (p<0.001). The result of stabilizing the COM on COP displacements was similar to that reported in previous studies (Carpenter et al., 2010; Murnaghan et al., 2011). Increases in COP displacements were observed primarily in the AP direction with minimal and non-significant 83  differences in the ML direction (p=0.16). In the AP direction, nine of twelve subjects showed increases in COP displacements from Unlocked to Locked and, on average, COP displacements increased from 4.18 mm to 13.2 mm (p=0.02) (Figure 5-3). Increases in AP COP displacements from Unlocked to Locked were associated with a significant increase in the amplitude of MGAS EMG (p=0.02) and LGAS (p=0.05), with a similar trend observed in SOL EMG (p=0.08).  Analysis of corticomuscular coherence showed that increases in COP displacements with locking were not associated with increases in coherence at frequencies in the range of 15-30 Hz. Specifically, when analyzing the individual records from each of the nine participants whose COP displacements increased from Unlocked to Locked, we found that there was no concomitant increase in coherence between oscillatory activities of the EEG and triceps surae EMG. Despite having significant increases in coherence in at least one muscle during the seated voluntary contraction (Figure 5-4A), when standing freely in the Unlocked condition, coherence between Cz and triceps surae muscles was reduced or absent (Figure 4B). Although COP displacements increased with locking in this group of participants, we found that the magnitude of coherence did not change in8 of 9 participants (Figure 5-4B). In the participant whose magnitude of coherence between Unlocked and Locked was significantly different, coherence was actually greater in the Unlocked condition compared to the Locked condition.  To confirm that increases in COP displacements were not associated with concomitant increases in CMC and that the absence of any change in CMC between 84  Unlocked and Locked conditions was not the result of insufficient power, data records from each of the 9 participants whose COP increased from Unlocked to Locked were pooled across each condition. Similar to our findings from the individual data analysis, clear increases in CMC were observed from seated relaxed to seated contracting conditions, illustrating that measurable levels of corticomuscular coherence between EEG and EMG activities were attainable during voluntary contraction (Figure 5-5A). When standing freely in the Unlocked condition, measures of CMC were minimal or absent, and there was no significant difference in coherence from Unlocked to Locked (Figure 5-5B).  5.4 Discussion  Postural sway is commonly thought to result from the interplay between movements of the body or center of mass (COM), and ground-reaction forces acting beneath the feet (center of pressure (COP)), where the COP controls, or corrects for, deviations of the COM from a desired position or point of equilibrium. Based on this theoretical framework, it has been hypothesized that when movements of the body or COM were stabilized, COP displacements would also be reduced in a similar manner. However, in accordance with our previous experiments (Carpenter et al. 2010; Murnaghan et al. 2011; Murnaghan et al., In Press), when displacements of the COM were minimized by the experimenter without participants’ knowledge, COP displacements increased in 75% of participants and these increases were accompanied by increases in triceps surae muscle activity. Given that postural sway under normal conditions may be actively generated in a feedforward manner (Gatev et al., 1999), it seems plausible that under conditions of external stabilization increases in COP  85  displacements may be driven in a similar manner, and potentially be mediated by the motor cortex.  When participants were standing in the apparatus and freely swaying, little to no coherence between EEG and surface EMG (lateral/medial gastrocnemius or soleus) in the 1530 Hz frequency range was observed. Observations of absent or low levels of coherence during normal standing were consistent with results of previous studies that have been unable to detect similar magnitudes of EEG-EMG coherence during postural tasks (standing relaxed and standing still) as those obtained in the same participants during voluntary contraction (Luu, 2010; Luu, 2010; Masakado et al., 2008). As a whole, these results suggest that postural sway in unrestricted conditions is not actively generated by the leg region of the motor cortex, and therefore is unlikely to be the origin of centrally-driven feedforward control as proposed by Gatev et al. (1999).  We initially hypothesized that when the COM was stabilized by the experimenter, increases in the magnitude of coherence would be observed. This hypothesis was based on the notion that, following COM stabilization, the amount or gain of available sensory information is most likely significantly reduced. As such, although participants are completely unaware of COM stabilization, they may increase motor drive to lower limb muscles in an attempt to move the body and maintain a level of afferent input. Contrary to our hypothesis, we found little to no coherence despite increases in triceps surae EMG. These results suggest that increases in COP displacements with locking were not the result of increasing oscillatory cortical drive (Mima & Hallett, 1999). 86  Despite the absence of any changes in oscillatory 15-30 Hz cortical drive to the musculature of the lower leg with locking, we cannot entirely dismiss a cortical origin for increases in COP displacements. Significant magnitudes of corticomuscular coherence between EEG and EMG are thought to arise when there is synchronous discharge of a large number of cortical neurons in an oscillatory manner. However, it could be that the motor cortex activates triceps surae motorneurons differently in postural tasks than in voluntary contractions (Masakado et al., 2008) and, in using an estimate of corticomuscular coherence, any cortical drive that is non-oscillatory in nature would go undetected (Petersen, WillerslevOlsen, Conway, & Nielsen, 2012). Furthermore, it could be argued that increases in COP displacements with stabilization do not originate from the leg sensorimotor area recorded in this study. Although corticomuscular coherence has been reported to be largest between Cz and shank muscle EMG under voluntary conditions (Salenius et al., 1997), it has been documented that there are corticospinal connections from other frontal and parietal areas (pre-frontal and supplementary motor areas, as well as area 5) (Dum & Strick, 1996; Geyer, Matelli, Luppino, & Zilles, 2000), and these areas have been suggested to contribute to various aspects of postural control (Jacobs & Horak, 2007; Maki & McIlroy, 2007). In addition, there is a debate regarding how lower limb musculature associates with changes in COP displacements (Gatev et al., 1999; Loram et al., 2004; Winter et al., 1998), questioning whether activation of triceps surae musculature represents the means by which the COP is controlled. Therefore, it is possible that muscles other than those of the triceps surae may contribute to the increases in COP observed following stabilization. In fact some research has suggested that foot musculature may provide active control of posture independent of any changes in ankle movement (Kelly, Kuitunen, Racinais, & Cresswell, 2012; Wright, 87  Ivanenko, & Gurfinkel, 2012). As such, we cannot ignore that there could be oscillatory cortical drive to smaller muscles of the foot that were not recorded in the current protocol. However, it should be noted that we observed changes in COP displacements with locking in the anterior-posterior direction, while the effects of foot muscle activation (abductor hallicus, flexor digitorum brevis, quadratus plantae) have been reported to correlate with mediallateral but not anterior-posterior displacements of the COP (Kelly et al., 2012).  It could be argued further, that COP displacements observed during locking were “dynamic” in nature and therefore not observable using estimates of corticomuscular coherence in the 15-30 Hz frequency band. In dynamic tasks that contain a dynamic ramp phase of contraction, the magnitude of corticomuscular coherence in the 15-30 Hz frequency range has been shown to be reduced compared to when the contraction is maintained (Kilner, Baker, Salenius, Hari, & Lemon, 2000). Rather than observing a simple reduction of frequencies within the 15-30 Hz during dynamic tasks, some have reported that there is actually a shift towards higher frequencies (Omlor, Patino, Hepp-Reymond, & Kristeva, 2007). However, our data do not suggest that this is the case since we did not find significant magnitudes of corticomuscular coherence in any frequencies up to 50 Hz (Figures 5-4B and 5-5B). In addition, although the magnitude of coherence was reported to be larger during phases of walking where the EMG is more stable or “static” in nature, significant magnitudes of coherence were still observed throughout phases of walking, a task which would involve greater modulation of EMG than that observed during our standing postural task (Petersen et al., 2012).  88  Finally, although our data do not suggest that increases in COP displacements following COM stabilization are produced via oscillatory cortical drive to triceps surae musculature, we should consider the possibility that increases could originate from other efferent pathways. One line of evidence supporting this hypothesis comes from experiments investigating whisking behaviour in rodents. Whisking is a sensorimotor behaviour used to rapidly gather detailed sensory information about the surrounding environment, and this behaviour has been shown to persist even in decorticated rats (Deschênes, Moore, & Kleinfeld, 2012; Semba & Komisaruk, 1984). While the premotor circuitry has been heavily debated, many have suggested that a large component of the modulation of whisking behaviour arises from a brainstem sensorimotor loop (Deschênes et al., 2012; Nguyen & Kleinfeld, 2005). With the many parallels that can be drawn between postural sway and whisking in the rat, it is therefore conceivable that COP displacements could be driven by subcortical structures.  The exploratory hypothesis of postural sway suggests that movements of the body during stance arising from active and/or passive mechanisms, serve to stimulate perceptual systems and provide the CNS with a broad array of afferent information (Gatev et al., 1999; Riccio, 1993; Riley et al., 1997). In the current and previous studies (Carpenter et al., 2010; Murnaghan et al., 2011; Murnaghan et al., In Press), it has been suggested that COM stabilization may significantly reduce the amount of sensory information being received by the CNS. As such, increases in COP displacements may reflect an attempt to re-establish movement of the body so as to acquire a critical level of incoming sensory information; however, this attempt does not appear to originate from the leg area of the motor cortex. 89  Under normal conditions, postural sway could arise from the independent or combined contributions of internal forces (i.e. breathing, heart rate), external forces (i.e. perturbations), and/or centrally-driven feedforward control. However, regardless of the origins of postural sway under normal conditions, movements of the body may serve a similar exploratory function and ensure the CNS is afforded a certain quality and/or quantity of sensory information.  In conclusion, the results of the current study provide further support for an exploratory role of postural sway, where displacements of the body during stance are used as a means of acquiring a broad array of sensory information from the surrounding environment. When postural sway is experimentally reduced, we suggest that COP displacements are increased in an attempt to move the body in order to maintain a critical level of sensory information that is otherwise acquired through normal postural sway. However, our results do not support that this increase is produced via oscillatory cortical input to lower limb musculature. Rather, this increase may be driven by other efferent pathways, potentially originating within the brainstem or other subcortical structures.  90  Figure 5-1  Illustration of experimental procedures used to screen participants for inclusion in the study. (A) Participants performed two two-minute seated trials. In the first trial, participants were completely relaxed, and in the second trial they maintained a low-level voluntary contraction of the plantar flexor musculature against a load (~30% MVC). (B) To be included in the study, participants were required to achieve significant magnitudes of coherence (>95% confidence interval) in the 15-30 Hz range in at least one muscle during the voluntary contraction (top panel, solid line). In addition, the magnitude of coherence had to be significantly greater than that achieved during the seated relaxed trial (top panel, dashed line). Significant differences were determined using a difference of coherence (DOC) test (bottom panel), and having the DOC exceed the 95% confidence intervals. If the DOC exceeded the lower interval, the magnitude of coherence during the voluntary contraction was statistically larger than the coherence estimated in the relaxed condition.  91  Figure 5-2  Sagittal plane view of the apparatus used to stabilize the COM without participants’ knowledge. During the trial, participants were firmly braced with their back against a rigid board with adjustable straps tightened firmly around the shoulders, chest, waist, hips/upper thighs, and upper shank, to prevent movement at any joint except the ankle. The board was attached to a closed-loop pulley system that allowed “normal postural sway‟ at the ankle joint unless the experimenter applied a brake that discretely locked the board (and thus COM) in place in the sagittal plane. Participants wore earplugs to eliminate any auditory cues, and blinders designed to occlude both horizontal and vertical peripheral vision, while maintaining full visual input anteriorly. In all conditions, participants stood with their arms crossed and feet shoulder width apart on a forceplate, and we measured EEG and bilateral surface EMG from lateral and medial gastrocnemius and soleus muscles.  92  Figure 5-3  Average COM (top panel) and COP displacements (bottom panel) in the Unlocked (grey boxes) and Locked (black boxes) conditions. Across all 12 participants, COM RMS was significantly reduced in the Locked compared to Unlocked condition. Stabilizing the COM resulted in a significant increase in COP displacements in 9 of 12 participants.  93  Figure 5-4  Estimates of coherence between EEG (Cz) and EMG (left MGAS) from a representative subject. (A) During a seated low level voluntary contraction, the participant achieved significant levels of coherence (top panel, solid black line). The difference of coherence test (bottom panel) illustrated that the magnitude of coherence during the voluntary contraction (top panel, solid line) was significantly larger than during the relaxed condition (top panel, dashed line). (B) When standing in the apparatus, there was little to no coherence in the Unlocked condition (top panel, grey line). The magnitude of coherence did not increase and also showed little to no coherence in the Locked condition (top panel, black line). The difference of coherence test confirmed that there was no significant difference in coherence between the Unlocked and Locked conditions (bottom panel).  94  Figure 5-5  Estimates of coherence pooled across the 9 participants who showed an increase in COP displacements following COM stabilization. (A) There were significant magnitudes of coherence in the seated voluntary contraction (top panel, solid lines) in the 15-30 Hz frequency range across all muscles recorded (LGAS-red, MGAS-blue, and SOL-green), and the DOC (bottom panel) illustrated that this magnitude was significantly greater than the magnitude of coherence in the seated relaxed trial (top panel, dashed line). (B) When standing in the apparatus, there was little to no coherence in the Unlocked condition (top panel, dashed lines). The magnitude of coherence did not increase and also showed little to no coherence in the Locked condition (top panel, solid lines). The difference of coherence test confirmed that there was no significant difference in coherence between the Unlocked and Locked conditions (bottom panel).  95  6 Chapter: Is exploratory behaviour observed in other postural tasks that do not involve whole body stability?  Traditional theories suggest that postural sway originates from the interaction between movements of the body (centre of mass, COM) and forces beneath the feet (centre of pressure, COP). The COP is commonly assumed to control or correct for deviations of the COM from equilibrium, and delays or errors in this control result in postural sway (F. Horak & MacPherson, 1996; Peterka, 2002; Prieto et al., 1993). However, recent evidence has shown that experimentally restricting postural sway leads to an unexpected increase in COP displacement (Carpenter et al., 2010), and this observation has persisted when participants are provided visual confirmation of stabilization (Murnaghan et al., 2011) or when they are provided an explicit verbal cue indicating how and when the body would be stabilized (Murnaghan et al., In Press). It has been argued that participants increase COP displacements under these conditions in an attempt to move the body and regain a certain level of afferent input, which is otherwise acquired through natural sway.  While the term postural control typically refers to controlling the position of the whole body relative to the gravitoinertial environment (F. Horak & MacPherson, 1996), maintaining a static position of a joint or limb in a variety of orientations has also been associated with the term postural control (Chew et al., 2008; Lacquaniti, 1992; S. Morrison & Newell, 1996; S. Morrison & Newell, 2000; S. Morrison & Newell, 2000). Irrespective of whether the term is applied to postural control of the whole body or a limb, the goal is very similar: to maintain a desired orientation or position. Interestingly, like whole body postural 96  control, attempts to maintain a static position of a limb result in small amplitude, higher frequency displacements of the limb that cannot be prevented. Although a large number of investigations have attempted to explain the origins of this behaviour, the mechanisms underlying these displacements are highly debated (Hagbarth & Young, 1979; Hallett, 1998; Joyce & Rack, 1974; Marsden, Meadows, Lange, & Watson, 1967). Many have argued for the combined or independent contributions of ballistocardiac impulses (Hallett, 1998; Marsden, Meadows, Lange, & Watson, 1969), the firing pattern of motor units (Allum, Dietz, & Freund, 1978), the tendency for a mechanical system to oscillate at a natural frequency (Joyce & Rack, 1974), the timing of stretch reflexes (A. M. Halliday & Redfearn, 1958; Joyce & Rack, 1974), as well as a central oscillator contained within the central nervous system (CNS) (McAuley & Marsden, 2000). While many consider the persistent movements that occur during static positioning to be irrelevant, or counter-productive, others have suggested that this behavior may be of functional importance and be used to facilitate other motor control behaviours (Goodman & Kelso, 1983), or indirectly serve as a means of acquiring information from the environment (Gibson, 1962; Riccio, 1993; Riley & Turvey, 2002; Stoffregen & Riccio, 1988). Therefore, it could be postulated that the movement observed when attempting to maintain a static limb position may actually be exploratory in nature and serve to maintain a certain level of afferent input to the CNS (Riccio, 1993; Riley et al., 1997), as has been proposed for the movements associated with normal postural sway (Carpenter et al., 2010; Murnaghan et al., 2011).  A preliminary study by Burgess (1989) provides indirect evidence of exploratory behaviour during an upper limb postural task. Participants were asked to maintain a steady 97  grip force against a transducer that was positioned on a surface with variable levels of friction. When trying to maintain a static and constant position in the low friction condition, small oscillations were observed. When friction was increased without subjects’ knowledge, increases in force were observed that would have moved the transducer significantly more than observed in the low friction condition. Based on these results, it was suggested that, when movement cues are available, force fluctuations are markedly reduced and participants are able to maintain a constant position (Burgess, 1989). Extending from these findings, it could be interpreted that when friction was increased, movement cues (which provided vital proprioceptive information) were prevented. As a result of this, the body may attempt to increase the magnitude of force in an attempt to maintain movement and generate a certain quantity and/or quality of sensory information. As such, the results from this study suggest that movement cues may be crucial for monitoring position in any type of postural task.  Based on the preliminary findings of Burgess (1989), the aim of the current experiment was to determine whether participants would attempt to generate movement cues when the arm is unknowingly stabilized during a task that requires participants to maintain a static position of a limb. To address this aim, participants were placed in a supine position with the arm pointing vertically and the wrist attached to a closed-loop pulley system described previously (Carpenter et al., 2010; Murnaghan et al., 2011) (Figure 6-1). We hypothesized that forces recorded following arm stabilization in the sagittal plane would predict angular accelerations larger than those measured when the arm was unrestricted and maintained in a static position. We also hypothesized, based on previous results observed during whole body postural control, that the increase in angular accelerations observed 98  following external stabilization would be greater when participants were provided visual feedback of the angular position of the arm.  6.1 Methods 6.1.1 Participants  Ten healthy young adults (5 females; mean ± sd for age = 24.4 ± 4.7 years; height = 173.7 ± 9.6 cm; weight = 70.2 ± 15.2 kg; arm length = 54.3 ± 4.9 cm) were recruited from the University of British Columbia student population. Each participant provided informed written consent, and the experimental protocol was approved by the Behavioural Research Ethics board at the University of British Columbia. All subjects were completely unaware of the goals of the experiment.  6.1.2  Apparatus  The apparatus used in the current experiment was similar to that described in Carpenter et al. (2010) and Murnaghan et al. (2011). Participants were asked to lie in a supine position on a solid support surface with the arm pointing vertically and the palm facing medially. Any flexion or extension at the wrist and/or elbow was prevented by applying a lightweight (<1kg) wooden splint to both joints, forcing all movement to occur about the shoulder. In addition, significant displacements of the scapula were prevented by using straps to secure the shoulder to the support surface. At the level of the wrist, the splint was attached to a closed-loop pulley system, allowing normal displacements of the arm unless the experimenter applied a brake that discretely locked the arm in place in the sagittal 99  plane without participant awareness. Participants also wore earplugs to reduce any noise within the testing area and blinders to prevent visual feedback of the limb or the apparatus (Figure 6-1).  6.1.3 Experimental protocol  All participants were fitted into the apparatus and asked to “keep the arm as still as possible” throughout the trials. Participants performed two ~5 minute trials and were asked to maintain the arm in a slight anterior position (~4 degrees from vertical). This position of the limb created a slight tonic activation in the shoulder flexor muscles, but required very little effort to maintain. During the first trial, participants performed the task with eyes closed. In the second trial, they performed the trial with eyes open and were provided real-time visual feedback of the sagittal plane angular displacements of the limb on a screen positioned at eye-level approximately 1 meter above the head. Although participants were unaware of stabilization, visual feedback or arm angular displacements provided visual confirmation of arm stabilization.  6.1.4 Measurements  Forces in the sagittal plane were measured at 1000 Hz using a force transducer (FT10, force displacement transducer, Grass Instrument Company, Quincy, MA) that was embedded in the splint and connected in series with the cable using aluminum wire. Raw data were amplified 100 times, and offline, raw voltages were converted to forces in Newtons. Conversion coefficients were based on calibrations performed with and without a tensor 100  preload equivalent to that applied during the experiments (5 Kg; the midpoint of the measurement range of the transducer). Forces were low pass filtered at 20 Hz and subsequently high pass filtered at 1 Hz to remove any drift from the signal. Once forces were obtained, the range and root mean square (RMS) were calculated. Kinematics were sampled at 100 Hz for the duration of each trial using an Optotrak three dimensional optical motion analysis system (Northern Digital Inc., Waterloo, Ontario, Canada) with infrared light emitting diodes (IRED) placed on the wrist, elbow, shoulder, support surface, and the cable. Kinematic data were low pass filtered at 20 Hz with a dual-pass Butterworth filter and used to calculate the cable and angular displacements of the arm in the sagittal plane. From the measured angular displacements, Fast Fourier Transform (FFT-based) differentiation (S. G. Johnson, 2011) was used to calculate angular accelerations (Labview, National Instruments Corporation, Austin, TX). Electromyographic (EMG) activity from anterior and posterior deltoid was recorded using surface electrodes (Telemyo 2400R G2, Noraxon, USA) at 1000 Hz, band-pass filtered between 10 and 500 Hz, and used to calculate RMS amplitudes.  Forward dynamics were used to determine whether forces in the Locked condition would elicit accelerations that exceeded, those measured in the Unlocked condition. In the Locked condition, torque was estimated as Tshoulder= Fx*d + mg, where the mass of the arm (m) is 0.050*total body mass (Winter 2005) and d is the vertical distance from the location of the force to the shoulder joint. As shown in Figure 6-2, the angular accelerations at the arm were calculated as α = Tshoulder/Ishoulder , where Ishoulder is the moment of inertia of the arm segment rotating about the shoulder joint. In this case, Ishoulder = m*(radius of gyration*segment length)2. The radius of gyration was drawn from anthropometric tables 101  (Winter 2005), and the segment length was defined as the distance in meters from the glenohumeral joint to the ulnar styloid (Winter 2005). All dependent variables (range of cable displacement, and the range, RMS and Mean Power Frequency (MPF) of angular accelerations) were calculated for each trial over the 120s periods in each of the Unlocked and Locked conditions. The 120s measurement periods began 135s prior to the beginning, and end, of the locking period respectively.  An important consideration in the current analysis is that the accelerations in the Unlocked and Locked conditions were derived from different sources of input. More specifically, Unlocked accelerations were calculated by differentiating three-dimensional motion capture data, while Locked accelerations were estimated using forces recorded from a force transducer. Because these two variables (kinematics versus force) may be susceptible to varying sources and magnitudes of noise, it was necessary to determine whether the noise from each of the measures could potentially lead to an over or under-estimation of actual accelerations. To eliminate this source of variability from the measures, we collected three trials on three subsequent days. In these trials, a pseudo-arm was placed in the apparatus and clamped at an angle 4 degrees from vertical, a condition where no changes in force or angular displacements would be expected. Using identical measurement procedures as described above, angular accelerations were acquired using two methods. First, angular displacements were calculated from kinematic data and differentiated using FFT-based differentiation to calculate angular accelerations. Then, using subject-specific anthropometric data, angular accelerations were predicted using measured forces and forward dynamics. The range and RMS of these accelerations were then calculated over 120s periods. All three trials 102  yielded very similar results, however the trial with the largest magnitude of calculated and predicted accelerations was used. The range and RMS calculated in this trial were subtracted from each participant’s trials, and these normalized values were used in further analyses.  6.2 Statistics  A 2 x 2 (lock x vision) repeated measures ANOVA was used on the range of cable displacements and RMS of arm angular displacements to ensure that stabilization of the arm was similar across conditions. A 2 x 2 (lock x vision) repeated measures ANOVA was also used to test whether forces measured in the Locked condition predicted RMS and range of angular accelerations that exceeded those calculated in the Unlocked condition, and whether any effects were altered when participants were provided visual feedback of arm angular displacements. In all cases, alpha level was set at 0.05 and Bonferroni corrections were applied to account for multiple comparisons.  6.3 Results The results of the current study showed that the apparatus was effective in minimizing even the small displacements of the arm during an upper limb postural task (Figure 6-3). There was a significant main effect of locking on the range of cable [F(1,9)=9.134, P= 0.014)] and arm angular displacements [F(1,9)=9.526, P = 0.013)]. When the lock was applied without participants’ knowledge by the experimenter, cable displacements were reduced from 11.2 mm (SE=4.32) to 0.19 mm (SE=0.03), respectively. Decreases in  103  linear displacements of the cable translated to a decrease in the angular displacements of the arm from 1.06 deg (SE=0.33) to 0.05 deg (SE=0.01).  The forces recorded following stabilization of the arm predicted greater accelerations than those recorded when the arm was freely moving (Figures 6-3 and 6-4). There was a significant interaction between locking and visual feedback on the RMS of angular accelerations [F(1,9)=5.498, P=0.044]. When participants were Locked, the RMS of angular accelerations was significantly greater than the accelerations calculated in the Unlocked condition, and this increase was larger when participants were provided visual feedback (Figures 6-3 and 6-4). From Unlocked to Locked, angular accelerations increased from 2.69 deg/s2 (SE=0.63) to 9.80 deg/s2 (SE=1.60) in the eyes closed condition, and from 1.89 deg/s2 (SE=0.23) to 13.5 deg/s2 (SE=2.35) when participants were provided visual feedback of arm angular displacements. The results also showed a significant main effect of locking on the range of angular accelerations [F(1,9)=48.189, P<0.001]. The range of angular accelerations predicted in the Locked condition was 5.7 times larger than the range of angular accelerations measured when the arm was Unlocked and freely moving (19.5 deg/s2 (SE=3.09) Unlocked; 111.3 deg/s2 (SE=13.87) Locked).  Power spectra of the accelerations illustrated changes in the dominant frequency components of the signal across Unlocked and Locked conditions. In the Unlocked condition, peaks were observed primarily at ~2-2.5 Hz, ~6 Hz and ~8-11 Hz with the dominant frequencies contained within ~6-8 or ~8-11 Hz. When participants were Locked, ~2-2.5 Hz became the dominant component of the signal, with some participants also showing some, 104  albeit reduced, power in the 6-8 Hz or 8-11 Hz components (Figure 6-3). This was characterized in the MPF of the signal where the results showed a significant main effect of locking on the MPF of angular acceleration [F(1,9)=76.675, P<0.001]. The MPF of accelerations in the Locked condition was 4 times smaller than that calculated when the arm was freely moving and decreased from 6.48 Hz (SE=0.41) to 2.30 Hz (SE=0.12) in the Unlocked and Locked conditions, respectively (Figure 6-4).  There were no significant main effects or interactions between locking and visual feedback on the RMS amplitude of anterior or posterior deltoid EMG activity (all P>0.05).  6.4 Discussion Traditional theories of whole body postural control generally assume the body acts as an inverted pendulum rotating about the ankle. It is believed that the goal of the CNS under these conditions is to maintain a static position of the body in space by using ground reaction forces (COP) to correct or control for displacements of the COM, and errors or delays in this control result in continuous movement or postural sway (F. Horak & MacPherson, 1996; Peterka, 2002; Prieto et al., 1993). Studies have consistently shown that when movements of the body are externally stabilized, contrary to what traditional theories would predict (F. Horak & MacPherson, 1996; Peterka, 2002; Prieto et al., 1993), COP displacements actually increase (Carpenter et al., 2010; Murnaghan et al., 2011). This increase has been suggested to reflect an attempt to move the body and maintain afferent input to the CNS. However, the question remained whether this behaviour was isolated to whole body postural control, or whether it also applied to postural control of a limb. 105  The results of the current study suggest this behaviour is in fact a more global phenomenon and may be observed in any postural task that requires individuals to maintain a static position of a body or limb. Confirming our first hypothesis, the results showed that forces recorded following arm stabilization predicted increases in the RMS and range of angular accelerations compared to when the arm was freely moving. This finding is consistent with the preliminary results reported by Burgess (1989), which showed that when friction was increased and the position of a force transducer was “stabilized”, participants generated forces which predicted displacements greater than those observed when the force transducer was freely moving in a low friction environment. In addition, the results support previous observations during whole body postural control of increased COP displacements following COM stabilization (Carpenter et al., 2010; Murnaghan et al., 2011).  As hypothesized, the increase in accelerations from Unlocked to Locked was larger when participants were provided visual feedback of arm angular position. This result parallels previous observations made during whole body postural control where increases in the RMS of COP displacements were larger when participants were provided visual confirmation of body stabilization (Murnaghan et al., 2011). As described in our previous study (Murnaghan et al., 2011), during the Locked condition there may be a mismatch between the actual and expected afferent feedback. In turn, this mismatch could have led to the development of sensory illusions, which might explain the increases in predicted accelerations during the Locked condition. However, because accurate visual information is known to reduce the potential role of sensory illusions (Lackner & Taublieb, 1984), and visual feedback did not lead to a decrease in predicted accelerations, it suggests that sensory 106  illusions were most likely not a contributing factor. While the results from this study cannot determine why predicted accelerations were larger in the Locked condition when participants were provided visual feedback, it could be speculated that the way the arm is controlled in the visual feedback condition differs from that during eyes closed, simply due to a change in available sources of afferent information (having proprioceptive and visual information in the feedback condition versus only proprioception in the eyes closed condition) (Sutton & Sykes, 1967).  Although it is believed that participants generate forces in both the eyes closed and visual feedback conditions in an attempt to generate continuous afferent input to the CNS, it could be argued that these forces are simply the result of increases in co-contraction around the shoulder joint. Some evidence has suggested that when individuals attempt to voluntarily reduce displacements of a limb by increasing voluntary muscle activity, it tends to result in an increase, rather than a decrease, in the amplitude of displacement (Carignan, Daneault, & Duval, 2009; McAuley & Marsden, 2000). However, the results of the current study suggest that this was not the case, given that there was no significant effect of locking or vision on the RMS of muscle activity from the anterior or posterior deltoid.  The results of the current study also showed that the MPF of accelerations was significantly decreased following stabilization. Studies that have investigated the small, involuntary displacements of the limb that occur when attempting to maintain a static position against a load (Chew et al., 2008; Joyce & Rack, 1974) have observed larger low frequency components that become more dominant following changes in the mechanical 107  properties of the limb. When participants were asked to maintain a static limb position and the stiffness of the system was increased, the contribution of lower frequency components to the total signal increased. However, these lower frequency components were thought to represent conscious voluntary attempts to keep the mean force and position of the limb constant (Chew et al., 2008; Joyce & Rack, 1974), and thus were generally disregarded. Interestingly, following stabilization of the limb (which could be considered a manipulation that increases stiffness) participants were unaware of any changes, yet still produced forces that predicted significantly larger, lower frequency accelerations of the limb. Rather than viewing these lower frequency components as voluntary movements that reveal feedback driven attempts to maintain force or position (Chew et al., 2008; Joyce & Rack, 1974), an involuntary change in the frequency components of the signal could reflect exploratory behaviour that serves to acquire sensory information (Riley & Clark, 2003).  Collectively, the results of the current study suggest that participants may attempt to generate movement during stabilization not only during whole body postural control (Carpenter et al., 2010; Murnaghan et al., 2011), but also during postural control of the arm. This supports the notion that movement in general may be used as an exploratory means of acquiring sensory information from the surrounding environment. Central to this idea, Riley and Turvey (2002), along with others (Riccio, 1993; Slifkin & Newell, 1999), have suggested that although various types of human behaviours are stable, they also exhibit movement and variability. These behaviours can withstand perturbations, be sustained over long periods of time, and are highly repeatable; yet they are also highly variable. In tasks where the goal is simply to maintain a position of the body or limb, it could be argued that the variability of 108  movement dynamics may actually provide as much, or more information regarding how the system is controlled (Slifkin & Newell, 1999). Not only could variability and movement be informative in terms of the underlying control processes but movement and variability observed in any type of task may be representative of exploratory behaviour that serves to acquire afferent information from the environment (Gibson, 1962; Riccio, 1993; Slifkin & Newell, 1999).  The interpretations of the results of the current study are in line with a large body of literature that has questioned our traditional perspectives on movement and variability (Riccio, 1993; Riley & Turvey, 2002; Riley & Clark, 2003; Slifkin & Newell, 1999; van Emmerik & van Wegen, 2002). Although movement and variability are generally thought to be representative of performance decrements and pathology (van Emmerik & van Wegen, 2002), as suggested in the current and previous studies (Carpenter et al., 2010; Murnaghan et al., 2011; Riccio, 1993; Riley & Turvey, 2002; Stoffregen & Riccio, 1988), many others have argued that movement and variability may be used in a functional manner by the CNS. This change in perspective has important implications for our understanding of how biological systems are controlled and therefore warrants significant consideration and scientific inquiry.  109  .Figure 6-1  Schematic of the setup used for the upper limb postural task. Participants were asked to lie in a supine position on a solid support surface with the arm pointing vertically and the palm facing medially. Any flexion or extension at the wrist and/or elbow was prevented by splinting both joints, forcing all movement to occur about the shoulder. At the level of the wrist, the splint was attached to a closed-loop pulley system that allowed normal displacements of the arm unless the experimenter applied a brake that discretely locked the arm in place in the sagittal plane. Forces in the sagittal plane were measured using a force transducer that was embedded in the splint and connected in series with the cable.  110  Figure 6-2  Diagram illustrating how angular accelerations that would be expected to occur if the arm were freely moving were calculated. Time-varying torque at the shoulder (Tshoulder) was calculated in the Locked condition. These measures of torque were then used to estimate the accelerations of the arm that would be expected if the arm was Unlocked and could move freely. Moment of inertia (Ishoulder) was calculated using anthropometrics as described in the text, and used to estimate the angular acceleration of the arm (α).  111  Figure 6-3  Accelerations and power spectra from a representative participant during a visual feedback trial in the Unlocked (left panels) and Locked (right panels) conditions. Plots of acceleration (top panels) illustrate the increased accelerations in the Locked compared to Unlocked condition. Plots of power spectra illustrate the shift to dominant lower frequency components (~2.5 Hz) in the Locked compared to Unlocked condition. Y-axes on graphs of power spectra have been optimized for visual purposes.  112  Figure 6-4  Mean ± SE for the range of cable displacements (top graph), RMS (middle graph) and MPF (bottom graph) of accelerations in the Unlocked (grey bars) and Locked (black bars) conditions when participants performed the trials with eyes closed and with visual feedback of arm angular displacements. There was a significant main effect of locking on the range of cable displacements (top panel) and MPF of accelerations (bottom panel), and a significant interaction between lock and vision on the RMS of accelerations (middle panel).  113  7 Chapter: General discussion  Postural sway is a behaviour observed during stance that traditionally has been assumed to be the product of general noise in the postural control system, or errors that develop when attempting to return the body to its equilibrium position. In a series of five studies, this thesis used a novel apparatus to test whether whole body posture is controlled in a negative feedback manner, where displacements of the COP are used to correct or control for displacements of the body or COM. In addition, this thesis attempted to provide insight into how postural sway is controlled or used by the CNS.  7.1 Summary of results from the thesis  The aim of Study 1 was to determine whether posture is controlled in a pure negative feedback manner, where COP displacements correct or control for displacements of the COM. Using a novel paradigm that allowed the COM to be stabilized or “locked” in the sagittal plane, it was hypothesized that, based on traditional theories of postural control (F. Horak & MacPherson, 1996; Peterka, 2002; Prieto et al., 1993), COP displacements would be reduced. Contrary to our original hypothesis it was observed that COP displacements actually increased when the body was externally stabilized. This finding suggests that changes in COP can occur independently from those of the body or COM and suggests that under normal stance conditions, the displacements of the body associated with postural sway may be exploratory and used as a means of stimulating the underlying sensory receptors.  114  While the results of Study 1 provided support for an exploratory role of postural sway, the possibility exists that increases in COP displacements following COM stabilization may not serve to acquire sensory information, but rather reflect the consequences of sensory illusions or motor drift. As such, Study 2 sought to replicate the results in Study 1, and to provide evidence against the possibility that the increases in COP following COM stabilization were simply the result of sensory illusions or motor drift. The results of Study 2 replicated our previous findings and found that COP displacements increased with COM stabilization. In addition, the results of Study 2 also confirmed that these increases were not artifacts of sensory illusions or motor drift, since increases were still observed when participants were provided visual confirmation of stabilization (COM feedback) and when they were provided real-time visual feedback of the COP and asked to maintain a mean position.  Study 3 extended the results from Studies 1 and 2 and investigated whether increases in COP with locking could be explained by internal models. In Studies 1 and 2, participants were completely unaware of COM stabilization. If posture is controlled using an internal model that predicts the dynamics of the task, then COM stabilization may have altered these dynamics, resulting in increased COP displacements that may reflect an attempt to adapt the internal model of the body during stance. In addition to replicating the results from Study 1, Study 3 showed that increases in COP displacements did not reflect an attempt to adapt the internal model of the body during stance. The results clearly indicated that even though participants were aware of COM stabilization and were achieving the task goal of standing still, increases in COP displacements of similar magnitude were still observed. This 115  observation provided further support for an exploratory role of postural sway and suggested that movement may be necessary to ensure adequate stimulation of sensory receptors.  Using corticomuscular coherence between measures of EEG and EMG of shank muscles, the results from Study 4 showed that increases in COP displacements during locking were most likely not generated by means of an increase in oscillatory behaviour from the motor cortex. Similar to Studies 2 and 3, the results of Study 4 replicated Study 1 and showed that COP displacements increased following COM stabilization in the majority of participants. The results also showed little to no coherence during unrestricted sway, replicating previous findings in the literature that have shown little cortical involvement under normal stance conditions (Luu, 2010; Masakado et al., 2008). Finally the results from Study 4 showed that, although participants showed clear corticomuscular coherence during sustained low level voluntary contractions, increases in cortical drive to the muscles (as characterized using CMC) could not explain the increases in COP displacements observed following stabilization.  The fifth and final Study used an upper limb postural task that required participants to maintain a static position of the limb to determine whether or not exploratory behaviour was specific to whole body postural control. When displacements of the arm were externally stabilized, participants showed significant fluctuations in horizontal forces compared to when the arm was unrestricted. These forces predicted accelerations that exceeded those measured in the Unlocked condition, suggesting that movement may be required even in other postural  116  motor control tasks. These results provide support for an exploratory role of movement beyond the realm of whole body postural control.  7.2 Thesis contributions to our understanding of the origins of postural sway One dominant theory in the literature proposes that postural sway of the body observed during stance is the passive consequence of various internal and/or external forces acting on the body. Analyzing the spectral properties of sway behaviour during stance, many researchers have attributed displacements of the body to the mechanical movements associated with respiration (Hunter & Kearney, 1981; Jeong, 1991), the beating of the heart (Soames & Atha, 1982), or the venous return of blood to the heart (Murray, Seireg, & Sepic, 1975). Some have also suggested that these displacements arise from various sources of noise including “intrinsic stochasticity” of perceptual motor processes (Slifkin & Newell, 1999) or “quasi-periodic spike noise” (Morasso & Schieppati, 1999).  Rather than assuming that a variety of internal and external forces act on the body and subsequently lead to the displacements of the body associated with normal postural sway, a second theory has proposed that participants actually generate displacements of the body during stance (Gatev et al., 1999). Using cross-correlations, it was observed that EMG activity was generated in advance of COP and COM displacements, suggesting that a central program and descending commands lead to the displacements of the body associated with postural sway.  117  The results of Studies 1-4 suggested that internal or external forces could not explain the observed increases in COP displacements. Following external stabilization of the COM, the mechanical displacements of the body that would have resulted from respiration or heart beat were reduced. As such, a concomitant decrease in COP displacements would have been expected following stabilization. Other factors including venous blood return (muscle pump) or intrinsic noise would have predicted no change in COP displacements following stabilization. Therefore, while each of these factors may contribute to the displacements of the body associated with postural sway under normal conditions, they cannot individually, or in combination explain why participants increase COP displacements following external stabilization of the COM.  Furthermore, while Gatev (1999) proposed that postural sway might be generated using a central program and descending motor commands, the results of Study 4 suggest that participants do not generate these movements (via increases in COP) at the level of the motor cortex. Little to no CMC was observed between measures of EEG and EMG from muscles of the lower leg when participants were swaying freely. Even under conditions where the body is externally stabilized, the results of Study 4 did not show any increases in CMC, suggesting that cortical drive is not used to increase postural sway even when it is absent. While there are a number of limitations to the coherence technique discussed in Study 4, the findings do suggest that postural sway is not driven by the cortex.  Collectively, the results from Studies 1-4 propose that, when displacements of the body are externally stabilized, participants generate COP displacements in an attempt to 118  move the body and ensure afferent information is delivered to the CNS. It is important to note that this thesis does not suggest that postural sway is necessarily generated in a feedforward manner under normal conditions. Following external stabilization, increases in COP displacements (Studies 1-4) and forces (Study 5) most likely occur because movement was significantly reduced. In these conditions (where there is little to no movement), there is likely a significant decrease in sensory receptor stimulation. Since sensory receptors prefer dynamic to static inputs (Gandevia, 1996; Johansson & Vallbo, 1983), individuals may need to produce movement in order to maintain afferent input. However, extrapolating from these results, under normal conditions, postural sway could be the product of a variety of factors, yet stimulate the underlying receptors in a similar manner.  7.3 Thesis contributions to our understanding of how postural sway is controlled or used by the CNS Many theories have also been proposed to explain how postural sway is controlled or used by the CNS. For example, while some suggest that the movements associated with postural sway must be controlled and reduced to prevent falls, others have suggested that they may be used in a functional manner by the CNS.  One theory described in the literature assumes that posture is controlled in a negative feedback manner. In this theory, it is suggested that afferent information arising from the displacements of the body that are associated with postural sway, is used in a feedback manner to generate corrective ground reaction forces (COP) that return the body to its equilibrium position (F. Horak & MacPherson, 1996; Prieto et al., 1993). Based on this 119  description, it is assumed that the goal of the CNS is always to maintain an equilibrium position of the body during stance and to minimize any deflections from this ideal position. Observations of increases in COP displacements in Studies 1-4 suggest that posture may not be controlled solely in this manner. If COP displacements were used only to correct or control for displacements of the body or COM, an equivalent reduction in COP displacements should have been observed following stabilization. However, the fact that increases in COP displacements were observed consistently across Studies 1-4 confirms that posture is not controlled in a pure negative feedback manner.  Other theories suggest that, rather than using afferent information in a negative feedback manner, the afferent information acquired from postural sway is received by the CNS, but ignored until the postural control system must implement feedback mechanisms (i.e. when the COG reaches the limits of stability) (J. J. Collins & De Luca, 1993). However, if, as suggested by Collins and Deluca (1993), afferent information associated with displacements of the body or COM was ignored until it reached a critical threshold, then the decreased COM displacements caused by external stabilization should not require any corrective COP displacements. In contrast, increases in COP displacements were consistently observed in Studies 1-4, providing evidence against the proposal that afferent information is ignored. Therefore, increases in COP displacements following stabilization suggest that afferent information may be monitored and used to provide the CNS with afferent information indicating where the body is positioned in space.  120  In accordance with this suggestion, further theories have suggested that rather than being ignored, afferent information acquired from postural sway is used and affords the CNS with sensory input. However, the notion that postural sway may be beneficial is supported by very little empirical evidence. Gatev (1999) suggested that humans generate sway behaviour in a feedforward manner and speculated that they may use sway as a means of gathering afferent information from the surrounding environment. Similarly, this theory has also been proposed by various researchers in the field of ecological psychology, where they focus on the perceptual benefits of movements associated with postural sway behaviour irrespective of its origin (Gibson, 1962; Riccio, 1993; Riley et al., 1997; Stoffregen & Riccio, 1988). In accordance with these researchers, this thesis proposes that when the body is freely moving, the CNS is continuously afforded sensory information indicating where the body is positioned in space. Following stabilization, it is proposed that increases in COP displacements reflect an attempt to move the body in order to regain afferent information and to ensure that a certain quality and quantity of afferent information is delivered to the CNS.  Theories explaining how posture is controlled often assume that the postural control system is unique and differs from control in other human behaviours. Despite an improved understanding, there is still a general lack of consensus regarding how the complex task of maintaining an upright and stable position of the body in space appears to be achieved in such a simplistic and automatic manner. The results from Study 5 suggest that whole body postural control may not be that different and may operate in a similar manner as the control of any task involving the maintenance of a static position, or postural control, of a body or a limb. During whole body postural control or upper limb postural control, increases in COP 121  displacements and predicted accelerations were both proposed to reflect an attempt to move the body or limb and regain afferent information. Interestingly, despite using different sensory systems in each task (there is a lack of vestibular involvement in the upper limb task), similar findings were observed. As such, it has been speculated that movement is required to attain afferent input from available sources during any postural task where the goal is to maintain a desired orientation or position of the body or limb.  Collectively, increases in COP displacements observed following external stabilization in Studies 1-4 have challenged a variety of theories that are proposed in the literature and used to explain the control or use of postural sway. The results of this thesis do not provide conclusive evidence of an exploratory role of postural sway under normal conditions. However, by challenging alternative explanations for increases in COP observed under conditions of external stabilization, the results provide further support for the theory previously proposed by other researchers (Gatev et al., 1999; Riccio, 1993; Riley et al., 1997). As put forward by these authors, and suggested throughout this thesis, independent of their origin, the movements of the body associated with normal postural sway may not differ from those observed during other postural tasks where the goal is to maintain a static position. This suggests that these movements could share similar functions and control processes. If this is the case, a great deal of insight could be gained regarding the role of postural sway and how posture is controlled. Using analysis, recording, and modeling techniques adopted from these investigations, new developments in our understanding of whole body postural control could be gained.  122  7.4 Evidence of exploratory behaviour in other tasks/systems The notion that postural sway may be beneficial and promote the delivery of sensory information to the CNS is not a completely novel interpretation. The concept that movement is required in order to stimulate the underlying sensory receptors has been suggested and established in a variety of other motor tasks and systems. In fact, movement in other tasks/systems is thought to be a critical method of ensuring that sensory information is received or produced (Deschênes et al., 2012; Gibson, 1962; Martinez-Conde, Macknik, Troncoso, & Hubel, 2009; Riccio, 1993). Throughout this thesis, examples of such behaviours have been briefly discussed and used to support the interpretation of increases in COP displacements or horizontal forces following stabilization: that the movement associated with these behaviours in whole body (Studies 1-4) or upper limb postural control (Study 5) under normal conditions may serve to acquire a certain quantity and/or quality of sensory information.  One system which clearly exemplifies the importance of movement in acquiring or maintaining incoming sensory information is the visual system. In fact, Martinez-Conde et al. (2006) have described the visual system as having a “built in paradox.” Interestingly, while we need to fixate the eye in order to obtain details from the visual environment, if we were to perfectly fixate the eye, then the entire visual scene would fade from view as a result of neural adaptation to the constant stimuli. As such, in order to ‘see,’ humans must produce microsaccades (small, involuntary movements of the eye) in order to continuously stimulate the underlying receptors and to ensure that an image is maintained on the retina during fixation (Ditchburn & Ginsborg, 1952; Ratliff & Riggs, 1950; Riggs et al., 1953). As 123  described throughout this thesis, it is postulated that this behaviour in the visual system can be likened to normal postural sway. In fact, other researchers have recognized the parallels between these involuntary behaviours and have even employed the same analysis techniques to characterize their contributions to the CNS (J. J. Collins & De Luca, 1993; Engbert & Kliegl, 2004). Using random walk analysis, Engbert & Kliegl (2011) suggested, as was described for postural sway, that on short time scales microsaccades contained open loop processes which maintain a certain level of incoming sensory information and counteract retinal adaptation.  The olfactory system provides another interesting example of a system that modulates its activity based on the availability of sensory information. As described by Johnson et al. (2003), “most mammalian sensory systems are supported by dedicated sensory-motor mechanisms,” and the mechanism used in the olfactory system is the sniff. Just as the eyes actively accommodate vision using microsaccades and other behaviours (Engbert & Kliegl, 2004; Martinez-Conde et al., 2006), or the ears of bats and cats are moved to accommodate audition (Jen & Sun, 1984; Populin & Yin, 1998), the olfactory system can be modulated involuntarily to accommodate smell. Similar to what has been proposed throughout this thesis, evidence from the olfactory system suggests that the frequency and amplitude of a sniff is modulated in accordance with the concentrations of an odorant; if there is less odor we will increase the magnitude and frequency of the sniff (Laing, 1983; Sobel et al., 2001; Walker et al., 2001).  124  In line with the notion that we acquire sensory information from the environment, Sasaki et al. (1995) have proposed that during planned actions, humans involuntarily make small sub-movements or “micro-slips” (Sasaki, Mishima et al. 1995). While these submovements were first noticed in behavioural psychology (e.g., Norman, 1981; Reason, 1989; c.f. (Ogai & Ikegami, 2008)), they were named “microslips” and interpreted as a form of environmental exploration by ecological psychologists (Gibson, 1966; Ogai & Ikegami, 2008). This thesis has repeatedly suggested that postural sway may not represent errors in the desired trajectory of the body during stance. Similarly, these “slips” are not believed to represent errors in the trajectory of the intended movement. Rather, they are believed to represent independent, involuntary actions that serve to “actively perceive” the environment (Ikegami, 2007).  While microsaccades and microslips refer to involuntary forms of “exploration”, there is also evidence in the literature of voluntary forms of environmental exploration. The concept of “active touch” has been a topic of debate in psychology for decades. J.J. Gibson (1962) heavily disputed the concept that touch is a passive or receptive input channel to the central nervous system. His philosophy was that touch was more often an exploratory, rather than a receptive sense and suggested that when a person touches something with their fingers they produce the stimulation. More specifically, he believed that variations in skin stimulation are caused by variation in an individual’s motor activity (Gibson, 1962). This ecological psychology perspective is also comparable to that used to describe whisking behaviour of the rat. Since rats are known to have very poor visual acuity (Deschênes et al., 2012). A large body of research has determined that these animals actually explore their 125  immediate environment by sweeping their whisker-like vibrissae across various surfaces (Berg & Kleinfeld, 2003; Diamond, von Heimendahl, Knutsen, Kleinfeld, & Ahissar, 2008; Kleinfeld, Berg, & O'Connor, 1999). Analogous to the Gibsonian theory of active touch, the information flow of afferent information to the brain in these animals is believed to be shaped by their whisking interactions with the environment.  As proposed in all of these other mammalian systems, increases in COP displacements and predicted accelerations observed following stabilization in Studies 1-5 have been proposed to reflect an exploratory attempt to acquire sensory information from the surrounding environment. In light of these results, it is proposed that movements of the body or limb observed under normal conditions may provide the CNS with afferent information regarding where the body or limb is positioned in space. If this is the case, these behaviours may be considered to provide a similar function as those proposed in all of these other systems.  7.5 Clinical Implications of an exploratory role of postural sway  The combined results of this thesis have important clinical implications. The progression from Studies 1 through 5 has yielded results that challenge traditional theories of how posture is controlled and suggest an exploratory role of postural sway. The exploratory hypothesis of postural sway questions the basis of current clinical practices for treating balance deficits associated with age and disease. For example, as described in Study 1, rather than viewing increases in the magnitude of postural sway as indicative of a failing postural control system that is the consequence of ageing or neurological disease, it could be 126  considered a natural adaptation employed by the CNS to ensure a certain quality and/or quantity of afferent information is maintained despite the changes in nerve conduction velocities (Verdú, Ceballos, Vilches, & Navarro, 2000), reduced receptor sensitivities (Kenshalo, 1986), etc. in these populations. Similarly, when we remove or alter afferent information from one source (i.e. eyes closed), increases in postural sway are believed to represent “poorer balance” or a loss of neuromuscular control (Nashner et al., 1982). However, based on the exploratory hypothesis, this increase in postural sway may simply reflect an attempt to regain a certain quality and/or quantity of sensory information from any available sources. Alternatively, this increase could reflect an attempt to move the body at an amplitude and/or frequency, which preferentially stimulates receptors from the system that is missing or altered. With a simple paradigm shift in the way we believe posture is controlled, and the role of postural sway, there are drastic differences in the way in which we interpret changes in clinical measures.  A significant concern that arises when we interpret increases in postural sway as a means of acquiring additional afferent information is that this increase will inevitably result in an increased risk of falls. However, there is a misconception that increases in postural sway are large enough to result in a fall. In a host of literature, increases in postural sway have been correlated with an increased incidence of falls (Overstall et al. 1977; Lord & Dayhew, 2001). However, it is important to recognize that this link is supported by correlational, rather than causative evidence, and that there is also other literature that has found no link between these two events (Fernie, Gryfe, Holliday, & Llewellyn, 1982). In fact, the magnitude of postural sway under normal conditions represents only a very small 127  percentage of the available base of support (Duarte & Freitas, 2010), making it highly unlikely that increases in postural sway would be the sole cause of an individual exceeding the limits of stability.  7.6 Future directions The major contribution of this thesis to the field of postural control is that the postural control system does not act as a pure negative feedback system, as traditional theories would suggest. Instead, the results have suggested that the movement associated with postural sway may be exploratory and serve to acquire a certain quantity and quality of sensory information. Furthermore, it has been suggested that movement, even in other postural control tasks, may be functional and ensure delivery of afferent information to the central nervous system. Although many alternative explanations for the observed increases in displacement/force have been discounted throughout this thesis, there are many questions that remain to be answered.  First, this thesis has proposed that increases in COP/force observed following stabilization reflect an attempt of the CNS to acquire a larger quality and/or quantity of sensory information. However, evidence of increased quantity and/or quality of sensory information being delivered to spinal or supraspinal centres has not been supported experimentally. Given that the results of this thesis question clinical practices in postural control, it is imperative that future work is focused on measuring the increases in sensory information that are gained with increases in COP/force. Within the same paradigm, increases in somatosensory evoked potentials may provide some indication of increased 128  delivery of afferent information to the cortex. Although it would be unclear whether increased delivery of afferent information was being used in a functional manner, it would suggest that this may be the case (Davis et al., 2011).  Second, the results of Study 4 have suggested that increases in COP are not the consequence of increased oscillatory drive from the cortex to the muscles recorded in the lower limb. As such, the question remains as to the origin of these increases. As discussed in Study 4, the cortex could still potentially produce increases in COP following stabilization in an attempt to regain a certain quantity and/or quality of sensory information in a manner that was not captured by the analysis techniques described in this thesis. However, collectively, the lack of CMC during locking in Study 4, the fact that increases in COP were observed when participants were unaware (Studies 1, 2 and 4) or when they were aware (Study 3) of stabilization, as well as evidence of a subcortical origin of similar behaviours in the rat (Berg & Kleinfeld, 2003), suggests that emphasis on subcortical structures is warranted and a promising area within which to focus further investigations.  Finally, the results suggest that in the absence of movement, humans generate COP/forces that are potentially an attempt to move the body and regain sensory information. Based on this, it has been suggested that under normal conditions, the natural sway of the body during stance acts to stimulate sensory receptors. Future work should focus on whether postural sway reflects an active and centrally-generated process that serves to acquire sensory information (Gatev et al., 1999), or whether it reflects a passive consequence of various  129  factors (i.e. breathing, respiration, etc) that could potentially serve the same purpose (J. J. Collins & De Luca, 1993).  7.7 Conclusion  In conclusion, the collective results from this thesis have challenged traditional assumptions of how posture is controlled and provided support for an alternative and potentially crucial role for postural sway. Firstly, the results from this thesis have shown that whole body posture is not controlled in a pure negative feedback manner, where displacements of the COP serve only to correct or control for displacements of the COM. Secondly, by challenging alternative explanations, the results from this thesis have suggested that movement associated with postural sway may actually be necessary and used as a means of acquiring sensory information regarding the position of the body in space. Extending the investigation beyond whole body postural control, the progression of this thesis has suggested that movement may be used in a functional manner during whole body postural control, but that this also may be a more global phenomenon, which is vital in any static positioning task, as is suggested in a host of other animal behaviours.  130  References Allum, J. H., Dietz, V., & Freund, H. J. (1978). Neuronal mechanisms underlying physiological tremor. Journal of Neurophysiology, 41(3), 557-571. Amjad, A. M., Breeze, P., Conway, B. A., Halliday, D. M., & Rosenberg, J. R. (1989). A framework for the analysis of neuronal networks. Prog Brain Res, 80, 243-55; discussion 239-42. Asai, H., Fujiwara, K., Toyama, H., Yamashina, T., Tachino, K., & Nara, I. (1992). The influence of foot soles cooling on standing postural control analyzed by tracking the center of foot pressure. In M. Woollacoot, & F. Horak (Eds.), Posture and gait: Control mechanisms. II. (pp. 151–154). Eugene, OR, USA: University of Oregon Books. Baker, S. N. (2000). ‘Pooled coherence’ can overestimate the significance of coupling in the presence of inter-experiment variability. Journal of Neuroscience Methods, 96(2), 171172. Berg, R. W., & Kleinfeld, D. (2003). Rhythmic whisking by rat: Retraction as well as protraction of the vibrissae is under active muscular control. J Neurophysiol, 89(1), 10417. Bottaro, A., Casadio, M., Morasso, P. G., & Sanguineti, V. (2005). Body sway during quiet standing: Is it the residual chattering of an intermittent stabilization process? Hum Mov Sci, 24(4), 588-615.  131  Brookhart, J. M., Parmeggiani, P. L., Petersen, W. A., & Stone, S. A. (1965). Postural stability in the dog. Am J Physiol, 208, 1047-57. Burgess, P. R. (1989). Movement cues are necessary for load stabilization against low friction. Society for Neuroscience Annual Meeting Abstracts, 15 173. Carignan, B., Daneault, J. F., & Duval, C. (2009). The amplitude of physiological tremor can be voluntarily modulated. Experimental Brain Research.Experimentelle Hirnforschung.Experimentation Cerebrale, 194(2), 309-316. Carpenter, M. G., Frank, J. S., Winter, D. A., & Peysar, G. W. (2001). Sampling duration effects on centre of pressure summary measures. Gait Posture, 13(1), 35-40. Carpenter, M. G., Murnaghan, C. D., & Inglis, J. T. (2010). Shifting the balance: Evidence of an exploratory role for postural sway. Neuroscience, 171(1), 196-204. Carroll, J. P., & Freedman, W. (1993). Nonstationary properties of postural sway. J Biomech, 26(4-5), 409-16. Chew, J. Z., Gandevia, S. C., & Fitzpatrick, R. C. (2008). Postural control at the human wrist. J Physiol, 586(5), 1265-75. Claydon, V. E., & Hainsworth, R. (2005). Increased postural sway in control subjects with poor orthostatic tolerance. J Am Coll Cardiol, 46(7), 1309-13.  132  Clayton, H. M., Bialski, D. E., Lanovaz, J. L., & Mullineaux, D. R. (2003). Assessment of the reliability of a technique to measure postural sway in horses. Am J Vet Res, 64(11), 1354-9. Cole, J. D., & Sedgwick, E. M. (1992). The perceptions of force and of movement in a man without large myelinated sensory afferents below the neck. The Journal of Physiology, 449(1), 503-515. Collins, D. F., Refshauge, K. M., Todd, G., & Gandevia, S. C. (2005). Cutaneous receptors contribute to kinesthesia at the index finger, elbow, and knee. J Neurophysiol, 94(3), 1699-706. Collins, J. J., & De Luca, C. J. (1993). Open-loop and closed-loop control of posture: A random-walk analysis of center-of-pressure trajectories. Exp Brain Res, 95(2), 308-18. Dakin, C. J., Luu, B. L., van den Doel, K., Inglis, J. T., & Blouin, J. (2010). Frequencyspecific modulation of vestibular-evoked sway responses in humans. Journal of Neurophysiology, 103(2), 1048-1056. Davis, J. R., Horslen, B. C., Nishikawa, K., Fukushima, K., Chua, R., Inglis, J. T., & Carpenter, M. G. (2011). Human proprioceptive adaptations during states of heightinduced fear and anxiety. Journal of Neurophysiology, 106(6), 3082-3090. Day, B. L., & Fitzpatrick, R. C. (2005). The vestibular system. Curr Biol, 15(15), R583-6. Deliagina, T. G., Orlovsky, G. N., Zelenin, P. V., & Beloozerova, I. N. (2006). Neural bases of postural control. Physiology (Bethesda), 21, 216-25. 133  Deschênes, M., Moore, J., & Kleinfeld, D. (2012). Sniffing and whisking in rodents. Current Opinion in Neurobiology, 22(2), 243-250. Diamond, M. E., von Heimendahl, M., Knutsen, P. M., Kleinfeld, D., & Ahissar, E. (2008). 'Where' and 'what' in the whisker sensorimotor system. Nature Reviews.Neuroscience, 9(8), 601-612. Dietz, V. (1992). Human neuronal control of automatic functional movements: Interaction between central programs and afferent input. Physiol Rev, 72(1), 33-69. Dietz, V., Schubert, M., & Trippel, M. (1992). Visually induced destabilization of human stance: Neuronal control of leg muscles. Neuroreport, 3(5), 449-52. Ditchburn, R. W., & Ginsborg, B. L. (1952). Vision with a stabilized retinal image. Nature, 170(4314), 36-7. Duarte, M., & Freitas, S. M. (2010). Revision of posturography based on force plate for balance evaluation. Revista Brasileira De Fisioterapia (Sao Carlos (Sao Paulo, Brazil)), 14(3), 183-192. Dum, R. P., & Strick, P. L. (1996). Spinal cord terminations of the medial wall motor areas in macaque monkeys. The Journal of Neuroscience : The Official Journal of the Society for Neuroscience, 16(20), 6513-6525. Engbert, R., & Kliegl, R. (2004). Microsaccades keep the eyes' balance during fixation. Psychol Sci, 15(6), 431-6.  134  Engbert, R., Mergenthaler, K., Sinn, P., & Pikovsky, A. (2011). An integrated model of fixational eye movements and microsaccades. Proceedings of the National Academy of Sciences of the United States of America, 108(39), E765-70. Enoka, R. M. (1994). Neuromechanical basis of kinesiology (2nd ed.). Champaign, IL, England: Human Kinetics Publishers. Eun Jung Hwang and,Reza Shadmehr. (2005). Internal models of limb dynamics and the encoding of limb state. Journal of Neural Engineering, 2(3), 266. Fearing, F. S. (1924). The factors influencing static equilibrium. an experimental study of the effects of practice upon amount and direction of sway. Journal of Comparative Psychology, 4(2), 163-183. Fernie, G. R., Gryfe, C. I., Holliday, P. J., & Llewellyn, A. (1982). The relationship of postural sway in standing to the incidence of falls in geriatric subjects. Age Ageing, 11(1), 11-6. Fitzpatrick, R., & McCloskey, D. I. (1994). Proprioceptive, visual and vestibular thresholds for the perception of sway during standing in humans. J Physiol, 478 ( Pt 1), 173-86. Fitzpatrick, R. C., Taylor, J. L., & McCloskey, D. I. (1992). Ankle stiffness of standing humans in response to imperceptible perturbation: Reflex and task-dependent components. J Physiol, 454, 533-47. Gage, W. H., Winter, D. A., Frank, J. S., & Adkin, A. L. (2004). Kinematic and kinetic validity of the inverted pendulum model in quiet standing. Gait Posture, 19(2), 124-32. 135  Gagey, P. (1992). History of posturology. Unpublished manuscript. Gandevia, S. C. (1996). Kinesthesia: Roles for afferent signals and motor commands. In S. J. Rowell LB (Ed.), Handbook of physiology (pp. 128–172). New York: Oxford University Press. Gatev, P., Thomas, S., Kepple, T., & Hallett, M. (1999). Feedforward ankle strategy of balance during quiet stance in adults. J Physiol, 514 ( Pt 3), 915-28. Gerloff, C., Braun, C., Staudt, M., Hegner, Y. L., Dichgans, J., & Krageloh-Mann, I. (2006). Coherent corticomuscular oscillations originate from primary motor cortex: Evidence from patients with early brain lesions. Hum Brain Mapp, 27(10), 789-98. Geyer, S., Matelli, M., Luppino, G., & Zilles, K. (2000). Functional neuroanatomy of the primate isocortical motor system. Anatomy and Embryology, 202(6), 443-474. Gibson, J. J. (1962). Observations on active touch. Psychol Rev, 69, 477-91. Gibson, J. J. (1966). The problem of temporal order in stimulation and perception. The Journal of Psychology, 62(2), 141-149. Goodman, D., & Kelso, J. A. (1983). Exploring the functional significance of physiological tremor: A biospectroscopic approach. Exp Brain Res, 49(3), 419-31. Gottlieb, G. L. (1994). The generation of the efferent command and the importance of joint compliance in fast elbow movements. Exp Brain Res, 97(3), 545-50.  136  Gurfinkel, V. S. (1973). Muscle afferentation and postural control in man. Agressologie, 14(Spec No C), 1-8. Gurfinkel, V. S., Lipshits, M. I., & Popov, K. E. (1974). [Is the stretch reflex a basic mechanism in the system of regulation of human vertical posture?]. Biofizika, 19(4), 744-8. Gurfinkel, V. S., & Osovets, S. M. (1972). [Equilibrium dynamics of human vertical posture]. Biofizika, 17(3), 478-86. Hagbarth, K., & Young, R. (1979). Participation of the stretch reflex in human physiological tremor. Brain, 102(3), 509-526. Hallett, M. (1998). Overview of human tremor physiology. Movement Disorders : Official Journal of the Movement Disorder Society, 13 Suppl 3, 43-48. Halliday, A. M., & Redfearn, J. W. T. (1958). Finger tremor in tabetic patients and its bearing on the mechanism producing the rhythm of the physiological tremor. Journal of Neurology, Neurosurgery & Psychiatry, 21(2), 101-108. Halliday, D. M., & Rosenberg, J. R. (2000). On the application, estimation and interpretation of coherence and pooled coherence. Journal of Neuroscience Methods, 100(1–2), 173174. Halliday, D. M., Rosenberg, J. R., Amjad, A. M., Breeze, P., Conway, B. A., & Farmer, S. F. (1995). A framework for the analysis of mixed time series/point process data--theory  137  and application to the study of physiological tremor, single motor unit discharges and electromyograms. Prog Biophys Mol Biol, 64(2-3), 237-78. Hellebrandt, F. A. &. F.,E.B. (1943). Physiological study of the vertical stance in man. Physiological Reviews, 23, 220-255. Hellebrandt, F. A., & Brogdon, E. (1938). The hydrostatic effect of gravity on the circulation in supported, unsupported and suspended postures. The American Journal of Physiology, 123, 95. Horak, F. B. (1996). Adaptation of automatic postural responses. Acquisition of motor behavior in vertebrates (pp. 57-85). Cambridge, Mass.: The MIT press. Horak, F., & MacPherson, J. (1996). Postural orientation and equilibrium. In S. J. Rowell LB (Ed.), Handbook of physiology (). New York: Oxford University Press. Hunter, I. W., & Kearney, R. E. (1981). Respiratory components of human postural sway. Neurosci Lett, 25(2), 155-9. Ikegami, T. (2007). Simulating active perception and mental imagery with embodied chaotic intinerancy. Journal of Consciousness Studies, 14(7), 111-125. Imamizu, H., Sugimoto, N., Osu, R., Tsutsui, K., Sugiyama, K., Wada, Y., & Kawato, M. (2007). Explicit contextual information selectively contributes to predictive switching of internal models. Exp Brain Res, 181(3), 395-408.  138  Ishida, A., & Miyazaki, S. (1987). Maximum likelihood identification of a posture control system. IEEE Trans Biomed Eng, 34(1), 1-5. Jacobs, J. V., & Horak, F. B. (2007). Cortical control of postural responses. J Neural Transm, 114(10), 1339-48. Jeka, J., Kiemel, T., Creath, R., Horak, F., & Peterka, R. (2004). Controlling human upright posture: Velocity information is more accurate than position or acceleration. J Neurophysiol, 92(4), 2368-79. Jen, P. H., & Sun, X. (1984). Pinna orientation determines the maximal directional sensitivity of bat auditory neurons. Brain Research, 301(1), 157-161. Jeong, B. Y. (1991). Respiration effect on standing balance. Arch Phys Med Rehabil, 72(9), 642-5. Johansson, R., Magnusson, M., & Akesson, M. (1988). Identification of human postural dynamics. IEEE Trans Biomed Eng, 35(10), 858-69. Johansson, R., & Vallbo, A. (1983). Tactile sensory coding in the glabrous skin of the human hand. Trends in Neuroscience, 6, 27-32. Johnson, S. G. (2011). Notes on FFT-based differentiation. Retrieved 12, 2012, from http://math.mit.edu/~stevenj/fft-deriv.pdf Johnson, B. N., Mainland, J. D., & Sobel, N. (2003). Rapid olfactory processing implicates subcortical control of an olfactomotor system. J Neurophysiol, 90(2), 1084-94. 139  Joseph, J., & Nightingale, A. (1952). [Electromyography of muscles of posture: Leg muscles in males]. J Physiol, 117(4), 484-91. Joyce, G. C., & Rack, P. M. (1974). The effects of load and force on tremor at the normal human elbow joint. J Physiol, 240(2), 375-96. Kandel, E. R., Schwartz, J. H., & Jessell, T. M. (Eds.). (2000). Principles of neural science. New York, New York: McGraw-Hill, Health Professions Division. Kawato, M. (1999). Internal models for motor control and trajectory planning. Curr Opin Neurobiol, 9(6), 718-27. Kelly, L. A., Kuitunen, S., Racinais, S., & Cresswell, A. G. (2012). Recruitment of the plantar intrinsic foot muscles with increasing postural demand. Clinical Biomechanics, 27(1), 46-51. Kelton, I. W., & Wright, R. D. (1949). The mechanism of easy standing by man. Australian Journal of Experimental Biology and Medicine, 27, 505-515. Kenshalo, D. R. (1986). Somesthetic sensitivity in young and elderly humans. Journal of Gerontology, 41(6), 732-742. Kiemel, T., Zhang, Y., & Jeka, J. J. (2011). Identification of neural feedback for upright stance in humans: Stabilization rather than sway minimization. The Journal of Neuroscience, 31(42), 15144-15153.  140  Kilner, J. M., Baker, S. N., Salenius, S., Hari, R., & Lemon, R. N. (2000). Human cortical muscle coherence is directly related to specific motor parameters. The Journal of Neuroscience, 20(23), 8838-8845. Kleinfeld, D., Berg, R. W., & O'Connor, S. M. (1999). Anatomical loops and their electrical dynamics in relation to whisking by rat. Somatosens Mot Res, 16(2), 69-88. Lackner, J. R., & Taublieb, A. B. (1984). Influence of vision on vibration-induced illusions of limb movement. Exp Neurol, 85(1), 97-106. Lacquaniti, F. (1992). Automatic control of limb movement and posture. Current Opinion in Neurobiology, 2(6), 807-814. Laing, D. G. (1983). Natural sniffing gives optimum odour perception for humans. Perception, 12(2), 99-117. Lee, D. N. (1980). The optic flow field: The foundation of vision. Philos Trans R Soc Lond B Biol Sci, 290(1038), 169-79. Lestienne, F. G., & Gurfinkel, V. S. (1988). Postural control in weightlessness: A dual process underlying adaptation to an unusual environment. Trends Neurosci, 11(8), 35963. Loram, I. D., Gawthrop, P. J., & Lakie, M. (2006). The frequency of human, manual adjustments in balancing an inverted pendulum is constrained by intrinsic physiological factors. J Physiol, 577(Pt 1), 417-32.  141  Loram, I. D., Kelly, S. M., & Lakie, M. (2001). Human balancing of an inverted pendulum: Is sway size controlled by ankle impedance? J Physiol, 532(Pt 3), 879-91. Loram, I. D., & Lakie, M. (2002). Human balancing of an inverted pendulum: Position control by small, ballistic-like, throw and catch movements. J Physiol, 540(Pt 3), 111124. Loram, I. D., Lakie, M., Di Giulio, I., & Maganaris, C. N. (2009). The consequences of short-range stiffness and fluctuating muscle activity for proprioception of postural joint rotations: The relevance to human standing. J Neurophysiol, 102(1), 460-74. Loram, I. D., Maganaris, C. N., & Lakie, M. (2004). Paradoxical muscle movement in human standing. J Physiol, 556(Pt 3), 683-9. Loram, I. D., Maganaris, C. N., & Lakie, M. (2005). Active, non-spring-like muscle movements in human postural sway: How might paradoxical changes in muscle length be produced? J Physiol, 564(Pt 1), 281-93. Luu, B. (2010). Perception, perfusion & posture. University of New South Wales). PhD Maki, B. E., & McIlroy, W. E. (2007). Cognitive demands and cortical control of human balance-recovery reactions. J Neural Transm, 114(10), 1279-96. Marsden, C. D., Meadows, J. C., Lange, G. W., & Watson, R. S. (1967). Effect of deafferentation on human physiological tremor. Lancet, 2(7518), 700-702.  142  Marsden, C. D., Meadows, J. C., Lange, G. W., & Watson, R. S. (1969). The role of the ballistocardiac impulse in the genesis of physiological tremor. Brain, 92(3), 647-662. Martinez-Conde, S., Macknik, S. L., Troncoso, X. G., & Dyar, T. A. (2006). Microsaccades counteract visual fading during fixation. Neuron, 49(2), 297-305. Martinez-Conde, S., Macknik, S. L., Troncoso, X. G., & Hubel, D. H. (2009). Microsaccades: A neurophysiological analysis. Trends Neurosci, 32(9), 463-75. Masakado, Y., Ushiba, J., Tsutsumi, N., Takahashi, Y., Tomita, Y., Kimura, A., & Liu, M. (2008). EEG-EMG coherence changes in postural tasks. Electromyogr Clin Neurophysiol, 48(1), 27-33. Massion, J. (1992). Movement, posture and equilibrium: Interaction and coordination. Prog Neurobiol, 38(1), 35-56. Massion, J. (1994). Postural control system. Curr Opin Neurobiol, 4(6), 877-87. Massion, J. (1998). Postural control systems in developmental perspective. Neurosci Biobehav Rev, 22(4), 465-72. Maurer, C., & Peterka, R. J. (2005). A new interpretation of spontaneous sway measures based on a simple model of human postural control. J Neurophysiol, 93(1), 189-200. Mazzoni, P., & Krakauer, J. W.An implicit plan overrides an explicit strategy during visuomotor adaptation. The Journal of Neuroscience, 26(14), 3642-3645.  143  McAuley, J. H., & Marsden, C. D. (2000). Physiological and pathological tremors and rhythmic central motor control. Brain, 123(8), 1545-1567. Mima, T., & Hallett, M. (1999). Corticomuscular coherence: A review. J Clin Neurophysiol, 16(6), 501-11. Mittelstaedt, H. (1983). A new solution to the problem of the subjective vertical. Naturwissenschaften, 70(6), 272-81. Morasso, P. G., Baratto, L., Capra, R., & Spada, G. (1999). Internal models in the control of posture. Neural Networks, 12(7–8), 1173-1180. Morasso, P. G., & Sanguineti, V. (2002). Ankle muscle stiffness alone cannot stabilize balance during quiet standing. J Neurophysiol, 88(4), 2157-62. Morasso, P. G., & Schieppati, M. (1999). Can muscle stiffness alone stabilize upright standing? J Neurophysiol, 82(3), 1622-6. Morrison, S., & Newell, K. M. (1996). Inter- and intra-limb coordination in arm tremor. Experimental Brain Research.Experimentelle Hirnforschung.Experimentation Cerebrale, 110(3), 455-464. Morrison, S., & Newell, K. M. (2000). Postural and resting tremor in the upper limb. Clinical Neurophysiology, 111(4), 651-663. Murnaghan, C. D., Horslen, B. C., Inglis, J. T., & Carpenter, M. G. (2011). Exploratory behavior during stance persists with visual feedback. Neuroscience, 195, 54-9. 144  Murnaghan, C. D., Squair, J. W., Chua, R., Inglis, J. T., & Carpenter, M. G. (In Press). Are increases in COP variability observed when participants are provided explicit verbal cues prior to COM stabilization? Gait and Posture Murray, M. P., Seireg, A. A., & Sepic, S. B. (1975). Normal postural stability and steadiness: Quantitative assessment. J Bone Joint Surg Am, 57(4), 510-6. Nardone, A., Tarantola, J., Miscio, G., Pisano, F., Schenone, A., & Schieppati, M. (2000). Loss of large-diameter spindle afferent fibres is not detrimental to the control of body sway during upright stance: Evidence from neuropathy. Exp Brain Res, 135(2), 155-62. Nashner, L. M. (1976). Adapting reflexes controlling the human posture. Exp Brain Res, 26(1), 59-72. Nashner, L. M., Black, F. O., & Wall, C.,3rd. (1982). Adaptation to altered support and visual conditions during stance: Patients with vestibular deficits. J Neurosci, 2(5), 53644. Neilson, P. D., Neilson, M. D., & O'Dwyer, N. J. (1988). Internal models and intermittency: A theoretical account of human tracking behavior. Biol Cybern, 58(2), 101-12. Nguyen, Q., & Kleinfeld, D. (2005). Positive feedback in a brainstem tactile sensorimotor loop. Neuron, 45(3), 447-457. Nomura, T., Oshikawa, S., Suzuki, Y., Kiyono, K., & Morasso, P.Modeling human postural sway using an intermittent control and hemodynamic perturbations. Mathematical Biosciences. 145  Ogai, Y., & Ikegami, T. (2008). Microslip as a simulated artificial mind. Adaptive Behavior, 16(2-3), 129-147. Omlor, W., Patino, L., Hepp-Reymond, M., & Kristeva, R. (2007). Gamma-range corticomuscular coherence during dynamic force output. NeuroImage, 34(3), 11911198. Orma, E. J. (1957). The effects of cooling the feet and closing the eyes on standing equilibrium, different patterns of standing equilibrium in young adult men and women. Acta Physiol Scand, 38(3-4), 288-97. Paulus, W. M., Straube, A., & Brandt, T. (1984). Visual stabilization of posture. physiological stimulus characteristics and clinical aspects. Brain, 107 ( Pt 4), 1143-63. Perez, M. A., Soteropoulos, D. S., & Baker, S. N. (2012). Corticomuscular coherence during bilateral isometric arm voluntary activity in healthy humans. Journal of Neurophysiology, 107(8), 2154-2162. Peterka, R. J. (2000). Postural control model interpretation of stabilogram diffusion analysis. Biol Cybern, 82(4), 335-43. Peterka, R. J. (2002). Sensorimotor integration in human postural control. J Neurophysiol, 88(3), 1097-118. Petersen, T. H., Willerslev-Olsen, M., Conway, B. A., & Nielsen, J. B. (2012). The motor cortex drives the muscles during walking in human subjects. The Journal of Physiology, 590(10), 2443-2452. 146  Populin, L. C., & Yin, T. C. (1998). Behavioral studies of sound localization in the cat. The Journal of Neuroscience : The Official Journal of the Society for Neuroscience, 18(6), 2147-2160. Prieto, T. E., Myklebust, J. B., Hoffmann, R. G., Lovett, E. G., & Myklebust, B. M. (1996). Measures of postural steadiness: Differences between healthy young and elderly adults. IEEE Trans Biomed Eng, 43(9), 956-66. Prieto, T. E., Myklebust, J. B., & Myklebust, B. M. (1993). Characterization and modeling of postural steadiness in the elderly: A review. Rehabilitation Engineering, IEEE Transactions on, 1(1), 26-34. Ratliff, F., & Riggs, L. A. (1950). Involuntary motions of the eye during monocular fixation. Journal of Experimental Psychology, 40(6), 687-701. Riccio, G. E. (1993). In K. M. Newell, & D. M. Corcos (Eds.), Variability and motor control (pp. pp. 317-358; 12). Champaign, Illinois: Human Kinetics. Riggs, L. A., Ratliff, F., Cornsweet, J. C., & Cornsweet, T. N. (1953). The disappearance of steadily fixated visual test objects. J Opt Soc Am, 43(6), 495-501. Riley, M. A., & Clark, S. (2003). Recurrence analysis of human postural sway during the sensory organization test. Neurosci Lett, 342(1-2), 45-8. Riley, M. A., Mitra, S., Stoffregen, T. A., & Turvey, M. T. (1997). Influences of body lean and vision on unperturbed postural sway. Motor Control, 1, 229-246.  147  Riley, M. A., & Turvey, M. T. (2002). Variability of determinism in motor behavior. J Mot Behav, 34(2), 99-125. Roll, J. P., Vedel, J. P., & Roll, R. (1989). Eye, head and skeletal muscle spindle feedback in the elaboration of body references. Prog Brain Res, 80, 113-23; discussion 57-60. Romberg, M. H. (1853). A manual of the nervous diseases of man (english translation). London: Syndenham Society. Rosenberg, J. R., Amjad, A. M., Breeze, P., Brillinger, D. R., & Halliday, D. M. (1989). The fourier approach to the identification of functional coupling between neuronal spike trains. Prog Biophys Mol Biol, 53(1), 1-31. Salenius, S., Portin, K., Kajola, M., Salmelin, R., & Hari, R. (1997). Cortical control of human motoneuron firing during isometric contraction. J Neurophysiol, 77(6), 3401-5. Sasaki, M., Mishima, H., Suzuki, K., & Ohkura, M. (1995). Observations on microexploration in everyday activities. In B. G. Bardy, R. J. Bootsma & Y. Guiard (Eds.), Studies in perception and action III (pp. 99-102). Hillsdale, NJ: Lawrence Erlbaum Associates. Semba, K., & Komisaruk, B. R. (1984). Neural substrates of two different rhythmical vibrissal movements in the rat. Neuroscience, 12(3), 761-774. Shadmehr, R., & Mussa-Ivaldi, F. A. (1994). Adaptive representation of dynamics during learning of a motor task. J Neurosci, 14(5 Pt 2), 3208-24.  148  Slifkin, A. B., & Newell, K. M. (1999). Noise, information transmission, and force variability. Journal of Experimental Psychology: Human Perception and Performance, 25(3), 837-851. Slobounov, S., Hallett, M., Stanhope, S., & Shibasaki, H. (2005). Role of cerebral cortex in human postural control: An EEG study. Clin Neurophysiol, 116(2), 315-23. Smith, J. W. (1954). Muscular control of the arches of the foot in standing; an electromyographic assessment. J Anat, 88(2), 152-63. Smith, J. W. (1957). The forces operating at the human ankle joint during standing. J Anat, 91(4), 545-64. Soames, R. W., & Atha, J. (1981). The role of the antigravity musculature during quiet standing in man. Eur J Appl Physiol Occup Physiol, 47(2), 159-67. Soames, R. W., & Atha, J. (1982). The spectral characteristics of postural sway behaviour. Eur J Appl Physiol Occup Physiol, 49(2), 169-77. Sobel, N., Thomason, M. E., Stappen, I., Tanner, C. M., Tetrud, J. W., Bower, J. M., . . . Gabrieli, J. D. (2001). An impairment in sniffing contributes to the olfactory impairment in parkinson's disease. Proc Natl Acad Sci U S A, 98(7), 4154-9. Stoffregen, T. A., & Riccio, G. E. (1988). An ecological theory of orientation and the vestibular system. Psychological Review, 95(1), 3-14.  149  Straube, A., Krafczyk, S., Paulus, W., & Brandt, T. (1994). Dependence of visual stabilization of postural sway on the cortical magnification factor of restricted visual fields. Exp Brain Res, 99(3), 501-6. Sutton, G. G., & Sykes, K. (1967). The effect of withdrawal of visual presentation of errors upon the frequency spectrum of tremor in a manual task. The Journal of Physiology, 190(2), 281-293. Taube, W., Schubert, M., Gruber, M., Beck, S., Faist, M., & Gollhofer, A. (2006). Direct corticospinal pathways contribute to neuromuscular control of perturbed stance. J Appl Physiol, 101(2), 420-9. Thomas, D. P., & Whitney, R. J. (1959). Postural movements during normal standing in man. J Anat, 93, 524-39. Thomson, D. B., Inglis, J. T., Schor, R. H., & Macpherson, J. M. (1991). Bilateral labyrinthectomy in the cat: Motor behaviour and quiet stance parameters. Exp Brain Res, 85(2), 364-72. van der Kooij, H., van Asseldonk, E., & van der Helm, F. C. (2005). Comparison of different methods to identify and quantify balance control. J Neurosci Methods, 145(1-2), 175203. van Emmerik, R. E., & van Wegen, E. E. (2002). On the functional aspects of variability in postural control. Exerc Sport Sci Rev, 30(4), 177-83.  150  Verdú, E., Ceballos, D., Vilches, J. J., & Navarro, X. (2000). Influence of aging on peripheral nerve function and regeneration. Journal of the Peripheral Nervous System, 5(4), 191208. Vette, A. H., Masani, K., Nakazawa, K., & Popovic, M. R. (2010). Neural-mechanical feedback control scheme generates physiological ankle torque fluctuation during quiet stance. IEEE Transactions on Neural Systems and Rehabilitation Engineering : A Publication of the IEEE Engineering in Medicine and Biology Society, 18(1), 86-95. Vuillerme, N., & Nafati, G. (2007). How attentional focus on body sway affects postural control during quiet standing. Psychol Res, 71(2), 192-200. Walker, J. C., Kendal-Reed, M., Hall, S. B., Morgan, W. T., Polyakov, V. V., & Lutz, R. W. (2001). Human responses to propionic acid. II. quantification of breathing responses and their relationship to perception. Chemical Senses, 26(4), 351-358. Winter, D. A. (1995). Human balance and posture control during standing and walking. Gait & Posture, 3(4), 193-214. Winter, D. A., & Eng, P. (1995). Kinetics: Our window into the goals and strategies of the central nervous system. Behav Brain Res, 67(2), 111-20. Winter, D. A., Patla, A. E., & Frank, J. S. (1990). Assessment of balance control in humans. Med Prog Technol, 16(1-2), 31-51. Winter, D. A., Patla, A. E., Prince, F., Ishac, M., & Gielo-Perczak, K. (1998). Stiffness control of balance in quiet standing. J Neurophysiol, 80(3), 1211-21. 151  Winter, D. A., Prince, F., Frank, J. S., Powell, C., & Zabjek, K. F. (1996). Unified theory regarding A/P and M/L balance in quiet stance. J Neurophysiol, 75(6), 2334-43. Wolpert, D. M., & Ghahramani, Z. (2000). Computational principles of movement neuroscience.3, 1212-1217. Wolpert, D. M., Ghahramani, Z., & Jordan, M. I. (1995). An internal model for sensorimotor integration. Science, 269(5232), 1880-2. Wolpert, D. M., & Kawato, M. (1998a). Multiple paired forward and inverse models for motor control. Neural Netw, 11(7-8), 1317-29. Wolpert, D. M., & Kawato, M. (1998b). Multiple paired forward and inverse models for motor control. Neural Networks, 11(7–8), 1317-1329. Wright, W. G., Ivanenko, Y. P., & Gurfinkel, V. S. (2012). Foot anatomy specialization for postural sensation and control. Journal of Neurophysiology, 107(5), 1513-1521. Yoneda, S., & Tokumasu, K. (1986). Frequency analysis of body sway in the upright posture. statistical study in cases of peripheral vestibular disease. Acta Otolaryngol, 102(1-2), 8792.  152  

Cite

Citation Scheme:

        

Citations by CSL (citeproc-js)

Usage Statistics

Share

Embed

Customize your widget with the following options, then copy and paste the code below into the HTML of your page to embed this item in your website.
                        
                            <div id="ubcOpenCollectionsWidgetDisplay">
                            <script id="ubcOpenCollectionsWidget"
                            src="{[{embed.src}]}"
                            data-item="{[{embed.item}]}"
                            data-collection="{[{embed.collection}]}"
                            data-metadata="{[{embed.showMetadata}]}"
                            data-width="{[{embed.width}]}"
                            async >
                            </script>
                            </div>
                        
                    
IIIF logo Our image viewer uses the IIIF 2.0 standard. To load this item in other compatible viewers, use this url:
http://iiif.library.ubc.ca/presentation/dsp.24.1-0073647/manifest

Comment

Related Items