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Implicit sequence-specific motor learning in individuals with chronic stroke : spatial and temporal accuracy Geldreich, Tessa; Furgala, Devon; Mahannah, Stephanie; Boyd, Lara A. 2011-08

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    IMPLICIT SEQUENCE-SPECIFIC MOTOR LEARNING IN INDIVIDUALS WITH CHRONIC STROKE : SPATIAL AND TEMPORAL ACCURACY  Tessa Geldreich1 BSc, MPT Student  Devon Furgala1 BSc, MPT Student  Stephanie Mahannah1 BSc, MPT Student Lara A. Boyd1,2 PT, PhD  1Department of Physical Therapy, UBC 2Brain Behaviour Lab, UBC  Overview ? Background & Purpose ? Methods ? Results ? Discussion ? Implications for Physical Therapists ? Q & A  PURPOSE The purpose of this study was to verify if sequence-specific implicit motor learning occurs in individuals with chronic middle cerebral artery (MCA) stroke and to investigate the affect of an MCA stroke on the spatial and temporal components of implicit learning on a sequence-specific motor task.   BACKGROUND Stroke - Burden of Disease ? Leading cause of adult disability in North America1 ? Affects over 300,000 Canadians2 ? $43 billion yearly burden in USA3 ? 67% left with permanent disability4 ? 60% have impaired function of their hand4 ? Self reported decrease in Quality of Life1 Study Rationale ? MCA is the most common site for infarct5 ? Rise in the incidence of stroke with an aging population2 ? Need effective rehabilitation techniques focused on improving motor function ? As the ability to learn motor skills is essential for rehabilitation Motor Learning  Motor Learning: ?A set of processes associated with practice or experience leading to relatively permanent changes in the capability for responding.? 6   Learning Two components:  ? Explicit learning - ability to accurately recall information even after one exposure7 ? Consciously accessible via recall memory ? Used in cognitive processes ? Stored in the medial temporal lobe Learning ? Implicit learning - ability to acquire complex information without awareness of what has been learned8  ? Develops over time with numerous exposures to information or practice of a skill8  ? Distributed throughout various regions of the cortex9 ? Cerebellum7 ? Sensorimotor cortex8,10 ? Supplemental motor cortex8,10 ? Prefrontal cortex8,10 ? Thalamus8,10 ? Basal ganglia8,10  ? Implicit learning is an element for motor learning8   Areas supplied by the MCA11 How Do You Teach Someone to Walk? Explicit Instructions ? At toe off, activate hip flexors to accelerate limb through first 20 degrees of hip flexion. At this point, allow momentum to carry limb until hip is at approximately 20 degrees of flexion. During this time, engage tibialis anterior to dorsiflex?. Implicit Instructions ? Give it a go!  Implicit Motor Learning Two distinct components: ? Spatial Accuracy12 ? Ability to locate objects in space or direct extremities to the correct location ?  Involves the motor cortex  ? Temporal Accuracy12 ? Relates timing of movements ? Involves the cerebellum Motor Cortex Cerebellum Temporal: Swinging the racket at the right time to match the speed of the ball Spatial vs. Temporal Motor Learning Spatial: Getting the racket into the same space as the ball Combined = Right Place at the Right Time Implicit Motor Learning in MCA Strokes  ? Little research has been done to determine the effect of MCA strokes on the temporal and spatial components of sequence-specific implicit motor learning  ? may be referred to as implicit learning  ? Cerebellar infarcts showed:14 ? Temporal accuracy impaired ? Spatial accuracy improved  ? More research into sequence-specific implicit motor learning is warranted to enhance treatment strategies   Relevance for Physical Therapists Sequence-specific implicit motor learning...  ? has been demonstrated in people with MCA  infarcts7,13-15  ? has been demonstrated without explicit information15  ? may be disrupted if explicit information is provided concurrently in stroke subjects14    Study Aim and Hypothesis Aim: ? Examine changes in temporal and spatial accuracy of sequence-specific implicit motor learning in individuals with chronic stroke in the MCA distribution  Hypothesis:  ? Sequence-specific implicit learning will be demonstrated with a difference in spatial versus temporal accuracy METHODS Present Study ? Present study is part of a larger study  currently in preparation entitled   ?Promotion of Brain Reorganization after Stroke?   (Boyd & Eng et al., 2011, Grant # G072750:PILAB)16  Ethics ? Ethics approval from the UBC   Clinical Ethics Research Board  Study Flow Chart Participants recruited from: ?GF Strong ?VGH ?Lion?s Gate ?Dr. Eng?s database Screened with inclusion & exclusion criteria Undergo specific tests: Fugl Meyer Frenchay Aphasia Screen MOCA  Randomized into 1of 3 treatment groups  with block randomization & computer software based on CONSORT statement17 If acceptable: Read & sign informed consent We used the control group as our experimental group   Inclusion Criteria ? >18 years old ? First clinically diagnosed stroke ? Ischemic stroke in the middle cerebral artery or functional equivalent ? > 6 months post-stroke onset  ? Motor output impaired in upper extremity ? Passing scores on screening tests ? Fugl-Meyer UE score ? MOCA ? Frenchay Aphasia Screen   MCA Strokes Exclusion Criteria  ? Major psychiatric diagnosis ? History of substance abuse ? Neglect ? History of seizures or epilepsy ? Pregnancy ? Obesity ? Metal in body ? Claustrophobia   ? Score of <13 on expression and comprehension sections of Frenchay Aphasia Screening Test  ? Drugs that impair brain plasticity  ? Anticholinergics, GABAergics, NMDA-receptor blockers  ? History of tumor, head trauma, neurodegenerative disorder  ? U/E impairment that limits participation in experimental motor skill task  Novel Motor Tracking Task  Tracking Task ? Motor Task Example Target Cursor  Participant Cursor Experimental Protocol ? Each consenting participant will be subjected to the following timeline:            Day Duration Experimental Task 1 60 min Consent; Screening tests; Baseline testing 2-6 60 min Task practice 7 60 min Retention testing Baseline testing Retention testing Day  1         2          3         4          5          6          7   Task practice Experimental Protocol 2 Blocks consist of trials Trials are 18 seconds long Outcome Measures Learning is inferred by a decrease in any of these: 1. Overall tracking error (RMSE) 2. Temporal Lag (ms) 3. Spatial accuracy (corrected RMSE)  (1) Computer Participant  Outcome Measures Learning is inferred by a decrease in any of these: 1. Overall tracking error (RMSE) 2. Temporal Lag (ms) 3. Spatial accuracy (corrected RMSE)  (2) Computer Participant  Outcome Measures Learning is inferred by a decrease in any of these: 1. Overall tracking error (RMSE) 2. Temporal Lag (ms) 3. Spatial accuracy (corrected RMSE)  (3) Computer Participant  RESULTS ? 11 complete data sets were analyzed ? Averages (SD), T-tests, and Effect Size were calculated ? T-tests significance level: p= 0.008 ? 6 tests were run ? New critical p-value is p= 0.05/6  ? Corrects for multiple comparisons Results Overview T-Test: Overall Repeated 0.0003 Random 0.0025 T-Test: Spatial Repeated 0.0002 Random 0.0025 T-Test: Temporal Repeated 0.0193 Random 0.0234 0510152025 Baseline  RetentionRMSE 02468101214161820 Baseline  RetentionCorrected RMSE 0100200300400500600700 Baseline  RetentionTime (ms)  Overall Tracking Error       Spatial Accuracy        Temporal Accuracy p= 0.008  Effect Size   0.0000.2000.4000.6000.8001.000OverallTracking ErrorSpatial Error Time LagEffect Size Components of Sequence-Specific Implicit Motor Learning   RepeatedRandom Overall Tracking          Spatial    Temporal           Error                   Accuracy             Accuracy Effect Size 0.2 small effect, 0.5 moderate effect, 0.8 large effect18  Effect Size (0.2=small, 0.5=moderate, 0.8=large) Repeated Overall Tracking Error 0.757 Random Overall Tracking Error 0.621 Repeated Spatial 0.669 Random Spatial 0.633 Repeated Temporal 0.790 Random Temporal 0.577 Summary of Results  ? This study confirms that sequence-specific implicit motor learning is possible with damage to the MCA  ? Our data suggests participants showed a greater change in the temporal domain compared to spatial  DISCUSSION Generalized Motor Learning7 (aka Practice Effect) ? Learning is expected with any novel motor task as task familiarity increases performance and decreases error  Overall Tracking Error  Decreased  error  Overall Tracking Error  Decreased error Sequence-Specific Implicit Motor Learning ? Generalized motor learning can be differentiated from sequence-specific implicit motor learning by comparing the effect size of repeated and random sequences ? Sequence-specific implicit motor learning is inferred by an increase in repeated effect size (vs. random)  0.0000.2000.4000.6000.8001.000 Effect Size   Generalized vs. Implicit Motor Learning  0.0000.2000.4000.6000.8001.000OverallTrackingSpatialAccuracyTime LagEffect Size   RepeatedRandomGeneralized Motor Learning Sequence-Specific Implicit Motor Learning Generalized Motor Learning  Sequence-specific Implicit Motor Learning If random and repeated sequences display equal effect sizes, generalized motor learning can be inferred  If random and repeated sequences display different effect sizes, more effect due to implicit sequence-specific motor learning can be inferred Generalized Motor Learning Sequence-Specific Implicit Motor Learning      Overall Tracking        S tial             Temporal              E ror                 racy            Accuracy     MCA vs. Cerebellar Infarcts ? In this study, MCA infarcts shows:  ? Temporal accuracy was improved ? Spatial accuracy shows less improvement  ? Cerebellar infarcts showed the opposite:14 ? Temporal accuracy impaired ? Spatial accuracy was improved  ? Neural networks supplied by the MCA are more involved in spatial accuracy than temporal accuracy  Implications for Physical Therapists ? Motor learning is capable with no explicit instructions  ? For individuals with strokes in MCA distribution: ? Focus rehabilitation on spatial accuracy distribution as this appears to be lagging (Remediation) ? Focus rehabilitation on temporal accuracy as this appears to improve with task specific practice (Compensation)  ? More research into sequence-specific implicit motor learning is warranted to enhance treatment strategies  Limitations ? Limited number of participants   ? Participant fatigue: 3 participants unable to complete all blocks of baseline and retention testing ? Data averaged and imputed  ? One participant eliminated due to erroneous results ? Data imputed from average of all remaining participants   CONCLUSION 1. Individuals with MCA stroke are able to learn new motor sequences implicitly without explicit instructions  2. Generalized motor learning can be seen in both spatial and temporal components 3. Greater gains were seen in temporal accuracy compared to spatial accuracy 4. Neural networks supplied by the MCA are involved in spatial accuracy to a greater extent than temporal accuracy   ACKNOWLEDGEMENTS ? The authors would like to thank Lara Boyd, PT, PhD, Janice Eng, PT, PhD and Elizabeth Dao, BA for their support and guidance. This work was made possible by the Brain Behaviour Lab at UBC. We would also like to thank the Department of Physical Therapy at UBC in Vancouver, Canada. REFERENCES 1. Edwards JD, Koehoorn M, Boyd LA, Levy AR. Is health-related quality of life improving after stroke? A comparison of health utilities indices among canadians with stroke between 1996 and 2005. Stroke. 2010;41:996-1000.  2. Lloyd-Jones D, Adams RJ, Brown TM, et al. Heart disease and stroke statistics--2010 update: A report from the american heart association. Circulation. 2010;121:e46-e215. 3. Quinn, Dawson. Acute ?strokenomics? efficacy and economic analyses of altephase for acute ischemic stroke.  Expert Rev. Pharmacoeconomics Outcomes Res. 2009; 9(6): 513-522. 4. Liepert J. Motor cortex excitability in stroke before and after constraint-induced movement therapy. Cogn Behav Neurol. 2006;19:41-47.  5. Seitz RJ, Hoflich P, Binkofski F, Tellmann L, Herzog H and Freund HJ (1998). Role of the Premotor Cortex in Recovery From Middle Cerebral Artery Infarction. Arch Neurol. 55:1081-1088. 6. Schmidt RA, Lee TD. Motor Control and Learning: A Behavioural Emphasis, 3rd Edition Champaign, IL:Human Kinetics. 7. Boyd LA, Winstein CJ. Cerebellar stroke impairs temporal but not spatial accuracy during implicit motor learning. Neurorehabil Neural Repair. 2004;18:134-143.  8. Seger CA. Implicit learning. Psychol Bull. 1994;115:163-196.  REFERENCES 9. Orban P, Peigneux P, Lungu O, et al. Functional neuroanatomy associated with the expression of distinct movement kinematics in motor sequence learning. Neuroscience. 2011;179:94-103.  10. Reber PJ, Squire LR. Encapsulation of implicit and explicit memory in sequence learning. J Cogn Neurosci. 1998;10:248-263.  11. Snell RS. Clinical Neuroanatomy, 7th Edition, 2010, Baltimore, MD: Lippincott Williams & Wilkins.  12. Lee D. Learning of spatial and temporal patterns in sequential hand movements. Brain Res Cogn Brain Res. 2000;9:35-39.  13. Pohl PS, McDowd JM, Filion DL, Richards LG, Stiers W. Implicit learning of a perceptual-motor skill after stroke. Phys Ther. 2001; 81: 1780-1789. 14.  Boyd L, Winstein C. Explicit information interferes with implicit motor learning of both continuous and discrete movement tasks after stroke. J Neurol Phys Ther. 2006;30:46-57. 15. Boyd LA, Winstein CJ. Implicit motor-sequence learning in humans following unilateral stroke: The impact of practice and explicit knowledge. Neurosci Lett. 2001;298:65-69.  16. Boyd LA, Eng J, Meehan S, Dao E, Linsdell M. Promotion of brain reorganization after stroke. Paper in preparation by Brain Behaviour Lab, UBC, Vancouver, Canada. 2011. 17. Consort Statement. 18. Thomas JR, Salazar W, Landers DM. What is missing in p<.05? Effect size. Research Quarterly for Exercise and Sport. 1991; 62: 344-348.  REFERENCES 19. Boyd LA, Vidoni ED, Wessel BD. Motor learning after stroke: Is skill acquisition a prerequisite for contralesional neuroplastic change? Neurosci Lett. 2010;482:21-25.  20. Boyd LA, Winstein CJ. Providing explicit information disrupts implicit motor learning after basal ganglia stroke. Learn Mem. 2004;11:388-396.  21. Boyd LA, Winstein CJ. Impact of explicit information on implicit motor-sequence learning following middle cerebral artery stroke. Phys Ther. 2003;83:976-989.  22. Cleeremans A, Destrebecqz A, Boyer M. Implicit learning: News from the front. Trends Cogn Sci. 1998;2:406-416.  23. J?rgensen ,H.S., Nakayama H, Raaschou HO, Vive-Larsen J, St?ier M, Olsen TS. Outcome and time course of recovery in stroke. part II: Time course of recovery. the copenhagen stroke study. Arch Phys Med Rehabil. 1995;76:406-412.  24. Meehan SK, Randhawa B, Wessel B, Boyd LA. Implicit sequence-specific motor learning after subcortical stroke is associated with increased prefrontal brain activations: An fMRI study. Hum Brain Mapp. 2011;32:290-303.  25. Meehan SK, Randhawa B, Wessel B, Boyd LA. Implicit sequence-specific motor learning after subcortical stroke is associated with increased prefrontal brain activations: An fMRI study. Hum Brain Mapp. 2011;32:290-303.  26. Nowak DA, Grefkes C, Ameli M, Fink GR. Interhemispheric competition after stroke: Brain stimulation to enhance recovery of function of the affected hand. Neurorehabil Neural Repair. 2009;23:641-656.  27. O'Dell M,W., Lin CD, Harrison V. Stroke rehabilitation: Strategies to enhance motor recovery. Annu Rev Med. 2009;60:55-68.  REFERENCES 28. Orrell AJ, Eves FF, Masters RSW, MacMahon KMM. Implicit sequence learning processes after unilateral stroke. Neuropsychol Rehabil. 2007;17:335-354.  29. Platz T, Pinkowski C, van Wijck F, Kim I, di Bella P, Johnson G. Reliability and validity of arm function assessment with standardized guidelines for the fugl-meyer test, action research arm test and box and block test: A multicentre study. Clin Rehabil. 2005;19:404-411.  30. Shadmehr R, Holcomb HH. Neural correlates of motor memory consolidation. Science. 1997;277:821-825.  31. Subramanian SK, Massie CL, Malcolm MP, Levin MF. Does provision of extrinsic feedback result in improved motor learning in the upper limb poststroke? A systematic review of the evidence. Neurorehabil Neural Repair. 2010;24:113-124.  32. Winstein CJ, Merians AS, Sullivan KJ. Motor learning after unilateral brain damage. Neuropsychologia. 1999;37:975-987.  33. Winstein CJ, Merians AS, Sullivan KJ. Motor learning after unilateral brain damage. Neuropsychologia. 1999;37:975-987.  34. Yozbatiran N, Alonso-Alonso M, See J, et al. Safety and behavioral effects of high-frequency repetitive transcranial magnetic stimulation in stroke. Stroke. 2009;40:309-312.  35.,r:4,s:0&tx=143&ty=46&biw=676&bih=694   REFERENCES 36.,r:5,s:0 37.,r:0,s:9&biw=676&bih=694 38.,r:1,s:0&biw=676&bih=694 Questions? Overview of Strokes Functionally Equivalent to MCA A sudden loss of function in a portion of the brain that is at a distance from the site of injury, but is connected to it by neurons.  A loss of function and electrical activity in an area of the brain due to a lesion in a remote area that is neuronally connected with it Diaschisis Definitions: Pontine Stroke with atrophy of sensorimotor cortex Statistics Effect size After comparing repeated Baseline data to repeated Retention data, the difference between these two data sets was converted to a numerical magnitude.   Overall Tracking Error   Overall Tracking Error  T-tests Compared repeated Baseline data to repeated Retention data Repeated and random sequences can be compared numerically but not statistically T-test results (p=0.008) Repeated Overall Tracking Error 0.0003 Random Overall Tracking Error 0.0025 Repeated Spatial 0.0002 Random Spatial 0.0025 Repeated Temporal 0.0193 Random Temporal 0.0234 Effect Size (0.2=small, 0.5=moderate, 0.8=large) Repeated Overall Tracking Error 0.757 Random Overall Tracking Error 0.621 Repeated Spatial 0.669 Random Spatial 0.633 Repeated Temporal 0.790 Random Temporal 0.577 Sample Size Calculations ? ? = 0.05 ? Power = 0.8 ? Effect size = 0.8 ? Pilot study by Boyd & Linsdell (2009) suggests effect size for treatment of 1.2 ? Required 12 subjects for each of the 3 groups ? Eleven suitable participants were assigned to the control group of the larger study; this group is our experimental group      Sample Size Calculation  


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