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Cortical influences upon the dive response of the muskrat (Ondatra zibethica) McCulloch, Paul Frederick 1989

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CORTICAL INFLUENCES UPON THE DIVE RESPONSE OF THE MUSKRAT {ONDATRA ZIBETHICA) by PAUL FREDERICK MCCULLOCH B.A., University of B r i t i s h Columbia, 1983 B.SC, University of B r i t i s h Columbia, 1986 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE in THE FACULTY OF GRADUATE STUDIES (Department of Zoology) We accept t h i s thesis as conforming to the required standard THE UNIVERSITY OF BRITISH COLUMBIA August 1989 ® Paul Frederick McCulloch, 1989 In presenting this thesis in partial fulfilment of the requirements for an advanced degree at the University of British Columbia, I agree that the Library shall make it freely available for reference and study. I further agree that permission for extensive copying of this thesis for scholarly purposes may be granted by the head of my department or by his or her representatives. It is understood that copying or publication of this thesis for financial gain shall not be allowed without my written permission. Department of The University of British Columbia Vancouver, Canada Date 1 t ^ j j ^ DE-6 (2/88) ABSTRACT Force dived animals undergo cardiovascular changes characterized by bradycardia, increased t o t a l peripheral resistance, and changes in blood flow d i s t r i b u t i o n . Since these changes occur i n decerebrated animals, the dive response must be a brainstem r e f l e x . However, in voluntary dives, animals may show anticipatory bradycardia and may also adjust t h e i r cardiovascular responses according to anticipated dive duration, i n d i c a t i n g suprabulbar influences upon dive responses. Studies of heart rate using telemetry have shown that there can be substantial differences in the dive response of v o l u n t a r i l y and force dived animals. Furthermore, some animals show a "fear bradycardia" when trapped i n a s t r e s s f u l s i t u a t i o n , leading some researchers to suggest that bradycardia during forced submersion i s an a r t i f a c t of the stress of the s i t u a t i o n . Muskrats (Ondatra zibethica) were observed f r e e l y diving for food i n an indoor tank using a video camera and VCR unit. EKG was telemetered from the animals and recorded on the audio channel of the VCR tape. Heart rate responses to voluntary dives were analyzed and compared with those from escape and forced dives. Heart rate responses were also recorded from decorticate and sham operated muskrats to elucidate the role that the cerebral cortex plays i n the dive response. In a l l types of dives, muskrats exhibited a rapid and large bradycardia upon submergence (heart rate declined by greater than 55% of the predive heart r a t e ) . Obviously diving bradycardia i n the muskrat was not due to fear or stress, but occurred as a response to submersion per se. There was no evidence of post-dive tachycardia or anticipatory immersion bradycardia. Disturbing the animal in a non-diving s i t u a t i o n resulted i n only a 13% decrease in heart rate. In intact animals voluntary, escape, and forced submergence resulted i n progressively greater decreases i n heart rate. Heart rate f e l l by 56% i n voluntary dives, 65% i n escape dives, and 73% i n forced dives. I n t e n s i f i c a t i o n of the bradycardia to a lower heart rate than that seen i n voluntary dives was mediated by the cerebral cortex, as heart rate i n decorticate muskrats in escape and forced dives did not f a l l below that seen i n voluntary dives. This indicates that the f i n a l adjustment of dive heart rate i s dependent upon an in t a c t cerebral cortex. However, i n decorticate muskrats there appeared to be a recovery of c o r t i c a l function, as i n t e n s i f i c a t i o n of bradycardia i n forced dives was dependent upon the time that had elapsed a f t e r surgery. " ' This study shows that there i s a c o r t i c a l influence upon the cardiovascular system during diving. It also indicates that in experiments with unanesthetized animals, the degree of stress of the s i t u a t i o n must be taken into account, as t h i s may affect physiological responses. V TABLE OF CONTENTS ABSTRACT i i LIST OF TABLES v i LIST OF FIGURES v i i ACKNOWLEDGEMENTS v i i i INTRODUCTION 1 METHODS 7 a) Surgical Procedures 10 1) EKG Transmitter Implantation 10 2) Decortication 11 b) Recording Techniques 12 c) Experimental Protocol 13 1) Types of dives 13 i) Voluntary dives 13 i i ) Escape dives 14 i i i ) Trapped dives 14 iv) Forced dives 14 2) Non-diving conditions 15 d) Anatomical Analysis of data 15 e) S t a t i s t i c a l Analysis of Data 17 RESULTS 18 a) Heart Rate Responses from Intact Muskrats 18 b) Heart Rate Responses from Decorticate and Sham Operated Muskrats 24 c) Anatomical Results 34 DISCUSSION 46 REFERENCES 55 APPENDIX 1 61 APPENDIX 2 62 APPENDIX 3 .- . 63 v i L i s t of Tables Table I Brain Measurements and C o r t i c a l Damage 37 Table II Abbreviations used i n Figures 7-10 44 v i i L i s t of Figures Figure 1 Diagram of diving tank 8 Figure 2 Heart rates during rest and a c t i v i t y 19 Figure 3 Dive heart rates of intact muskrats 21 Figure 4 Dive heart rates of sham operated muskrats ... 26 Figure 5 Dive heart rates of decorticate muskrats 29 F i g u r e 6 Forced dive heart rates as a function of weeks afte r decortication 32 Figure 7 Cross sections of sham operated and decorticate muskrat brains 35 Figure 8 S e r i a l brain cross sections from decorticate Muskrat M14 38 Figure 9 S e r i a l brain cross sections from decorticate Muskrat M31 40 Figure 10 S e r i a l brain cross sections from decorticate Muskrat M20 42 v i i i ACKNOWLEDGEMENTS I thank Dr. David Jones for his help, guidance, and enthusiasm for t h i s project. I also thank Dr. Geoff Gabbott for his help with the figures, Mike Hedrick and Dr. Peter Bushnell for t h e i r help with s t a t i s t i c s , Dr. Richard Tees and L u c i l l e Hoover for t h e i r help with the decortication procedure, and my colleagues i n the lab of Dr. Jones for t h e i r help and c r i t i c i s m s throughout the years. I am grateful for the Teaching Assistantships I received from the Department of Zoology. 1 INTRODUCTION Upon enforced submergence a i r breathing animals invoke certain cardiovascular changes as part of an oxygen conserving mechanism known as the dive response (Butler and Jones 1982). During submersion, a r t e r i a l blood pressure i s maintained while cardiac output i s reduced and peripheral resistance i s increased (Butler and Jones 1982). There are changes in blood flow d i s t r i b u t i o n s with increased flow to the heart and CNS and a decreased flow to less oxygen sensi t i v e tissues such as muscles and abdominal organs (Zapol et al. 1979/ Jones et al. 1982). The marker which has been used most frequently to indicate the onset of these cardiovascular events during submersion i s decreased heart rate (Andersen 1963a; Dykes 1974). The physiological responses to restrained diving are medullary reflexes since the cardiovascular adjustments to diving can be e l i c i t e d i n decerebrate ducks (Andersen 1963b; Gabbott and Jones 1985) and muskrats (Drummond and Jones 1979). However, i t has been known since 1940 that suprabulbar regions (those areas of the CNS above the pons and medulla) can affect the dive response as Scholander (1940) observed that seals can show an anticipatory diving bradycardia and a decrease i n heart rate due to threatening gestures by the researcher. The nucleus tractus s o l i t a r i u s (NTS) i n the medulla i s considered to be the primary integration s i t e of 2 cardiovascular information (Galosy et al. 1981/ Spyer 1982). The NTS receives direct afferent projections from systemic and pulmonary a r t e r i a l baroreceptors, a r t e r i a l chemoreceptors, and pulmonary stretch receptors v i a c r a n i a l nerves IX and X (Galosy et al. 1981), and from upper respiratory passages v i a c r a n i a l nerve V (Korner 1979). The NTS i s also involved i n efferent cardiovascular control as i t sends projections to the dorsal motor nucleus of the vagus (DMV) i n the medulla and to the intermediolateral nucleus (ILN) of the spinal cord, the s i t e s of o r i g i n of the cardiovascular parasympathetic and sympathetic preganglionic neurons, respectively (Galosy et al. 1981). Direct suprabulbar projections to the NTS also arise from limbic and c o r t i c a l regions (Saper 1982; van der Kooy et al. 1984). It i s from these higher CNS leve l s that central modification of the dive response could be made. Conditioning experiments have implied a role of the CNS in the control of heart rate (cf. Galosy et al. 1981). C l a s s i c a l heart rate conditioning i n sea li o n s Zalophus californianus, can produce a more intense bradycardia than can immersion (Ridgeway et al. 1975), and habituation may attenuate or completely eliminate diving bradycardia i n ducks (Gabrielsen 1985; Gabbott and Jones 1985; Gabbott and Jones 1987). It i s possible that the dive response routinely involves some form of associative learning (Butler and Jones 1982). Vo l u n t a r i l y diving harbour seals Phoca vitulina, and 3 tufted ducks Aythya fuligvla, may show anticipatory bradycardia before immersion and an increase i n heart rate before resurfacing (Scholander 1940; Jones et al. 1973; Butler and Woakes 1982). Animals such as Weddell seals Leptonychotes weddelli, and tufted ducks A. fuligula, may also adjust the int e n s i t y of cardiovascular responses according to the anticipated dive length or duration (Kooyman and Campbell 1972; H i l l et al. 1983; Stephenson et al. 1986). The "psychological condition" or "state of arousal" of an animal can have an important e f f e c t upon the dive response (Butler and Jones 1982; Gabbott and Jones 1987). The d i s p o s i t i o n and nervous state of seals i s important for f u l l development of the dive bradycardia (Irving et al. 1941). "Calm" ducks also show a much better response than "alarmed" ducks (Folkow et a l 1967) .- In humans, "preoccupation" or mental a c t i v i t y (mental arithmetic) almost completely attenuates the dive response (Ross and Steptoe 1980, Wolf 1978) while fear or anxiety may enhance the bradycardia (Wolf 1978). The portion of the brain thought to be most involved with emotional experience and expression i s the limbic system, which consists of the hippocampus, amygdala, septum, and hypothalamus (Hilton 1982). Limbic structures have extensive connections with the NTS, and might mediate the cardiovascular changes observed i n emotional situations and during periods of stress (Swanson 1982). 4 EKGs telemetered from free l y diving animals have shown that there can be substantial differences i n cardiac responses to voluntary and forced diving. Researchers working with tufted A. fuligula, and pochard ducks A. ferina, (Butler and Woakes, 1979), Canada geese Branta canadensis, and double crested cormorants Phalacrocorax auritus,• (Kanwisher et al. 1981), swamp rabbits Sylvalagus aquaticus, (Smith and Tobey 1983), American a l l i g a t o r s Alligator mississippiensis, (Smith et al. 1974), and caimans Caiman crocodilus, (Gaunt and Gans 1969) have reported a substantial decrease i n heart rate during enforced dives, but found l i t t l e or no bradycardia during voluntary dives. This i s quite d i f f e r e n t from the " c l a s s i c a l " forced dive response as outlined by Andersen (1966). In contrast to the active (fight or f l i g h t ) defence response, some animals show an alternative response when faced with a threatening stimulus. Small prey animals, when caught i n a si t u a t i o n with l i t t l e p o s s i b i l i t y of escape, have a tendency to remain motionless and hide i n an- e f f o r t to avoid detection (Gabrielsen et a l . 1977; Jacobsen 1979; Gabrielson and Smith 1985). In t h i s s i t u a t i o n these animals show a reduction i n heart rate which i s known as a "fear" bradycardia (Gab'rielsen et al. 1977) . The defense reaction i s controlled by an area located in the postero l a t e r a l hypothalamus and e l e c t r i c a l stimulation of t h i s area results i n a defense response (Galosy et al. 1981), which may include the appropriate 5 behavioural actions for f l i g h t , threat or attack (Spyer 1984). "Playing dead", with a drop i n heart and respiratory rates, i s considered to be a second type of defence response (Hilton 1982). U n t i l recently, studies investigating diving bradycardia have mainly involved forced dived animals. This has raised doubts as to whether the bradycardia seen during submersion i s due to submersion alone, or whether i t i s an experimental a r t i f a c t caused by the emotional ("fearful") s i t u a t i o n of the enforced submersion (Gaunt and Gans 1969; Kanwisher et al. 1981). Some researchers have even stated that diving bradycardia i s s o l e l y fear-induced and a res u l t of the methods used to study the physiological responses to diving i n the laboratory (Smith and De Carvalho 1985). However the following evidence counters the argument that involuntary submersion bradycardia i s a defence response. Naive dabbling ducks Anas platyrhynchos, given 100% oxygen ( F u r i l l a and Jones 1986; Gabbott and Jones 1987) and redhead ducks A. americana, having l o c a l anesthetic applied to t h e i r nasal mucosa ( F u r i l l a and Jones 1986) f a i l to show a forced dive bradycardia. Presumably they should have experienced the same amount of "fear" as untreated ducks. Secondly, there appears to be d i f f e r e n t efferent mechanisms involved in the control of fear and dive bradycardias (Causby and Smith 1981; Smith and Tobey 1983). F i n a l l y , decerebrate animals show a dive response (Andersen 1963b; Drummond and Jones 1979; Gabbott and Jones 1987), and 6 they are " f a i r l y d i f f i c u l t to scare" (Blix and Folkow 1984). Although t h i s evidence supports the reflexogenic basis of the dive response, higher CNS levels are undoubtedly involved i n the cardiovascular responses to diving. Certain areas of the cortex (the insular, medial prefrontal, and anterior cingulate regions) have extensive connections to the NTS in the rat and mouse (Saper 1982; Terreberry and Neafsey 1983; van der Kooy et al. 1984) and e l e c t r i c a l stimulation of these areas can produce cardiovascular changes (Lofving 1961; Buchanan et al. 1985; Burns and Wyss 1985; Powell et al. 1985; Ruggiero et a l 1987; Verberne et al. 1987; Verberne et al. 1988). The connections provide a route by which c o r t i c a l a c t i v i t y may modulate cardiovascular functioning during both diving and non-diving. The intent of t h i s study was to investigate the contention that the bradycardia which occurs during forced submersion i s a fear-induced defence response. Comparisons of the dive response of the muskrat Ondatra zibethica, i n voluntary, escape, and forced dives were made. Furthermore, the dive response from decorticate and sham operated muskrats was recorded. These experiments have elucidated the role the cortex plays i n the dive response and indicated to what degree the cortex can affect cardiovascular functioning. 7 METHODS Experiments were carr i e d out on 18 adult muskrats {Ondatra zibethica) of both sexes, ranging i n weight from 0.673 to 1.320 kg. The muskrats, trapped i n the v i c i n i t y of Richmond, Surrey, and Delta B.C., were held i n the University animal holding f a c i l i t y before being transferred to two concrete tanks (155 X 60 X 80 cm) i n the B i o l o g i c a l Sciences Building where a l l experiments were performed. One tank was usually dry and used as a temporary holding and recovery unit while the other contained the diving set-up (see figure 1). The depth of water i n the tank was held at 40 cm. Horizontal and v e r t i c a l sub-surface wire mesh created a 2 m (4m round t r i p ) tunnel that the muskrats were required to swim through to reach food placed on the bottom of the pool. A 50 X 35 cm platform at one end of the pool provided a nesting area for the muskrats. Straw or wood shavings served as bedding i n both tanks. During the experiments the animals were fed unmedicated Purina Rabbit Chow and water ad libitum. Diet was supplemented with apples, carrots, and on occasion lettuce and celery. 8 Figure 1. Diagram of diving tank. Diagram of concrete tank used during diving experiments. Refer to text for d e t a i l s . ©CKU.1t Figure 1. Diagram of diving tank. 10 (a) Surgical Procedures (1) EKG Transmitter Implantation A modified design of a Narco Biosystems (Downsview Ont.) EKG transmitter was used to record heart rate from spontaneously behaving muskrats. After attaching a 3 v o l t l i t h i u m battery, the transmitter was embedded i n tissue wax and then covered with a s i l i c o n e sealant. For a l l surgical procedures sodium pentobarbitol (Somnotol, MTC Pharmaceuticals, Mississauga Ont.) was injected i n t r a p e r i t o n e a l l y a f t e r i n i t i a l sedation by inhalation of ether or Halothane (Fluothane, Ayerst Laboratories, Montreal). The i n i t i a l dose of Somnotol, 40-50 mg'kg - 1, was supplemented as required. Fur was clipped from the area where the i n c i s i o n s were to be made, and the exposed skin swabbed with a t o p i c a l germicide (Betadine, Purdue Frederick, Toronto). After i n j e c t i o n of l o c a l anesthetic (Xylocaine 2%, Astra Pharmaceuticals, Mississauga, Ont.), i n c i s i o n s were made over the sternum, and abdomen just caudal to the r i b cage. A subcutaneous pocket was formed on the ventral surface of the abdomen to hold the transmitter. From t h i s pocket the EKG transmitter leads were threaded subdermally to the sternum i n c i s i o n . The overlying muscle tissue was teased apart and the exposed i n t e r c o s t a l muscles were c a r e f u l l y pierced with an intravenous catheter placement unit (20 gauge; Desderet Medical Inc. Sandy, Utah). The intracath served as a guide along which the EKG 11 leads were introduced into the thoracic cavity. The leads were sutured in place, and anchored with instant bond cement (Histoacryl, B.Braun Melsungen AG, Melsungen, West Germany). The i n c i s i o n s were then closed and reswabbed with the t o p i c a l germicide. The muskrat was kept i n a carrying cage u n t i l i t recovered from the anaesthetic and then was returned to the concrete pool. (2) Decortication Muskrats were anesthetized with sodium pentobarbitol and placed in a stereotaxic head-holder (Narishigi S c i e n t i f i c , Tokyo, Japan). The fur on the top of the head was clipped, and the exposed area swabbed with t o p i c a l germicide. A 3 cm i n c i s i o n was made along the midline of the s k u l l . The temporal muscle was retracted l a t e r a l l y to expose most of the p a r i e t a l and parts of the f r o n t a l and squamosal bones. Using a dental d r i l l , two 1 cm^ s k u l l pieces were removed to expose the dorsolateral aspects of the cerebral hemispheres. A narrow s t r i p of bone was l e f t over the superior s a g i t a l sinus. After r e t r a c t i o n of the dura, the exposed neocortex was removed by aspiration. Care was taken not to aspirate deeper than the corpus callosum, although the l a t e r a l v e n t r i c l e was exposed i n every muskrat. C o r t i c a l removal was extended underneath the edges of the exposed bone, r o s t r a l l y towards the f r o n t a l cortex, caudally towards the o c c i p i t a l cortex, medially towards the midline, and l a t e r a l l y towards the r h i n a l f i s s u r e . Bleeding was 12 controlled with absorbant g e l a t i n sponges (Gelfoam, Upjohn, Don M i l l s , Ont.) or m i c r o f i b r i l l a r collagen hemostat (Avitene, Avicon, Humancao, Puerto Rico). The scalp wound was then sutured and reswabbed with the t o p i c a l germicide. The muskrat was given an intramuscular a n t i b i o t i c i n j e c t i o n (Oxytetracycline hydrochloride, Rogar/ST, Montreal; 45-65 m g / k g ) and l e f t to recover overnight before being returned to the dry concrete tank. Sham decortications followed the same operative and recovery procedures as the decortications, except that the cortex was l e f t i n t a c t . (b) Recording Techniques Behaviour of the animals was recorded on a VCR unit (HR-S20U, JVC Canada Inc, Scarborough, Ont.) with a video camera (GX-N4UT, JVC Canada Inc, Scarborough, Ont.). The EKG signal was received by a communication receiver . (IC-R7000, ICOM, Osaka, Japan) and recorded on the audio channel of the VCR tape. After an experiment the tape was viewed at high speed. When a dive occurred, the tape was slowed, and the EKG was displayed on a pen recorder. Pre-dive heart rates were averaged over the 5-10 second i n t e r v a l immediately preceding the dive. Instantaneous dive heart rates at selected time during the dives were determined by ca l c u l a t i n g the average of two adjacent cardiac inte r v a l s (although on occasion only one cardiac i n t e r v a l was used) 13 and converting t h i s to beats per minute (BPM). In non-diving conditions, heart rates were calculated by converting the number of EKG signals obtained during 10 second periods into BPM. (c) Experimental Protocol (1) Types of dives (i) Voluntary dives. One to two weeks before any surgical procedures, intact muskrats were placed i n the diving tank to acclimate to t h e i r surroundings. It was during t h i s time that they were trained to dive for food on the bottom of the tank. The EKG transmitter was then implanted and after 2 to 3 days the experiments began. Voluntary dives by the muskrat were recorded i n a quiet room with no researcher present. The VCR recording apparatus and radio receiver were positioned to f i l m the muskrats as they dived spontaneously for submerged food. Decorticate and sham operated muskrats were reintroduced to water about a week afte r decortication. They were housed on a platform i n the holding tank, and the water l e v e l i n the tank was then raised i n steps over a 3 day period. When they were swimming competently, they were transferred to the dive tank and trained to dive underneath the screens. It was found that decorticate animals would not take submerged food, but they would read i l y take f l o a t i n g food. Consequently, the end of the dive tunnel 14 that was furthest from the nesting platform was open to the surface which resulted in a shorter dive path (2 m as opposed to 4 m for the intact animals). Sham operated animals were exposed to the same shortened dive path as the decorticated animals. Once decorticated and sham operated animals were trained to dive, the experimental protocol was simi l a r to that for intact animals. ( i i ) Escape dives. These dives were caused by disturbances such as noises and/or gestures made by the researcher. The animal was unrestrained and perhaps mimicked the behaviour of muskrats escaping a predator in the wild. A recovery period of 5 minutes separated each dive. ( i i i ) Trapped dives. The muskrat was trapped underwater after f i r s t performing an escape dive. The muskrat was prevented from resurfacing by placing a screen across the mouth of the underwater tunnel. The object of t h i s protocol was to record any a l t e r a t i o n i n the heart rate of the muskrat afte r i t became trapped. The screen was removed approximately 10 seconds after the animal became aware that i t was trapped, thus allowing i t to resurface. (iv) Forced dives. Muskrats were placed i n a 30 X 30 X 100 cm wire cage. The cage and muskrat were then lowered underwater for 60 seconds. The size of the cage allowed the muskrat to move about, but they could not control the onset 15 or duration of the dive. A recovery period of 5 minutes separated each dive. (2) Non-diving conditions Resting and active heart rates of muskrats were obtained during the same filming session i n which voluntary dives were recorded. EKG signals were displayed on a chart recorder when the muskrats appeared to be sleeping (resting condition), and when they were eating, grooming or nest building (active condition). Heart rate was analyzed for 60 seconds p r i o r to voluntary dives. To record the response to a non-diving s t r e s s f u l condition, muskrats were placed i n a wooden box for one hour and l e f t alone in a quiet room. The EKG was recorded during the l a s t ten minutes of t h i s hour. Then, for the next ten minutes, the muskrat was disturbed by drumming on the box and t i l t i n g and moving the box around. During t h i s time the muskrat's EKG was recorded. The recorded EKG signals were then displayed on a chart recorder and converted to BPM. (d) Anatomical Analysis of Data At the conclusion of the experiments a l l muskrats were k i l l e d with an overdose of sodium pentobarbitol. Brains of sham operated and decorticate muskrats were removed and placed i n 10% formaldehyde. The brains were transferred to a 25% sucrose solution for 3-4 days, after which they were photographed, weighed, and measured. Before being weighed, brains were trimmed to remove the spinal cord caudal to the cerebellum, the p a r a f l o c c u l i , and the optic nerves r o s t r a l to the chiasm. Cerebral width was measured at i t s widest point, and length was measured from the posterior edge of the olfactory bulb to the edge of the cortex at the midline. The brains were coronally sectioned (50 p thick) on a freezing microtome and every tenth section was mounted onto a glass s l i d e . The brains were stained with neutral red. The extent of decortication was estimated using a micrograph projector (Microfilm Reader DL II, Zeiss, Jena, German Democratic Republic). A s l i d e image of the brain (dorsal view) was projected onto the screen and the t o t a l area of the cortex was measured. The area of the lesion s i t e was also measured, and a percentage decortication was calculated. The extent of c o r t i c a l lesions and subcortical damage was assessed by comparing muskrat brain sections with a rat brain atlas (Paxinos and Watson 1986), and by comparing dorsal view photographs of the decorticate brains with a dorsal view c o r t i c a l map of a rat ( Z i l l e s and Wree 1985). Brains of sham operated muskrats were s i m i l a r i l y examined. 17 (e) S t a t i s t i c a l Analysis of Data In each diving and non-diving condition, a mean heart rate value for each muskrat was calculated. Generally 10 values per muskrat were averaged; i n some instances when many more than 10 t r i a l s were recorded, 10 values were randomly chosen for analysis. Mean values from each muskrat were averaged to give a grand mean value for each condition. In the text and figures, heart rate values are given as the grand mean +/- standard error of the mean. Within each experimental condition, mean heart rate values from the three diving conditions at the selected dive time were compared using a two-way ANOVA with the aid of a computer s t a t i s t i c a l package (Systat, Systat Inc, Evanston, I l l i n o i s ) . Significance was set at P < 0.05, and i n the case of s i g n i f i c a n t F values, post hoc pair-wise comparisons were made. Other s t a t i s t i c a l comparisons were made using paired Student's t - t e s t s . Semi-logarithmic regressions comparing dive heart rates and time aft e r decortication were generated by transforming the dive heart rates into t h e i r natural log equivalents and using them i n least squares regression analyses. The general form of the regression equation that best f i t the data was y = b e _ m x . 18 RESULTS (a) Heart Rate Responses from Intact Muskrats Heart rates were recorded from eight in t a c t animals. Not a l l dives were of the same duration, as some of the muskrats performed shorter duration voluntary and escape dives. Consequently only the f i r s t 15 seconds of the dive are presented i n the r e s u l t s . Complete dive r e s u l t s are presented i n Appendix 1. Heart rate of res t i n g muskrats was 241 ± 16 BPM. During periods when muskrats were active but not diving (grooming, eating, or nest building) the heart rate was 282 ± 14 BPM. Approximately 30 seconds before voluntary dives, heart rate started to increase to the predive l e v e l (297 + 13 BPM) (see figure 2). Under a l l three diving conditions a substantial bradycardia was observed (see figure 3). The voluntary dive heart rate decreased from 297 ± 13 BPM predive to 130 + 9 BPM at 5 seconds, and then was f a i r l y steady at approximately 115 BPM for the remainder of the dive. In escape dives heart rate was 274 + 17 BPM predive, and dropped to 95 ± 1 8 BPM at 5 seconds. It remainded at thi s l e v e l for the next 10 seconds. In forced dives the heart rate was 273 ± 17 BPM predive, decreased to 74 + 7 BPM at 5 seconds and was steady for the remainder of the dive at Figure 2. Heart rate during rest and a c t i v i t y . Mean heart rate (± SEM) of intact muskrats during rest and a c t i v i t y (grooming, eating, or nest-building), and during the 60 seconds p r i o r to a voluntary dive. Voluntary predive heart rate i s also included. Approximately 30 seconds before voluntary dives, heart rate starts to increase to the predive l e v e l . 20 Figure 2. Heart rate during rest and activity CL CD Ld f -x 400-i 300-200-100 T Resting Active 60 50 40 30 20 10 Voluntary Time (s) before voluntary dive Predive Figure 3. Dive heart rates of inta c t muskrats. Mean heart rates (+ SEM) of inta c t muskrats during voluntary, escape, and forced dives. In a l l three dives there i s a substantial bradycardia upon submersion. Heart rates from the three dives show separation from each other throughout t h e i r duration, but only at 15 seconds into the dive are a l l three s i g n i f i c a n t l y d i f f e r e n t from each other. Dive onset occurs at time =0. ** indicates heart rate i s s i g n i f i c a n t l y d i f f e r e n t from other two heart rates at that time (P < 0.05). Figure 3. Dive heart rates of intact muskrats 0-1 . 1 • • PRE-DWE 0 5 10 1 TIME (s) 23 approximately 55 BPM. There was l i t t l e or no post -dive tachycardia i n any of the condi t ions . During escape dives muskrats tended to dive underneath the wire screens and remain motionless throughout the duration of submergence. This was i n contrast with forced dives i n which the muskrats were cont inua l ly a c t i v e . The voluntary predive heart rate was s i g n i f i c a n t l y higher than i n the other two d iv ing condi t ions . The dive heart rates during the f i r s t 10 seconds of the three dives showed separation from each other, and at 15 seconds into the dive a l l three were s i g n i f i c a n t l y d i f f eren t from each other. Using the predive and dive heart rate at 5 seconds, the absolute and percentage change i n heart rate were ca l cu la ted for the three dive condi t ions . The voluntary, escape, and forced dive condit ions showed a 56%, 65%, and 73% decrease i n heart ra te , r e s p e c t i v e l y . This represents an absolute reduct ion i n heart rate of 168 + 11 BPM, 178 + 19 BPM, and 199 + 16 BPM, re spec t ive ly . Differences i n bradycardia among the three condit ions were not s t a t i s t i c a l l y d i f f e r e n t . Preventing the muskrats from surfac ing at the end of an escape dive (trapping) resu l ted i n a further decrease in heart ra te . The dive heart rate 2 seconds before trapping was 118 + 28 BPM; two seconds af ter trapping the heart rate dropped to 84 + 20 BPM. This decrease was not s i g n i f i c a n t . In fac t , sometimes the heart rate would increase after the animal reached the screen that prevented i t from resurfacing. Disturbing the muskrats i n a non-diving s i t u a t i o n resulted in a s i g n i f i c a n t decrease i n heart rate from 299 + 1 BPM to 259 + 13 BPM, a decrease of 13%. (b) H e a r t Rate Responses from Decorticate and Sham operated  Muskrats Three sham operated and seven decorticate muskrats were used i n t h i s series of experiments. Because voluntary and escape dives were of variable durations, a decreasing number of values were used i n determining heart rate values i n these conditions (see Appendices 2 and 3). One week afte r decortication, the muskrats' appetite had returned, they groomed themselves, b u i l t nests with the available straw, and moved f r e e l y around the concrete recovery/holding tank. Decorticate muskrats appeared to be less aggressive and less wary of humans compared with intact muskrats. They b u i l t less elaborate nests, and were not as good at keeping the nest and surrounding nesting platform clean. They groomed themselves, but t h e i r fur did not seem as well maintained as i n intact muskrats. Sham operated animals tended to be more aggressive and much more wary of humans compared with int a c t muskrats. Upon being approached they often performed long duration escape dives (see appendix 2), with many l a s t i n g over 2 25 minutes. One uninstrumented animal remained motionless under water for 5 minutes 3 seconds. Once i t remained under water for 7.5 minutes out of an 8 minute period, b r i e f l y surfacing only twice, and a second time i t remained under water for 4 minutes 45 seconds out of 5 minutes, again b r i e f l y surfacing twice. The resting heart rate of sham operated muskrats was 170 ± 17 BPM, which rose to 236 + 12 BPM when they became active. In decorticate muskrats, the resting heart rate was 232 + 17 BPM which rose to 275 + 7 when the animals became active. Like intact animals, both the sham operated and decorticate muskrats showed an increase i n heart rate approximately 30 seconds before voluntary dives. Sham operated animals showed s i g n i f i c a n t bradycardia i n a l l three dive conditions. During voluntary dives, the predive heart rate was 274 ± 11 BPM; dive heart rate was 109 + 5 BPM at 5 seconds, and was 113 at 10 seconds (see figure 4 ) . In the escape and forced dive conditions predive heart rates were 238 + 21 BPM and 260 + 8 BPM, respectively. The escape predive heart rate was s i g n i f i c a n t l y lower than those of the other two conditions. Dive heart rates for escape and forced dives were not s i g n i f i c a n t l y d i f f e r e n t from each other, but were s i g n i f i c a n t l y lower than those of the voluntary dives. Dive heart rates of approximately 45 BPM were maintained throughout the duration of escape and forced dives. There was no post-dive tachycardia i n any of the conditions. Figure 4. Dive heart rates of sham operated muskrats. Mean heart rates (+ SEM) of sham operated muskrats during voluntary, escape, and forced dives. In a l l three dives there i s a substantial bradycardia upon submersion. Escape and forced dive heart rates are s i g n i f i c a n t l y lower than voluntary dive heart rate. Dive onset occurs at time =0. ** indicates heart rate i s s i g n i f i c a n t l y d i f f e r e n t from other two heart rates at that time (P < 0.05). Only one value was obtained for voluntary dive at 10 seconds, and was not included i n s t a t i s t i c a l analyses. No voluntary dive lasted 15 seconds. 27 Figure 4. Dive heart rates of sham operated muskrats 04 1 1 . 1 1 PRE-DIVE 0 5 10 15 TIME (s) 28 Decorticate muskrats showed a substantial bradycardia i n a l l three dive conditions. However, afte r decortication the dive heart rates did not show the separation that intact and sham operated animals showed (see figure 5 ) . In a l l dives, heart rates were similar at around 90 BPM; voluntary dive heart rates were s l i g h t l y higher at approximately 105 BPM. However the voluntary dive was only s i g n i f i c a n t l y d i f f e r e n t from the forced dive at 5 seconds into the dive. Predive heart rates for the voluntary, escape, and forced dive conditions were 2 9 5 + 3 , 247 + 7 , and 2 6 3 + 12 BPM, respectively. The voluntary predive heart rate was s i g n i f i c a n t l y higher than the other two conditions. At 5 seconds into the dive, decorticate dive heart rates and the sham operated voluntary dive heart rate were not s t a t i s t i c a l l y d i f f e r e n t from each other. Voluntary predive heart rate from sham operated muskrats was not s i g n i f i c a n t l y d i f f e r e n t from decorticate predive heart rates. Using the predive and dive heart rate at 5 seconds, the percentage changes i n heart rate for the sham operated animals were 60%, 82%, and 80% for the voluntary, escape, and forced dives, respectively. For the decorticate animals, the percentage changes i n heart rate were 64%, 65%, and 70%, respectively. In sham operated animals the voluntary dive condition showed the least absolute heart rate drop (164 + 14 BPM) whereas the escape dive showed a 194 + 19 BPM drop, and the forced dive showed a 208 + 4 BPM Figure 5. Dive heart rates of decorticate muskrats. Mean heart rates (+ SEM) of decorticate muskrats during voluntary, escape, and forced dives. In a l l three dives there i s a substantial bradycardia upon submersion. A l l three dives were similar, dive heart rates being around 90 BPM. Dive onset occurs at time = 0. * indicates heart rate i s s i g n i f i c a n t l y d i f f e r e n t from one other heart rate at that time (P < 0.05). Figure 5. Dive heart rates of decorticate muskrats 0-1 . 1 . . > PRE-DIVE 0 5 10 15 TIME (s) drop. The absolute heart rate drop i n decorticate animals during voluntary dives was 189 + 12 BPM which was s l i g h t l y higher than the 1 6 1 + 7 and 183 + 15 for the escape and forced dives. Preventing sham operated animals from surfacing a f t e r escape dives resulted i n a decrease i n heart rate from 51 + 2 BPM two seconds before trapping to 41 + 2 BPM two seconds afte r trapping, which was not a s t a t i s t i c a l l y s i g n i f i c a n t heart rate change. Preventing decorticate animals from resurfacing resulted i n the heart rate increasing from 91 + 10 BPM to 102 + 17 BPM, which again was not a s t a t i s t i c a l l y s i g n i f i c a n t change i n heart rate. As i n the i n t a c t animals in both sham operated and decorticate muskrats the response to being prevented from resurfacing was quite variable; the heart rate increased as often as i t decreased. Disturbing sham operated animals resulted i n a non-s i g n i f i c a n t 45% decrease i n heart rate from 189 + 4 BPM to 103 + 24 BPM. Disturbing decorticate muskrats resulted i n heart rate decreasing s i g n i f i c a n t l y from 243 + 20 BPM to 19 + 25 BPM, a 19% decrease i n heart rate. At 5 seconds into the forced dive the equation comparing dive heart rate and time aft e r decortication was y = 138e~0*0 7 x w i t h a c o e f f i c i e n t of determination (r^) of 0.83 (see figure 6a). At 10 seconds into the forced dive the equation was y = 152e-0-09x with an r^ of 0.96 (see figure 6b). For decorticate voluntary and escape dives, there were no s i g n i f i c a n t regression r e l a t i o n s h i p s . There Figure 6. Forced dive heart rate as a fuction of weeks after decortication. Mean heart rate (± SEM) of decorticate muskrats at (A) 5 seconds and (B) 10 seconds into a forced dive as a function of weeks afte r decortication. The best f i t equation of the l i n e s and c o e f f i c i e n t of determinations (r^) are given. The l i n e s from sham operated animals are also presented. The decorticates' forced dive heart rate becomes lower with time aft e r decortication, and becomes sim i l a r to that of the sham operated response. Figure 6. Forced dive heart rate as a function of weeks after decortication 33 34 were no s i g n i f i c a n t r e g r e s s i o n r e l a t i o n s h i p s between di v e heart r a t e s and extent of d e c o r t i c a t i o n . In the sham operated animals there was no s i g n i f i c a n t r e l a t i o n s h i p between time a f t e r the sham o p e r a t i o n and d i v e h e a r t r a t e s f o r the v o l u n t a r y , escape, and f o r c e d d i v e s . (c) Anatomical Results Sham operated muskrat b r a i n s appeared t o be a n a t o m i c a l l y undamaged, with the c o r t e x being w e l l v a s c u l a r i z e d . This was confirmed by h i s t o l o g i c a l a n a l y s i s (see f i g u r e 7). This c o n t r a s t s with the d e c o r t i c a t e d animals, which a l l showed evidence of c o r t i c a l l e s i o n i n g (see f i g u r e 7). The extent of the damage v a r i e d among muskrats, r a n g i n g from 22 t o 61 percent of co r t e x removed (see Table 1). The weight of the d e c o r t i c a t e b r a i n s was s i g n i f i c a n t l y l e s s than t h a t of the sham c o n t r o l s , although the dimensions of the b r a i n s were s i m i l a r (see t a b l e 1). In a l l d e c o r t i c a t e muskrats the o c c i p i t a l , p a r i e t a l , f o r e l i m b , and hindlimb c o r t i c a l r e g i o n s were damaged, although i n some muskrats the damage was more e x t e n s i v e than i n others (see f i g u r e s 8-10). The f r o n t a l r e g i o n s were damaged i n a l l but Muskrat 14. The medial a n t e r i o r c i n g u l a t e and r e t r o s p l i n a l r e g i o n s appeared not t o be damaged. The more l a t e r a l i n s u l a r , p e r i r h i n a l , and temporal r e g i o n s a l s o appeared t o be undamaged. Figure 7. Cross sections of sham operated and decorticate muskrat brains. A) Cross section and corresponding drawing of brain from sham operated Muskrat (M28) located at Bregma 0.0. B) Cross section and corresponding drawing of brain from decorticate Muskrat (M20) located at Bregma 0.0. Shaded areas of the drawing correspond to areas of the cortex that were removed. Refer to Table 2 for abbreviations. 37 Table I. Brain measurements and c o r t i c a l damage. Muskrat Brain Width Length Percentage Weight (mm) (mm) C o r t i c a l (g) Damage Ml 4 4 . 62 22 19 22 M20 3.75 20 16 61 M21 3.93 20 19 48 M25 3.71 20 19 51 M27 3.87 21 18 58 M31 3. 91 20 17 47 M33 3.68 19 16 44 M28 4 .27 20 15 — M2 9 4.71 20 19 -M30 4.44 21 16 -The mean weight of decorticate brains was 3.93 + 0.12 g. The mean weight of sham operated brains was 4.47 + 0.13 g. Figure 8. S e r i a l brain cross sections from decorticate Muskrat M14. Dorsal view photograph and drawings of s e r i a l cross sections from Muskrat M14 that had the least (22%) cortex removed. Lines across photograph correspond to location of cross sections. Shaded areas of the drawings indicate c o r t i c a l areas that were removed. A) Located at Bregma +3.5 B) Located at Bregma 0.0 C) Located at Bregma -3.5 D) Located at Bregma -7.0 Refer to Table 2 for abbreviations. Figure 9. S e r i a l bra in cross sections from decort icate Muskrat M31. Dorsal view photograph and drawings of s e r i a l cross sections from Muskrat M31 that had an average amount (47%) of cortex removed. Lines across photograph correspond to l oca t ion of cross sect ions . Shaded areas of the drawings indicate c o r t i c a l areas that were removed. A) Located at Bregma +3.5 B) Located at Bregma 0.0 C) Located at Bregma -3.5 D) Located at Bregma -7.0 Refer to Table 2 for abbreviat ions . F i g u r e 9. S e r i a l b r a i n c r o s s s e c t i o n s f r o m d e c o r t i c a t e M u s k r a t M31. 41 Figure 10. S e r i a l brain cross sections from decorticate Muskrat M20. Dorsal view photograph and drawings of s e r i a l cross sections from Muskrat M20 that had the most (61%) cortex removed. Lines across photograph correspond to location of cross sections. Shaded areas of the drawings indicate c o r t i c a l areas that were removed. A) Located at Bregma +3.5 B) Located at Bregma 0.0 C) Located at Bregma -3.5 D) Located at Bregma -7.0 Refer to Table 2 for abbreviations. 44 Table I I . Abbreviations used i n figures 7-10 • ac anterior commisure Aq aquaduct cc corpus callosum eg cingulum CG central gray CP caudate putamen DG dentate gyrus DV3 dorsal t h i r d v e n t r i c l e ec external capsule fmi forceps minor corpus callosum fm j forceps major corpus callosum IG indusium griseum LV l a t e r a l v e n t r i c l e OF olfactory t r a c t RF r h i n a l f i s s u r e SN septal nucleus 0 45 The forceps minor corpus callosum, cingulum, and external capsule were damaged, and the l a t e r a l v e n t r i c l e was exposed i n a l l muskrats. However, upon gross inspection there appeared to be l i t t l e i f any subcortical damage to any of the muskrats. The p o s s i b i l i t y that there was an interruption of f i b r e t r a c t s between c o r t i c a l regions and subcortical structures was not investigated. 46 DISCUSSION Muskrats exhibited a rapid bradycardia (heart rate declined by greater than 55% of the pre-dive heart rate) upon submergence in a l l dives. Other researchers have reported s i m i l a r decreases i n heart rate during both restrained and unrestrained diving i n muskrat, mink Mustela vison, and beaver Castor canadensis, (Drummond and Jones 1979; Gilbert and Gofton 1982a,b; Jones et al. 1982; West and Van V l i e t 1986; Stephenson et al. 1988; Swain et al. 1988; MacArthur and Karpan 1989). The i n i t i a l bradycardia seen i n a l l dives i n t h i s study was probably a re f l e x response caused by water stimulation of the nasal passages (cf. Drummond and Jones 1979). Bradycardia seen during voluntary dives when the animals were diving of t h e i r own v o l i t i o n and without experimenter intervention was of sim i l a r magnitude to the bradycardia seen during forced dives. This indicates that bradycardia i s not a response to a s t r e s s f u l s i t u a t i o n , but that i t occurs reflexogenically as a consequence of the actual submersion. Disturbing intact muskrats while they were being held in a holding cage resulted i n a 13% decrease i n heart rate. MacArthur and Karpan (1989) found a 38% "alarm" bradycardia in muskrats i n the absence of submersion. This appears to be a c h a r a c t e r i s t i c response of small mammals. In similar situations the heart rate decreased by 12% i n opossum 47 Didelphis marsupialis, (Gabrielsen and Smith 1985), 27% i n woodchucks Marmota monax, (Smith and Woodruff 1980), 29% i n chipmunks Tamias s t r i a t u s , (Smith et al. 1981), 30% i n deer fawns Odocoileus v i r g i n i a n u s , (Jacobson 1979), and 36% i n both rabbits Sylvilagus floridanus, and swamp rabbits S. aquaticus, (Smith and Sweet 1980, Causby and Smith 1981). Swain et al. (1988) found that beavers threatened on land "freeze", and heart rate decreases by 57% i n t h i s situation, although the beavers would have probably escaped into the water had i t been available. In t h i s study the 13% decrease in heart rate could be termed a fear bradycardia, however i t i s no where near as intense as the bradycardia seen during diving. Thus in muskrats, although bradycardia occurs i n response to both diving and threatening situations, the magnitude of the heart rate decline to each i s vastly d i f f e r e n t . This suggests that fear bradycardia and submersion bradycardia are separate physiological responses, evoked by d i f f e r e n t s i t u a t i o n s . Gaunt and Gans (1969) stated that although "withdrawal" and diving bradycardia are independent processes, they can occur simultaneously. Fear bradycardia i s a physiological response to a s t r e s s f u l s i t u a t i o n , but i t i s not the cause of the i n i t i a l bradycardia seen in diving. In in t a c t animals, the three dive heart rates were separated throughout the duration of the dives. With increasingly s t r e s s f u l conditions, there was a tendency 48 towards lower dive heart rates, with voluntary dive heart rates being the highest and forced dive heart rates the lowest. Gilbert and Gofton (1982b) found a s i m i l a r s i t u a t i o n i n the beaver with the bradycardia i n forced dives being much more intense than i n unrestrained dives. Stephenson et al. (1988) found that mink i n novel surroundings had lower dive heart rates compared with dive heart rates when dives were made in f a m i l i a r surroundings. In tufted ducks, escape dive heart rates were sim i l a r to spontaneous (feeding) dive heart rates, but heart rates during involuntary submergence were s i g n i f i c a n t l y lower (Stephenson et al. 1986). Hence i t appears that i n a variety of animals, that increasing the stress of a diving condition results i n lower dive heart rates. Naturally occurring voluntary dives i n most small animals appear to be short i n duration and aerobic i n nature, and do not show the complete cardiovascular adjustments that maximize oxygen conservation (Kooyman et al. 1980). In contrast, animals during forced dives have no control of the dive duration, which possibly could approach the l i m i t s of t h e i r underwater endurance c a p a b i l i t i e s . It therefore would be to t h e i r advantage to evoke metabolic and cardiovascular adjustments (including increased peripheral vasoconstriction and a lowered heart rate) to maximize oxygen conservation and increase underwater endurance. In the present study forced dive heart rates were s i g n i f i c a n t l y lower than those of voluntary dives. This has 49 also been observed i n redhead ducks ( F u r i l l a and Jones 1986). Stephenson et al. (1986) suggested that the stress of the dive condition, which results i n lowered dive heart rates, could be related to the uncertainty of when surface access w i l l next become available. In sham operated muskrats there was a separation of the dive heart rates, although not a gradation as i n intact animals. Escape dive heart rates i n shams were much lower than escape dive heart rates i n intact animals, and were not s i g n i f i c a n t l y d i f f e r e n t from sham forced dive heart rates. Sham operated animals had undergone a major surgical procedure, and may have been able to remember t h i s . Muskrats (Gilbert and Gofton 1982a) and beavers (Swain et al. 1988) both dive into water to escape potential danger. The sham operated animals possibly considered further human contact a pote n t i a l threat to t h e i r well being, and attempted to escape the danger by remaining underwater for as long as possible. Sham operated animals exhibited longer duration escape dives compared with intact animals. They were also much more aggressive towards and wary of humans. Thus, the i n t e n s i f i e d escape dive bradycardia i n the sham operated animals may have been an e f f o r t to maximize underwater endurance. The intense bradycardia of 45 BPM exhibited by sham operated animals during escape dives was sim i l a r to the dive heart rates observed i n unrestrained diving muskrats by Drummond and Jones (1979) and Jones et a l . (1982). Both 50 these studies found that unrestrained diving muskrats had a much lower heart rate than forced dived animals. Jones et al. (1982) concluded that the additional stress of forced diving reduced the a b i l i t y of animals to evoke cardiovascular diving adjustments. Even though the animals were unrestrained, the psychological state of the animals was not f u l l y appreciated. This most l i k e l y was the cause of the i n t e n s i f i e d dive heart rates recorded by Drummond and Jones (1979) and Jones et a l . (1982) during unrestrained diving. In whole animal unanesthetized experiments, the CNS arousal state of the animal must be taken into account, because t h i s can have an e f f e c t upon physiological responses. In contrast with sham operated animals, decorticate muskrats did not show a separation of dive heart rates. A l l three dive heart rates were approximately the same. It would appear that an intact cerebral cortex i s necessary for the d i f f e r e n t i a t i o n i n the dive heart rates. Since a l l three decorticate dive heart rates were the same as the voluntary dive from the sham operated animals, the cortex has the e f f e c t of further lowering the heart rate, and i n t e n s i f y i n g the bradycardia during increasingly s t r e s s f u l conditions (escape and forced dives). Although the i n i t i a l heart rate drop i n a dive may be i n i t i a t e d by nasal receptors, the f i n a l adjustment of the dive heart rate i s dependant upon an intact cortex. The parts of the cortex that were removed, the 51 o c c i p i t a l and p a r i e t a l regions, have not been shown to be d i r e c t l y involved in cardiovascular control i n other animals. For example, no connections towards or from the NTS terminate i n these regions of the cortex i n rats and mice (Saper 1982; van der Kooy et al. 1984). C o r t i c a l areas involved i n autonomic responses i n the rat and mouse are the i n s u l a r cortex (Powell et al. 1985; Ruggiero et al. 1987), medial prefrontal cortex (Buchanan et al. 1985; Verberne et al. 1987; Verberne et al. 1988), and anterior cingulate regions (Lofving 1961; Burns and Wyss 1985). In t h i s study the insular and cingulate regions were not damaged at a l l , and not every muskrat had damage to medial f r o n t a l regions. One muskrat (M14) had no f r o n t a l region damage, and yet showed the same responses as the other decorticate muskrats. Al t e r n a t i v e l y , removal of c o r t i c a l regions may have a general non-specific damaging e f f e c t that interrupts passage of information from the cortex to the NTS, thus temporarily eliminating c o r t i c a l input to the dive response. This hypothesis i s supported by the apparent recovery of function over time that made the forced dive response of decorticate muskrats si m i l a r to that of sham operated muskrats. Perhaps other c o r t i c a l or subcortical regions were taking over t h i s function of the o c c i p i t a l and p a r i e t a l regions. Experiments that should help i n determining the v a l i d i t y of t h i s idea are controlled lesioning of s p e c i f i c c o r t i c a l areas, lesions of d i f f e r i n g sizes, lesioning of animals of varying developmental ages, and t e s t i n g for the forced dive response 52 in the same animal at varying lengths of time aft e r decortication. MacArthur and Karpan (1989) found that exercise attenuates dive bradycardia in muskrats. Contradictory evidence was found in t h i s study. Intact animals exercised vigorously i n forced dives yet had a lower heart rate than i n escape dives when they rested underneath the screens. Furthermore, in sham operated and decorticate animals, escape and forced dive heart rates were the same, even though t h e i r a c t i v i t y l e v e l s were very d i f f e r e n t . The conclusion drawn from t h i s i s that underwater a c t i v i t y does not influence dive heart rates i n muskrats. Although the response was variable, trapping muskrats underwater resulted i n a decrease i n heart rate. This contrasts with trapping tufted ducks where heart rate always immediately dropped to leve l s recorded during involuntary submersion (Stephenson et al. 1986). This a l t e r a t i o n i n dive heart rate indicates posible c o r t i c a l influence upon heart rate during the dive. The heart rate of muskrat and beaver are higher during active behaviour (grooming and swimming) than during less active behaviour (resting and sleeping) (Gilbert and Gofton 1982b; Swain et a l . 1988). This was also found i n intact, decorticate, and sham operated animals i n t h i s study. However, an in t e r e s t i n g question i s why i n sham operated animals t h e i r resting and active heart rates were so much lower than in intact animals. Apparently the ef f e c t s of 53 surgery resulted in a lowered resting heart rate. The predive voluntary heart rate of muskrats i s higher than that of t h e i r active heart rate. Approximately 30 seconds before voluntary dives, heart rates of muskrats star t to increase from the active heart rate to the voluntary predive heart rate. This trend was also seen by MacArthur and Karpan (1989). Butler and Woakes (1979) found in t u fted and pochard ducks that approximately 5 seconds before the f i r s t dive of a diving bout there i s both a tachycardia and hyperventilation, and concluded that t h i s had the ef f e c t of loading oxygen stores before the star t of a diving bout (Butler and Woakes 1979). Possibly oxygen loading accompanies the anticipatory predive tachycardia in muskrats. The active heart rate of muskrats was sim i l a r to that of escape and forced predive heart rates. Butler and Woakes (1979) found no anticipatory "increase i n heart rate in forced dived ducks. Perhaps i n these conditions the animals entered the water before being able to engage i n a preparatory tachycardia. In conclusion, t h i s i s the f i r s t study to date that has investigated the suprabulbar mechanisms involved i n the dive response of spontaneously behaving animals. In previous studies, e l e c t r i c a l stimulation of s p e c i f i c suprabulbar brain areas has resulted in only p a r t i a l manifestation of cardiovascular and respiratory diving adjustments (cf. Butler and Jones 1982). This study provides p o s i t i v e evidence for c o r t i c a l involvement i n the dive response of muskrats, and i t eliminates the contention that bradycardia i s solely fear-induced. 55 REFERENCES Anderson H . 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G.Paxinos), Academic Press, Toronto p375-415 61 Appendix 1 Dive heart rates from intac t muskrats DIVE TIME (s) Voluntary Escape Forced MEAN SEM N MEAN SEM N MEAN SEM N Predive 297 13 8 274 17 7 273 17 7 5 130 9 8 95 18 7 74 7 7 10 113 8 8 95 18 7 63 6 7 15 118 8 8 91 13 7 57 4 7 20 105 15 7 90 21 5 58 4 7 25 102 12 6 84 19 5 54 3 7 30 111 15 5 93 33 5 56 4 7 35 112 10 4 48 10 4 54 4 7 40 145 21 2 62 6 4 56 4 7 45 - - - 48 24 2 57 5 7 50 - - - 35 10 2 55 2 7 55 - - - 68 - 1 54 3 7 60 - - - 61 - 1 58 4 7 Postdive 303 13 8 290 21 7 289 14 7 Grand mean heart rate values and standard error of the mean from N animals. Some muskrats performed shorter durat ion voluntary and escape dives r e s u l t i n g i n decreasing N numbers i n the longer durat ion unrestrained d ives . 62 Appendix 2 Dive heart rates from sham operated muskrats DIVE TIME (s) Voluntary Escape Forced MEAN SEM N MEAN SEM N MEAN SEM N Predive 274 11 3 248 21 3 260 8 3 5 109 5 3 44 3 3 52 4 3 10 113 - 1 46 3 3 55 5 3 15 - - - 38 8 3 42 4 3 20 - - - 37 6 3 42 3 3 25 - - - 39 7 3 47 8 3 30 - - - 37 3 3 40 2 3 35 - - - 42 3 3 44 10 3 40 - - - 41 5 2 49 4 3 45 - - - 39 4 2 48 6 3 50 - - - 39 5 2 48 6 3 55 - - - 34 1 2 45 2 3 60 - - - 38 4 2 45 8 3 Postdive 269 4 3 233 11 3 272 11 3 Grand mean heart rate values and standard error of the mean from N animals. A l l sham operated muskrats performed short duration voluntary dives, while many escape dives lasted over 2 minutes. 63 Appendix 3 Dive heart rates from decort icate muskrats DIVE TIME (s) Voluntary Escape Forced MEAN SEM N MEAN SEM N MEAN SEM N Predive 295 3 7 246 7 7 263 12 6 5 106 8 7 86 9 7 80 10 6 10 101 6 6 84 8 7 75 12 6 15 109 8 2 80 6 5 79 12 6 20 117 - 1 74 5 3 78 15 6 25 - - - 81 13 4 83 18 6 30 - - - 125 - 1 71 11 6 35 - - - 52 - 1 73 10 6 40 - - - - - - 78 11 6 45 - - - - - - 77 11 6 50 - - - - - 82 10 6 55 - - - - - - 86 15 6 60 - - - - - - 82 11 6 Postdive 285 3 7 274 9 7 271 10 6 Grand mean heart rate values and standard error of the mean from N animals. Some muskrats performed shorter durat ion voluntary and escape dives r e s u l t i n g i n decreasing N numbers i n the longer duration unrestrained d ives . 

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