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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., U n i v e r s i t y o f B r i t i s h Columbia, 1983 B . S C , U n i v e r s i t y o f 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 o f Zoology) We accept t h i s t h e s i s as conforming t o the r e q u i r e d standard  THE UNIVERSITY OF BRITISH COLUMBIA August 1989 ® Paul F r e d e r i c k McCulloch, 1989  In  presenting  degree freely  at  this  the  available  copying  of  department publication  of  in  partial  fulfilment  University  of  British  Columbia,  for  this or  thesis  reference  thesis by  this  for  his thesis  and  study.  scholarly  or for  her  financial  of  The University of British Columbia Vancouver, Canada  Date  DE-6 (2/88)  1  I  I further  purposes  t^jj^  gain  the  shall  requirements  agree  that  agree  may  representatives.  permission.  Department  of  be  It not  that  the  Library  by  understood be  an  allowed  the  advanced  shall  permission for  granted  is  for  make  extensive  head  that  without  it  of  copying my  my or  written  ABSTRACT  Force  d i v e d animals undergo c a r d i o v a s c u l a r changes  c h a r a c t e r i z e d by b r a d y c a r d i a , r e s i s t a n c e , and  increased t o t a l peripheral  changes i n b l o o d  these changes occur  i n decerebrated  response must be a brainstem d i v e s , animals may  flow d i s t r i b u t i o n . animals,  reflex.  the  Since  dive  However, i n v o l u n t a r y  show a n t i c i p a t o r y b r a d y c a r d i a  and  may  a l s o a d j u s t t h e i r c a r d i o v a s c u l a r responses a c c o r d i n g a n t i c i p a t e d d i v e d u r a t i o n , i n d i c a t i n g suprabulbar upon d i v e  to  influences  responses.  Studies of heart r a t e u s i n g t e l e m e t r y t h e r e can be  have shown t h a t  s u b s t a n t i a l d i f f e r e n c e s i n the d i v e response of  v o l u n t a r i l y and  f o r c e d i v e d animals.  Furthermore, some  animals show a " f e a r b r a d y c a r d i a " when trapped stressful situation, that bradycardia  l e a d i n g some r e s e a r c h e r s to suggest  d u r i n g f o r c e d submersion i s an a r t i f a c t  the s t r e s s of the  zibethica)  were observed  freely  d i v i n g f o r food i n an indoor tank u s i n g a v i d e o camera VCR  unit.  EKG  on the audio  was  telemetered  from the animals and  channel of the VCR  tape.  t o v o l u n t a r y d i v e s were analyzed from escape and a l s o recorded  forced dives.  and  and  recorded  Heart r a t e responses compared with  those  Heart r a t e responses were  from d e c o r t i c a t e and  sham operated  muskrats to  e l u c i d a t e the r o l e t h a t the c e r e b r a l cortex p l a y s i n the d i v e response.  of  situation.  (Ondatra  Muskrats  in a  In a l l types of d i v e s , muskrats e x h i b i t e d a r a p i d and large bradycardia g r e a t e r than 55%  upon submergence  of the p r e d i v e heart r a t e ) .  diving bradycardia s t r e s s , but There was  i n the muskrat was  occurred  not due  no evidence of p o s t - d i v e t a c h y c a r d i a  a non-diving  Obviously t o f e a r or  as a response t o submersion p e r  a n t i c i p a t o r y immersion b r a d y c a r d i a . in  (heart r a t e d e c l i n e d by  se.  or  D i s t u r b i n g the animal  s i t u a t i o n r e s u l t e d i n only a 13% decrease i n  heart r a t e . In i n t a c t animals v o l u n t a r y , escape, and  forced  submergence r e s u l t e d i n p r o g r e s s i v e l y g r e a t e r decreases i n heart r a t e . in  Heart r a t e f e l l by  escape d i v e s , and  of the b r a d y c a r d i a v o l u n t a r y d i v e s was  73%  56%  i n voluntary dives,  i n forced dives.  Intensification  to a lower heart r a t e than t h a t seen i n mediated by the c e r e b r a l cortex,  heart r a t e i n d e c o r t i c a t e muskrats i n escape and d i v e s d i d not  as  forced  f a l l below t h a t seen i n v o l u n t a r y d i v e s .  i n d i c a t e s t h a t the  However, i n  d e c o r t i c a t e muskrats t h e r e appeared t o be a recovery  of  cortical  in  f u n c t i o n , as i n t e n s i f i c a t i o n of b r a d y c a r d i a  a f t e r surgery.  dependent upon the time t h a t had  " '  This  f i n a l adjustment of d i v e heart r a t e i s  dependent upon an i n t a c t c e r e b r a l c o r t e x .  f o r c e d d i v e s was  65%  elapsed  This  study shows t h a t t h e r e i s a c o r t i c a l  upon the c a r d i o v a s c u l a r i n d i c a t e s that the  system during  diving.  influence It also  i n experiments with u n a n e s t h e t i z e d animals,  degree of s t r e s s of the s i t u a t i o n must be taken i n t o  account, as t h i s may a f f e c t p h y s i o l o g i c a l  responses.  V  TABLE OF CONTENTS ABSTRACT LIST OF TABLES LIST OF FIGURES ACKNOWLEDGEMENTS INTRODUCTION METHODS a) S u r g i c a l Procedures 1) EKG T r a n s m i t t e r I m p l a n t a t i o n 2) D e c o r t i c a t i o n b) Recording Techniques c) E x p e r i m e n t a l P r o t o c o l 1) Types o f d i v e s i) V o l u n t a r y d i v e s i i ) Escape d i v e s i i i ) Trapped d i v e s iv) Forced d i v e s 2) Non-diving c o n d i t i o n s d) Anatomical A n a l y s i s o f data e) S t a t i s t i c a l A n a l y s i s o f Data RESULTS a) Heart Rate Responses from I n t a c t Muskrats b) Heart Rate Responses from D e c o r t i c a t e and Sham Operated Muskrats c) Anatomical R e s u l t s DISCUSSION REFERENCES APPENDIX 1 APPENDIX 2 APPENDIX 3 .-  i i vi v i i viii 1 7 10 10 11 12 13 13 13 14 14 14 15 15 17 18 18  .  24 34 46 55 61 62 63  vi List  of Tables  Table I  B r a i n Measurements and C o r t i c a l Damage  37  Table I I  A b b r e v i a t i o n s used i n F i g u r e s 7-10  44  vii List  of Figures  Figure 1  Diagram o f d i v i n g tank  Figure 2  Heart r a t e s d u r i n g r e s t and a c t i v i t y  19  Figure 3  Dive heart r a t e s of i n t a c t muskrats  21  Figure 4  Dive heart r a t e s o f sham operated  Figure 5  Dive heart r a t e s o f d e c o r t i c a t e muskrats  29  Figure 6  Forced d i v e heart r a t e s as a f u n c t i o n o f weeks a f t e r d e c o r t i c a t i o n  32  Cross s e c t i o n s o f sham operated and d e c o r t i c a t e muskrat b r a i n s  35  S e r i a l b r a i n c r o s s s e c t i o n s from d e c o r t i c a t e Muskrat M14  38  S e r i a l b r a i n c r o s s s e c t i o n s from d e c o r t i c a t e Muskrat M31  40  F i g u r e 10 S e r i a l b r a i n c r o s s s e c t i o n s from d e c o r t i c a t e Muskrat M20  42  Figure 7 Figure 8 Figure  9  8  muskrats  ...  26  viii ACKNOWLEDGEMENTS  I thank Dr. David Jones enthusiasm  for this project.  f o r h i s help, guidance, and I a l s o thank Dr. Geoff  Gabbott  f o r h i s h e l p with the f i g u r e s , Mike Hedrick and Dr. Peter B u s h n e l l f o r t h e i r help with s t a t i s t i c s ,  Dr. R i c h a r d Tees  and L u c i l l e Hoover f o r t h e i r h e l p w i t h the d e c o r t i c a t i o n procedure,  and my c o l l e a g u e s i n t h e l a b o f Dr. Jones f o r  t h e i r help and c r i t i c i s m s throughout I am g r a t e f u l  the y e a r s .  f o r the Teaching A s s i s t a n t s h i p s I  r e c e i v e d from the Department of Zoology.  1  INTRODUCTION  Upon e n f o r c e d submergence a i r b r e a t h i n g animals invoke c e r t a i n c a r d i o v a s c u l a r changes  as p a r t of an  oxygen  c o n s e r v i n g mechanism known as the d i v e response Jones 1 9 8 2 ) .  ( B u t l e r and  During submersion, a r t e r i a l b l o o d p r e s s u r e i s  m a i n t a i n e d w h i l e c a r d i a c output i s reduced and p e r i p h e r a l resistance i s increased changes the  ( B u t l e r and Jones 1982).  There are  i n b l o o d flow d i s t r i b u t i o n s w i t h i n c r e a s e d flow t o  heart and CNS  and a decreased flow t o l e s s  oxygen  s e n s i t i v e t i s s u e s such as muscles and abdominal (Zapol et al.  1979/  Jones et al.  1982).  organs  The marker which  has been used most f r e q u e n t l y t o i n d i c a t e the onset of these c a r d i o v a s c u l a r events d u r i n g submersion i s rate  (Andersen 1963a; Dykes  decreased heart  1974).  The p h y s i o l o g i c a l responses t o r e s t r a i n e d d i v i n g are medullary r e f l e x e s s i n c e the c a r d i o v a s c u l a r adjustments t o d i v i n g can be e l i c i t e d i n d e c e r e b r a t e ducks Gabbott and Jones 1985) 1979).  and muskrats  (Andersen 1963b;  (Drummond and  However, i t has been known s i n c e 1940  suprabulbar r e g i o n s  (those areas o f the CNS  Jones  that  above the pons  and medulla) can a f f e c t the d i v e response as Scholander (1940) observed t h a t s e a l s can show an a n t i c i p a t o r y  diving  b r a d y c a r d i a and a decrease i n heart r a t e due t o t h r e a t e n i n g g e s t u r e s by the r e s e a r c h e r . The nucleus t r a c t u s s o l i t a r i u s  (NTS)  i n the medulla i s  c o n s i d e r e d t o be the primary i n t e g r a t i o n s i t e of  2 cardiovascular  information  et al.  (Galosy  1981/ Spyer 1982).  The  N T S r e c e i v e s d i r e c t a f f e r e n t p r o j e c t i o n s from systemic  and  pulmonary a r t e r i a l b a r o r e c e p t o r s ,  arterial  chemoreceptors, and pulmonary s t r e t c h r e c e p t o r s v i a c r a n i a l et al.  nerves IX and X (Galosy  1981), and from upper  r e s p i r a t o r y passages v i a c r a n i a l nerve V (Korner 1979). NTS i s a l s o i n v o l v e d i n e f f e r e n t c a r d i o v a s c u l a r it  The  c o n t r o l as  sends p r o j e c t i o n s t o the d o r s a l motor nucleus of the (DMV) i n the medulla and t o the i n t e r m e d i o l a t e r a l  vagus  nucleus  (ILN) of the s p i n a l cord,  the s i t e s o f o r i g i n of the  c a r d i o v a s c u l a r parasympathetic and sympathetic neurons, r e s p e c t i v e l y  (Galosy  et al.  1981).  preganglionic  Direct  suprabulbar p r o j e c t i o n s t o the NTS a l s o a r i s e from l i m b i c and  c o r t i c a l regions  (Saper 1982; van der Kooy et al.  I t i s from these higher  1984).  CNS l e v e l s t h a t c e n t r a l m o d i f i c a t i o n  of the dive response c o u l d be made. Conditioning  experiments have i m p l i e d a r o l e o f the CNS  i n the c o n t r o l of heart C l a s s i c a l heart californianus, can  ducks  (cf.  Galosy et  al.  r a t e c o n d i t i o n i n g i n sea l i o n s  1981). Zalophus  can produce a more i n t e n s e b r a d y c a r d i a  immersion  attenuate  rate  (Ridgeway et al.  than  1975), and h a b i t u a t i o n may  or completely e l i m i n a t e d i v i n g b r a d y c a r d i a i n  (Gabrielsen  1985; Gabbott and Jones 1985; Gabbott and  Jones 1987). It i s p o s s i b l e t h a t the d i v e response r o u t i n e l y i n v o l v e s some form of a s s o c i a t i v e l e a r n i n g 1982).  ( B u t l e r and Jones  V o l u n t a r i l y d i v i n g harbour s e a l s Phoca  vitulina,  and  3 t u f t e d ducks Aythya  may show a n t i c i p a t o r y  fuligvla,  b r a d y c a r d i a b e f o r e immersion and an i n c r e a s e i n heart before resurfacing  (Scholander 1940; Jones et al.  B u t l e r and Woakes 1982). Leptonychotes  weddelli,  rate  1973;  Animals such as Weddell s e a l s and t u f t e d ducks A.  fuligula,  may  a l s o a d j u s t the i n t e n s i t y of c a r d i o v a s c u l a r responses a c c o r d i n g t o the a n t i c i p a t e d d i v e l e n g t h or d u r a t i o n (Kooyman and Campbell 1972; H i l l al.  et al.  1983; Stephenson et  1986). The " p s y c h o l o g i c a l c o n d i t i o n " or " s t a t e of a r o u s a l " o f  an animal can have an important e f f e c t upon the d i v e response  ( B u t l e r and Jones 1982; Gabbott and Jones 1987).  The d i s p o s i t i o n and nervous s t a t e of s e a l s i s important f o r f u l l development 1941).  of the d i v e b r a d y c a r d i a  al.  ( I r v i n g et  "Calm" ducks a l s o show a much b e t t e r response than  "alarmed" ducks  (Folkow et a l 1967) .- In humans,  " p r e o c c u p a t i o n " or mental a c t i v i t y  (mental a r i t h m e t i c )  almost completely a t t e n u a t e s the d i v e response (Ross and Steptoe 1980, Wolf 1978) w h i l e f e a r or a n x i e t y may the b r a d y c a r d i a  enhance  (Wolf 1978).  The p o r t i o n o f the b r a i n thought t o be most i n v o l v e d w i t h emotional e x p e r i e n c e and e x p r e s s i o n i s the l i m b i c system, which c o n s i s t s o f the hippocampus, and hypothalamus  ( H i l t o n 1982).  amygdala,  septum,  Limbic s t r u c t u r e s have  e x t e n s i v e c o n n e c t i o n s w i t h the NTS, and might mediate the c a r d i o v a s c u l a r changes observed i n emotional s i t u a t i o n s and d u r i n g p e r i o d s of s t r e s s  (Swanson 1982).  4 EKGs t e l e m e t e r e d from f r e e l y d i v i n g animals have shown t h a t t h e r e can be s u b s t a n t i a l d i f f e r e n c e s i n c a r d i a c responses t o v o l u n t a r y and f o r c e d d i v i n g . working with t u f t e d A. fuligula, ferina,  Researchers  and pochard ducks A.  ( B u t l e r and Woakes, 1979), Canada geese  canadensis, auritus,• aquaticus, Alligator Caiman  Phalacrocorax  and double c r e s t e d cormorants (Kanwisher  et al.  1981),  crocodilus,  Sylvalagus  swamp r a b b i t s  (Smith and Tobey 1983), American mississippiensis,  Branta  (Smith et al.  alligators  1974),  and caimans  (Gaunt and Gans 1969) have r e p o r t e d a  s u b s t a n t i a l decrease i n h e a r t r a t e d u r i n g e n f o r c e d d i v e s , but found l i t t l e  or no b r a d y c a r d i a d u r i n g v o l u n t a r y d i v e s .  This i s quite d i f f e r e n t  from the " c l a s s i c a l " f o r c e d d i v e  response as o u t l i n e d by Andersen In  c o n t r a s t t o the a c t i v e  (1966).  ( f i g h t or f l i g h t )  defence  response, some animals show an a l t e r n a t i v e response when faced w i t h a t h r e a t e n i n g s t i m u l u s .  Small prey animals, when  caught i n a s i 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 o f escape, have a tendency t o remain m o t i o n l e s s and h i d e i n an- e f f o r t to  avoid detection  ( G a b r i e l s e n et a l . 1977; Jacobsen 1979;  G a b r i e l s o n and Smith 1985).  In t h i s s i t u a t i o n these animals  show a r e d u c t i o n i n h e a r t r a t e which i s known as a " f e a r " bradycardia  (Gab'rielsen et al.  1977) .  The defense r e a c t i o n i s c o n t r o l l e d by an area l o c a t e d in  the p o s t e r o l a t e r a l hypothalamus and e l e c t r i c a l  s t i m u l a t i o n o f t h i s area r e s u l t s i n a defense response (Galosy et al.  1981), which may i n c l u d e the a p p r o p r i a t e  5 behavioural actions for f l i g h t ,  t h r e a t or a t t a c k  (Spyer  1984).  " P l a y i n g dead", with a drop i n heart and r e s p i r a t o r y  rates,  i s c o n s i d e r e d t o be a second type of defence response  (Hilton  1982).  Until recently,  studies investigating  diving  b r a d y c a r d i a have mainly i n v o l v e d f o r c e d d i v e d animals.  This  has r a i s e d doubts as t o whether the b r a d y c a r d i a seen d u r i n g submersion i s due t o submersion alone, or whether experimental a r t i f a c t  caused by the emotional  s i t u a t i o n of the e n f o r c e d submersion Kanwisher  et al.  1981).  i t i s an  ("fearful")  (Gaunt and Gans  Some r e s e a r c h e r s have even  1969; stated  t h a t d i v i n g b r a d y c a r d i a i s s o l e l y f e a r - i n d u c e d and a r e s u l t of the methods used t o study the p h y s i o l o g i c a l responses t o d i v i n g i n the l a b o r a t o r y  (Smith and De Carvalho 1985).  However the f o l l o w i n g evidence counters the argument t h a t i n v o l u n t a r y submersion b r a d y c a r d i a i s a defence Naive d a b b l i n g ducks Anas platyrhynchos,  response. 100% oxygen  ( F u r i l l a and Jones 1986;  and redhead ducks A.  americana,  a p p l i e d t o t h e i r n a s a l mucosa  given  Gabbott and Jones  having l o c a l  anesthetic  ( F u r i l l a and Jones 1986)  t o show a f o r c e d d i v e b r a d y c a r d i a .  1987)  fail  Presumably they should  have e x p e r i e n c e d the same amount of " f e a r " as u n t r e a t e d ducks.  Secondly, t h e r e appears t o be d i f f e r e n t  efferent  mechanisms i n v o l v e d i n the c o n t r o l of f e a r and d i v e bradycardias Finally,  (Causby and Smith 1981;  Smith and Tobey  d e c e r e b r a t e animals show a d i v e response  1983).  (Andersen  1963b; Drummond and Jones 1979; Gabbott and Jones 1987),  and  6 they  are " f a i r l y  difficult  ( B l i x and Folkow 1 9 8 4 ) .  to scare"  Although t h i s evidence  supports  of the d i v e response, higher CNS  the r e f l e x o g e n i c b a s i s  l e v e l s are undoubtedly  i n v o l v e d i n the c a r d i o v a s c u l a r responses to d i v i n g . areas  of the cortex  (the i n s u l a r , medial p r e f r o n t a l , and  a n t e r i o r c i n g u l a t e regions) the NTS  van  der Kooy et al.  s t i m u l a t i o n of these changes 1985; al.  areas  (Lofving 1961;  Powell 1987;  have e x t e n s i v e connections  i n the r a t and mouse (Saper 1982;  Neafsey 1983;  et al.  1984)  Buchanan et al.  1985;  Verberne et al.  Terreberry and  1988).  i n t e n t of t h i s study was  1985;  Burns and Wyss  The  Verberne et  connections  provide  non-diving. t o i n v e s t i g a t e the  submersion i s a f e a r - i n d u c e d defence response. of the d i v e response of the muskrat Ondatra  sham  forced  Comparisons  zibethica,  f o r c e d d i v e s were made.  the d i v e response from d e c o r t i c a t e and recorded.  a  modulate c a r d i o v a s c u l a r  c o n t e n t i o n t h a t the b r a d y c a r d i a which occurs d u r i n g  muskrats was  and  electrical  Ruggiero et a l 1987;  f u n c t i o n i n g d u r i n g both d i v i n g and  v o l u n t a r y , escape, and  to  can produce c a r d i o v a s c u l a r  route by which c o r t i c a l a c t i v i t y may  The  Certain  in  Furthermore,  operated  These experiments have e l u c i d a t e d  the r o l e the cortex p l a y s i n the d i v e response and i n d i c a t e d to  what degree the cortex can a f f e c t  functioning.  cardiovascular  7 METHODS  Experiments {Ondatra  were c a r r i e d out on 18 a d u l t muskrats  zibethica)  o f both sexes,  0.673 t o 1.320 kg.  ranging i n weight  from  The muskrats, trapped i n the v i c i n i t y o f  Richmond, Surrey, and D e l t a B.C., were h e l d i n the U n i v e r s i t y animal h o l d i n g f a c i l i t y b e f o r e b e i n g t r a n s f e r r e d t o two concrete tanks  (155 X 60 X 80 cm) i n the B i o l o g i c a l  Sciences B u i l d i n g where a l l experiments  were performed.  One  tank was u s u a l l y dry and used as a temporary h o l d i n g and recovery u n i t while the other c o n t a i n e d the d i v i n g (see f i g u r e 1 ) . 40 cm.  set-up  The depth o f water i n the tank was h e l d at  H o r i z o n t a l and v e r t i c a l sub-surface wire mesh  c r e a t e d a 2 m (4m round t r i p ) t u n n e l t h a t the muskrats were r e q u i r e d t o swim through t o reach food p l a c e d on the bottom of the p o o l .  A 50 X 35 cm p l a t f o r m at one end o f the p o o l  p r o v i d e d a n e s t i n g area f o r the muskrats.  Straw or wood  shavings served as bedding  During t h e  experiments  i n both t a n k s .  the animals were f e d unmedicated P u r i n a Rabbit  Chow and water ad libitum.  D i e t was supplemented with  apples, c a r r o t s , and on o c c a s i o n l e t t u c e and c e l e r y .  8  F i g u r e 1. Diagram of d i v i n g tank. Diagram of c o n c r e t e tank used d u r i n g d i v i n g experiments. Refer t o t e x t f o r details.  ©CKU.1t  F i g u r e 1.  Diagram of d i v i n g tank.  10 (a) S u r g i c a l  (1) EKG  Procedures  T r a n s m i t t e r Implantation  A m o d i f i e d design of a Narco Biosystems Ont.)  EKG t r a n s m i t t e r was  spontaneously  behaving  used t o r e c o r d heart r a t e from  muskrats.  After attaching a 3 volt  l i t h i u m b a t t e r y , the t r a n s m i t t e r was  embedded i n t i s s u e  and then covered with a s i l i c o n e s e a l a n t . procedures  sodium p e n t o b a r b i t o l (Somnotol,  Pharmaceuticals,  M i s s i s s a u g a Ont.)  intraperitoneally after i n i t i a l e t h e r or Halothane Montreal).  The  (Downsview  was  wax  For a l l s u r g i c a l MTC  injected  s e d a t i o n by i n h a l a t i o n of  (Fluothane, A y e r s t L a b o r a t o r i e s ,  initial  dose of Somnotol, 40-50 mg'kg ,  was  -1  supplemented as r e q u i r e d .  Fur was  c l i p p e d from the area  where the i n c i s i o n s were t o be made, and the exposed s k i n swabbed with a t o p i c a l germicide Frederick, Toronto). (Xylocaine 2%,  (Betadine, Purdue  A f t e r i n j e c t i o n of l o c a l a n e s t h e t i c  A s t r a Pharmaceuticals, M i s s i s s a u g a ,  Ont.),  i n c i s i o n s were made over the sternum, and abdomen j u s t caudal t o the r i b cage.  A subcutaneous pocket was  formed on  the v e n t r a l s u r f a c e of the abdomen t o h o l d the t r a n s m i t t e r . From t h i s pocket the EKG subdermally t i s s u e was  t r a n s m i t t e r leads were threaded  t o the sternum i n c i s i o n .  The o v e r l y i n g muscle  t e a s e d 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 p i e r c e d with an intravenous c a t h e t e r placement u n i t Utah).  The  (20 gauge; Desderet  M e d i c a l Inc. Sandy,  i n t r a c a t h served as a guide along which the  EKG  11  leads were i n t r o d u c e d i n t o the t h o r a c i c c a v i t y .  The  leads  were sutured i n p l a c e , and anchored with i n s t a n t bond cement ( H i s t o a c r y l , B.Braun Melsungen AG, The  Melsungen, West Germany).  i n c i s i o n s were then c l o s e d and reswabbed with  t o p i c a l germicide. u n t i l i t recovered  The muskrat was  kept  the  i n a c a r r y i n g cage  from the a n a e s t h e t i c and then  was  r e t u r n e d t o the concrete p o o l .  (2) D e c o r t i c a t i o n Muskrats were a n e s t h e t i z e d with sodium p e n t o b a r b i t o l and p l a c e d i n a s t e r e o t a x i c head-holder Scientific, was  Tokyo, Japan).  The  (Narishigi  f u r on the top of the head  c l i p p e d , and the exposed area swabbed with  germicide.  A 3 cm  the s k u l l .  The  i n c i s i o n was  topical  made along the m i d l i n e of  temporal muscle was  retracted laterally  expose most of the p a r i e t a l and p a r t s of the f r o n t a l squamosal bones.  Using a d e n t a l d r i l l ,  two  1 cm^  and  skull  p i e c e s were removed t o expose the d o r s o l a t e r a l aspects the c e r e b r a l hemispheres.  A narrow s t r i p of bone was  over the s u p e r i o r s a g i t a l s i n u s . dura, was  the exposed neocortex  was  of left  A f t e r r e t r a c t i o n of the removed by a s p i r a t i o n .  taken not t o a s p i r a t e deeper than the corpus  although the l a t e r a l v e n t r i c l e was C o r t i c a l removal was  to  Care  callosum,  exposed i n every  muskrat.  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, c a u d a l l y towards the o c c i p i t a l cortex, m e d i a l l y towards the m i d l i n e , 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 c o n t r o l l e d with absorbant Don M i l l s ,  g e l a t i n sponges  (Gelfoam, Upjohn,  Ont.) or m i c r o f i b r i l l a r c o l l a g e n hemostat  (Avitene, Avicon,  Humancao, Puerto R i c o ) .  The s c a l p wound  was then sutured and reswabbed with the t o p i c a l  germicide.  The muskrat was g i v e n an i n t r a m u s c u l a r a n t i b i o t i c  injection  ( O x y t e t r a c y c l i n e h y d r o c h l o r i d e , Rogar/ST, Montreal; mg/kg)  to  and l e f t  t o recover overnight b e f o r e being  the dry concrete  45-65  returned  tank.  Sham d e c o r t i c a t i o n s f o l l o w e d the same o p e r a t i v e and recovery procedures c o r t e x was l e f t  (b) Recording  as the d e c o r t i c a t i o n s , except t h a t the  intact.  Techniques  Behaviour  o f the animals was recorded on a VCR u n i t  (HR-S20U, JVC Canada Inc, Scarborough, Ont.) with a v i d e o camera  (GX-N4UT, JVC Canada Inc, Scarborough, Ont.).  The  EKG s i g n a l was r e c e i v e d by a communication r e c e i v e r . (ICR7000, ICOM, Osaka, Japan) and recorded on the audio of  the VCR tape.  h i g h speed.  A f t e r an experiment the tape was viewed at  When a d i v e occurred, the tape was slowed, and  the EKG was d i s p l a y e d on a pen r e c o r d e r . r a t e s were averaged immediately  channel  over the 5-10 second  p r e c e d i n g the d i v e .  P r e - d i v e heart interval  Instantaneous  d i v e heart  r a t e s at s e l e c t e d time d u r i n g the d i v e s were determined  by  c a l c u l a t i n g the average of two adjacent c a r d i a c i n t e r v a l s (although on o c c a s i o n only one c a r d i a c i n t e r v a l was used)  13 and  c o n v e r t i n g t h i s t o beats per minute  (BPM).  In non-  d i v i n g c o n d i t i o n s , heart r a t e s were c a l c u l a t e d by c o n v e r t i n g the number of EKG s i g n a l s obtained d u r i n g 10 second p e r i o d s into  BPM.  (c) Experimental  Protocol  (1) Types of d i v e s (i) V o l u n t a r y procedures,  dives.  One t o two weeks b e f o r e any s u r g i c a l  i n t a c t muskrats were p l a c e d i n the d i v i n g tank  t o a c c l i m a t e t o t h e i r surroundings.  I t was d u r i n g t h i s time  t h a t they were t r a i n e d t o d i v e f o r food on the bottom of the tank. The EKG t r a n s m i t t e r was then implanted 3 days the experiments began. muskrat were recorded present.  Voluntary  and a f t e r 2 t o  d i v e s by the  i n a q u i e t room with no r e s e a r c h e r  The VCR r e c o r d i n g apparatus and r a d i o r e c e i v e r  were p o s i t i o n e d t o f i l m the muskrats as they  dived  spontaneously f o r submerged food. D e c o r t i c a t e and sham operated  muskrats were  r e i n t r o d u c e d t o water about a week a f t e r d e c o r t i c a t i o n . They were housed on a p l a t f o r m i n the h o l d i n g tank, and the water l e v e l i n the tank was then r a i s e d i n steps over a 3 day p e r i o d .  When they were swimming competently, they were  t r a n s f e r r e d t o the d i v e tank and t r a i n e d t o d i v e underneath the screens. not take  I t was found t h a t d e c o r t i c a t e animals would  submerged food, but they would r e a d i l y  f l o a t i n g food.  take  Consequently, the end of the d i v e  tunnel  14 that was f u r t h e s t  from the n e s t i n g p l a t f o r m was open t o the  s u r f a c e which r e s u l t e d i n a s h o r t e r d i v e path opposed t o 4 m f o r the i n t a c t a n i m a l s ) .  (2 m as  Sham operated  animals were exposed t o the same shortened d i v e path as the d e c o r t i c a t e d animals.  Once d e c o r t i c a t e d and sham operated  animals were t r a i n e d t o d i v e , the experimental p r o t o c o l was s i m i l a r t o that  ( i i ) Escape  for intact  dives.  animals.  These d i v e s were caused by d i s t u r b a n c e s  such as n o i s e s and/or gestures made by the r e s e a r c h e r . animal was u n r e s t r a i n e d and perhaps  The  mimicked the behaviour  of muskrats escaping a p r e d a t o r i n the w i l d .  A recovery  p e r i o d of 5 minutes separated each d i v e .  (iii)  Trapped  dives.  The muskrat was trapped underwater  a f t e r f i r s t performing an escape prevented  dive.  The muskrat was  from r e s u r f a c i n g by p l a c i n g a screen across the  mouth o f the underwater t u n n e l .  The o b j e c t o f t h i s p r o t o c o l  was t o r e c o r d any a l t e r a t i o n i n the heart r a t e o f the muskrat a f t e r i t became t r a p p e d . approximately  10 seconds  The screen was removed  a f t e r the animal became aware t h a t  i t was trapped, thus a l l o w i n g i t t o r e s u r f a c e .  (iv) Forced d i v e s . cm wire cage.  Muskrats  were p l a c e d i n a 30 X 30 X 100  The cage and muskrat were then  underwater f o r 60 seconds.  lowered  The s i z e of the cage allowed the  muskrat t o move about, but they c o u l d not c o n t r o l the onset  15 or d u r a t i o n separated  of the d i v e .  p e r i o d o f 5 minutes  each d i v e .  (2) Non-diving Resting obtained  A recovery  conditions  and a c t i v e heart  r a t e s o f muskrats were  d u r i n g the same f i l m i n g s e s s i o n i n which  d i v e s were recorded. recorder  EKG s i g n a l s were d i s p l a y e d on a chart  when the muskrats appeared t o be s l e e p i n g  condition), building  voluntary  (resting  and when they were e a t i n g , grooming or nest  (active condition).  seconds p r i o r t o v o l u n t a r y  Heart r a t e was analyzed  f o r 60  dives.  To r e c o r d the response t o a non-diving c o n d i t i o n , muskrats were p l a c e d alone i n a q u i e t room.  stressful  i n a wooden box f o r one hour  and  left  The EKG was recorded  the  l a s t t e n minutes of t h i s hour.  during  Then, f o r the next t e n  minutes, the muskrat was d i s t u r b e d by drumming on the box and  t i l t i n g and moving the box around.  muskrat's EKG was recorded.  During t h i s time the  The recorded  then d i s p l a y e d on a chart r e c o r d e r  EKG s i g n a l s were  and converted t o BPM.  (d) Anatomical A n a l y s i s of Data  At the c o n c l u s i o n killed  o f the experiments a l l muskrats were  w i t h an overdose o f sodium p e n t o b a r b i t o l .  B r a i n s of  sham operated and d e c o r t i c a t e muskrats were removed and placed  i n 10% formaldehyde.  The b r a i n s were t r a n s f e r r e d t o  a 25% sucrose s o l u t i o n f o r 3-4 days, a f t e r which they were  photographed, weighed, and measured.  Before b e i n g weighed,  b r a i n s were trimmed to remove the  s p i n a l cord caudal t o  cerebellum, the p a r a f l o c c u l i ,  the  t o the  chiasm.  point,  and  Cerebral  l e n g t h was  and  width was  measured from the p o s t e r i o r edge of  The b r a i n s were c o r o n a l l y  a glass s l i d e . The  The  s i t e was  thick)  every t e n t h s e c t i o n was  midline.  on a  mounted onto  projected was  estimated using  ( M i c r o f i l m Reader DL  German Democratic R e p u b l i c ) .  cortex  at the  b r a i n s were s t a i n e d w i t h n e u t r a l  micrograph p r o j e c t o r  area of the  cortex  (50 p  sectioned  extent of d e c o r t i c a t i o n was  (dorsal view) was  o p t i c nerves r o s t r a l  measured at i t s widest  t h e o l f a c t o r y bulb to the edge of the  f r e e z i n g microtome and  the  measured.  a l s o measured, and  The  a  I I , Z e i s s , Jena,  A s l i d e image of the onto the  red.  screen and  brain  the  area of the  total  lesion  a percentage d e c o r t i c a t i o n  was  calculated. The was  extent of c o r t i c a l  assessed by  brain atlas  l e s i o n s and  s u b c o r t i c a l damage  comparing muskrat b r a i n s e c t i o n s with a r a t  (Paxinos and Watson 1986), and  by  comparing  d o r s a l view photographs of the d e c o r t i c a t e b r a i n s w i t h a d o r s a l view c o r t i c a l map Brains  of a r a t  ( Z i l l e s and Wree 1985).  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  A n a l y s i s of Data  In each d i v i n g and non-diving r a t e value  c o n d i t i o n , a mean heart  f o r each muskrat was c a l c u l a t e d .  G e n e r a l l y 10  v a l u e s p e r muskrat were averaged; i n some i n s t a n c e s when many more than  10 t r i a l s were recorded,  randomly chosen f o r a n a l y s i s .  10 v a l u e s were  Mean values  from each muskrat  were averaged t o g i v e a grand mean value f o r each c o n d i t i o n . In the t e x t and f i g u r e s , heart r a t e v a l u e s are given as the grand mean +/- standard e r r o r o f the mean. experimental  Within  each  c o n d i t i o n , mean heart r a t e v a l u e s from the  t h r e e d i v i n g c o n d i t i o n s at the s e l e c t e d d i v e time were compared u s i n g a two-way ANOVA with the a i d o f a computer statistical  package  (Systat, S y s t a t Inc, Evanston,  Illinois).  S i g n i f i c a n c e was s e t at P < 0.05, and i n the  case o f s i g n i f i c a n t F v a l u e s , post hoc p a i r - w i s e were made.  Other s t a t i s t i c a l  p a i r e d Student's  comparisons  comparisons were made u s i n g  t-tests.  Semi-logarithmic  r e g r e s s i o n s comparing d i v e heart r a t e s  and time a f t e r d e c o r t i c a t i o n were generated  by t r a n s f o r m i n g  the d i v e heart r a t e s i n t o t h e i r n a t u r a l l o g e q u i v a l e n t s and u s i n g them i n l e a s t squares r e g r e s s i o n a n a l y s e s .  The  g e n e r a l form o f t h e r e g r e s s i o n equation t h a t best f i t the data was  y = be  _ m x  .  18 RESULTS  (a) Heart Rate Responses from I n t a c t Muskrats  Heart r a t e s were recorded Not  from e i g h t i n t a c t  animals.  a l l d i v e s were o f the same d u r a t i o n , as some o f the  muskrats performed s h o r t e r d u r a t i o n v o l u n t a r y and escape dives.  Consequently only the f i r s t  are presented presented  i n the r e s u l t s .  15 seconds o f the d i v e  Complete d i v e r e s u l t s are  i n Appendix 1.  Heart r a t e o f r e s t i n g muskrats was 241 ± 16 BPM. During  p e r i o d s when muskrats were a c t i v e but not d i v i n g  (grooming, e a t i n g , or nest b u i l d i n g ) the heart r a t e was 282 ± 14 BPM.  Approximately 30 seconds b e f o r e v o l u n t a r y  heart r a t e s t a r t e d t o i n c r e a s e t o the p r e d i v e l e v e l 13 BPM)  dives, (297 +  (see f i g u r e 2 ) .  Under a l l t h r e e d i v i n g c o n d i t i o n s a s u b s t a n t i a l b r a d y c a r d i a was observed heart r a t e decreased  (see f i g u r e 3 ) . The v o l u n t a r y  dive  from 297 ± 13 BPM p r e d i v e t o 130 + 9  BPM at 5 seconds, and then was f a i r l y steady at approximately  115 BPM f o r the remainder o f the d i v e .  In  escape d i v e s heart r a t e was 274 + 17 BPM p r e d i v e , and dropped t o 95 ± 1 8 BPM at 5 seconds. l e v e l f o r the next 10 seconds.  I t remainded at t h i s  In f o r c e d d i v e s the heart  r a t e was 273 ± 17 BPM p r e d i v e , decreased seconds and was steady  t o 74 + 7 BPM at 5  f o r the remainder o f t h e d i v e at  F i g u r e 2. Heart r a t e d u r i n g r e s t activity.  and  Mean heart r a t e (± SEM) of i n t a c t muskrats d u r i n g r e s t and a c t i v i t y (grooming, e a t i n g , or n e s t - b u i l d i n g ) , and d u r i n g the 60 seconds p r i o r t o a v o l u n t a r y d i v e . V o l u n t a r y p r e d i v e heart r a t e i s a l s o i n c l u d e d . Approximately 30 seconds b e f o r e v o l u n t a r y d i v e s , heart r a t e s t a r t s t o i n c r e a s e t o the p r e d i v e level.  20  Figure 2. Heart rate during rest and activity 400-i  CL CD  300-  Ld  f-  T  200-  x  100  Resting Active 60 50 40 30 20 10 Voluntary Time (s) before voluntary dive Predive  F i g u r e 3. Dive heart r a t e s of i n t a c t muskrats. Mean heart r a t e s (+ SEM) o f i n t a c t muskrats d u r i n g v o l u n t a r y , escape, and f o r c e d d i v e s . In a l l t h r e e d i v e s t h e r e i s a s u b s t a n t i a l b r a d y c a r d i a upon submersion. Heart r a t e s from the t h r e e d i v e s show s e p a r a t i o n from each other throughout t h e i r d u r a t i o n , but only at 15 seconds i n t o the d i v e are a l l t h r e e 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 . ** i n d i c a t e s heart r a t e 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 r a t e s at t h a t time (P < 0.05).  Figure 3. Dive heart rates of intact muskrats  0-1  . PRE-DWE  1 0  • 5  TIME (s)  10  • 1  23 approximately 55 BPM.  There was l i t t l e  t a c h y c a r d i a i n any of the  or no p o s t - d i v e  conditions.  During escape dives muskrats tended to d i v e underneath the wire screens and remain motionless d u r a t i o n of submergence.  throughout the  T h i s was i n c o n t r a s t w i t h f o r c e d  d i v e s i n which the muskrats were c o n t i n u a l l y The v o l u n t a r y p r e d i v e heart r a t e was  active.  significantly  h i g h e r than i n the other two d i v i n g c o n d i t i o n s . heart r a t e s d u r i n g the f i r s t  The d i v e  10 seconds of the t h r e e  showed s e p a r a t i o n from each o t h e r ,  and at 15 seconds  the d i v e a l l t h r e e were s i g n i f i c a n t l y d i f f e r e n t  dives into  from each  other. Using the p r e d i v e and d i v e heart r a t e at 5 seconds, absolute  and percentage  change i n h e a r t r a t e were  f o r the t h r e e d i v e c o n d i t i o n s .  i n heart r a t e ,  respectively.  calculated  The v o l u n t a r y , escape,  f o r c e d d i v e c o n d i t i o n s showed a 56%,  the  and  65%, and 73% decrease  This represents  an absolute  r e d u c t i o n i n h e a r t r a t e of 168 + 11 BPM, 178 + 19 BPM, and 199 + 16 BPM, r e s p e c t i v e l y .  Differences  among the t h r e e c o n d i t i o n s were not  in bradycardia  statistically  different. P r e v e n t i n g the muskrats from s u r f a c i n g at the end of an escape d i v e heart r a t e .  (trapping)  r e s u l t e d i n a f u r t h e r decrease  The d i v e heart r a t e 2 seconds b e f o r e t r a p p i n g  was 118 + 28 BPM; two seconds a f t e r t r a p p i n g the heart dropped to 84 + 20 BPM. In f a c t ,  in  T h i s decrease was not  rate  significant.  sometimes the heart r a t e would i n c r e a s e  after  the  animal reached the screen t h a t prevented i t from resurfacing. D i s t u r b i n g the muskrats  i n a non-diving s i t u a t i o n  r e s u l t e d i n a s i g n i f i c a n t decrease i n h e a r t r a t e from 299 + 1 BPM  (b)  t o 259 + 13 BPM,  Heart  a decrease of 13%.  Rate Responses from D e c o r t i c a t e and Sham operated  Muskrats  Three sham operated and seven d e c o r t i c a t e muskrats were used i n t h i s s e r i e s of experiments.  Because v o l u n t a r y and  escape d i v e s were o f v a r i a b l e d u r a t i o n s , a d e c r e a s i n g number of v a l u e s were used i n d e t e r m i n i n g h e a r t r a t e v a l u e s i n these c o n d i t i o n s  (see Appendices  2 and 3).  One week a f t e r d e c o r t i c a t i o n , the muskrats'  appetite  had r e t u r n e d , they groomed themselves, b u i l t n e s t s w i t h the a v a i l a b l e straw, and moved f r e e l y around the c o n c r e t e r e c o v e r y / h o l d i n g tank.  D e c o r t i c a t e muskrats  appeared t o be  l e s s a g g r e s s i v e and l e s s wary of humans compared w i t h i n t a c t muskrats.  They b u i l t  l e s s e l a b o r a t e n e s t s , a n d were not as  good at keeping the nest and surrounding n e s t i n g p l a t f o r m clean.  They groomed themselves, but t h e i r f u r d i d not seem  as w e l l maintained as i n i n t a c t  muskrats.  Sham operated animals tended t o be more a g g r e s s i v e and much more wary o f humans compared with i n t a c t  muskrats.  Upon b e i n g approached they o f t e n performed l o n g d u r a t i o n escape d i v e s (see appendix 2), with many l a s t i n g over 2  25  minutes.  One uninstrumented animal remained  under water f o r 5 minutes 3 seconds.  motionless  Once i t remained under  water f o r 7.5 minutes out o f an 8 minute p e r i o d , s u r f a c i n g only twice,  briefly  and a second time i t remained under  water f o r 4 minutes 45 seconds out o f 5 minutes,  again  b r i e f l y surfacing twice. The  r e s t i n g heart r a t e o f sham operated  muskrats was  170 ± 17 BPM, which rose t o 236 + 12 BPM when they active.  became  In d e c o r t i c a t e muskrats, the r e s t i n g heart r a t e was  232 + 17 BPM which rose t o 275 + 7 when t h e animals became active.  L i k e i n t a c t animals,  both the sham operated and  d e c o r t i c a t e muskrats showed an i n c r e a s e i n heart approximately  30 seconds b e f o r e v o l u n t a r y  Sham operated  rate  dives.  animals showed s i g n i f i c a n t b r a d y c a r d i a i n  a l l three dive conditions.  During  v o l u n t a r y d i v e s , the  p r e d i v e heart r a t e was 274 ± 11 BPM; d i v e heart r a t e was 109 + 5 BPM at 5 seconds, and was 113 at 10 seconds 4).  (see f i g u r e  In the escape and f o r c e d d i v e c o n d i t i o n s p r e d i v e  r a t e s were 238 + 21 BPM and 260 + 8 BPM,  respectively.  escape p r e d i v e heart r a t e was s i g n i f i c a n t l y lower than of the other two c o n d i t i o n s . and  voluntary dives. were maintained dives.  The those  Dive heart r a t e s f o r escape  f o r c e d d i v e s were not s i g n i f i c a n t l y d i f f e r e n t  other, but were s i g n i f i c a n t l y  heart  lower than those  from each  o f the  Dive heart r a t e s o f approximately  45 BPM  throughout t h e d u r a t i o n o f escape and f o r c e d  There was no p o s t - d i v e t a c h y c a r d i a i n any o f the  conditions.  F i g u r e 4. Dive heart r a t e s o f sham operated muskrats. Mean heart r a t e s (+ SEM) o f sham operated muskrats d u r i n g v o l u n t a r y , escape, and f o r c e d d i v e s . In a l l t h r e e dives there i s a s u b s t a n t i a l bradycardia upon submersion. Escape and f o r c e d d i v e heart r a t e s are s i g n i f i c a n t l y lower than v o l u n t a r y d i v e heart r a t e . Dive onset occurs at time = 0 . ** i n d i c a t e s heart r a t e 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 r a t e s at t h a t time (P < 0.05). Only one v a l u e was obtained f o r v o l u n t a r y d i v e at 10 seconds, and was not i n c l u d e d i n s t a t i s t i c a l analyses. No v o l u n t a r y d i v e l a s t e d 15 seconds.  27  Figure 4. Dive heart rates of sham operated muskrats  04  1  PRE-DIVE  1  .  1  1  0  5  10  15  TIME (s)  28 D e c o r t i c a t e muskrats showed a s u b s t a n t i a l b r a d y c a r d i a i n a l l three dive c o n d i t i o n s .  However, a f t e r d e c o r t i c a t i o n  the d i v e heart r a t e s d i d not show the s e p a r a t i o n t h a t and  sham operated  animals showed  intact  (see f i g u r e 5 ) . In a l l  d i v e s , heart r a t e s were s i m i l a r at around 90 BPM;  voluntary  d i v e heart r a t e s were s l i g h t l y h i g h e r at approximately BPM.  However the v o l u n t a r y d i v e was only  105  significantly  from the f o r c e d d i v e at 5 seconds i n t o the d i v e .  different  P r e d i v e heart 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 c o n d i t i o n s were 2 9 5 + 3 , respectively.  247 + 7,  and 2 6 3 + 12 BPM,  The v o l u n t a r y p r e d i v e heart r a t e was  s i g n i f i c a n t l y h i g h e r than the other two c o n d i t i o n s . At 5 seconds i n t o the d i v e , d e c o r t i c a t e d i v e heart r a t e s and the sham operated  v o l u n t a r y d i v e heart r a t e were  not  from each other.  s t a t i s t i c a l l y different  p r e d i v e heart r a t e from sham operated significantly different  Voluntary  muskrats was not  from d e c o r t i c a t e p r e d i v e  heart  rates. Using the p r e d i v e and d i v e heart r a t e at 5 seconds, the percentage changes i n heart r a t e f o r t h e sham  operated  animals were 60%, 82%, and 80% f o r t h e v o l u n t a r y , and  forced dives, r e s p e c t i v e l y .  animals, and  F o r the d e c o r t i c a t e  t h e percentage changes i n heart r a t e were 64%, 65%,  70%, r e s p e c t i v e l y .  In sham operated  animals t h e  v o l u n t a r y d i v e c o n d i t i o n showed the l e a s t a b s o l u t e r a t e drop 194  escape,  heart  ( 1 6 4 + 14 BPM) whereas the escape d i v e showed a  + 19 BPM drop, and the f o r c e d d i v e showed a 2 0 8 + 4 BPM  F i g u r e 5. Dive heart r a t e s of d e c o r t i c a t e muskrats. Mean heart r a t e s (+ SEM) of d e c o r t i c a t e muskrats d u r i n g v o l u n t a r y , escape, and f o r c e d d i v e s . In a l l t h r e e d i v e s t h e r e i s a s u b s t a n t i a l b r a d y c a r d i a upon submersion. A l l t h r e e d i v e s were s i m i l a r , d i v e heart r a t e s being around 90 BPM. Dive onset occurs at time = 0. * i n d i c a t e s heart r a t e 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 r a t e at t h a t time (P < 0.05).  Figure 5. Dive heart rates of decorticate muskrats  0-1  . PRE-DIVE  1 0  .  .  5  10  TIME (s)  > 15  drop.  The  absolute  during voluntary higher  than the  forced  dives.  heart  r a t e drop i n d e c o r t i c a t e animals  d i v e s was 161+7  Preventing  189  and  + 12 BPM  183  which was  + 15 f o r the escape  seconds before  after trapping, heart  not  Preventing  a statistically  significant  + 17 BPM,  i n both sham operated and t o being heart  rate.  As  not  significant  a  i n the  statistically intact  d e c o r t i c a t e muskrats the  prevented from r e s u r f a c i n g was  rate increased  seconds  r a t e i n c r e a s i n g from 91 +  which again was  change i n heart  two  d e c o r t i c a t e animals from  r e s u r f a c i n g r e s u l t e d i n the heart t o 102  r a t e from 51 +  t r a p p i n g t o 41 + 2 BPM  which was  r a t e change.  10 BPM  and  sham operated animals from s u r f a c i n g a f t e r  escape d i v e s r e s u l t e d i n a decrease i n heart 2 BPM two  slightly  animals response  q u i t e v a r i a b l e ; the  as o f t e n as i t decreased.  D i s t u r b i n g sham operated animals r e s u l t e d i n a nons i g n i f i c a n t 45% 103  decrease i n heart  + 24 BPM.  heart  a 19%  significantly  decrease i n heart  At 5 seconds i n t o the comparing d i v e heart y = 138e~0*0 0.83  7x w  ith  the e q u a t i o n was  t h e r e were no  from 243  + 20 BPM  to  to  f o r c e d dive the  equation  a c o e f f i c i e n t of determination At  10 seconds i n t o the  y = 152e-0-09  x  19  rate.  r a t e and time a f t e r d e c o r t i c a t i o n  (see f i g u r e 6a).  f i g u r e 6b).  + 4 BPM  D i s t u r b i n g d e c o r t i c a t e muskrats r e s u l t e d i n  rate decreasing  + 25 BPM,  r a t e from 189  (r^) of  forced  w i t h an r ^ of 0.96  For d e c o r t i c a t e v o l u n t a r y  and  was  dive (see  escape d i v e s ,  s i g n i f i c a n t regression relationships.  There  F i g u r e 6. Forced dive heart r a t e as a f u c t i o n of weeks a f t e r d e c o r t i c a t i o n . Mean heart r a t e (± SEM) o f d e c o r t i c a t e muskrats at (A) 5 seconds and (B) 10 seconds i n t o a f o r c e d d i v e as a f u n c t i o n of weeks a f t e r d e c o r t i c a t i o n . The best f i t equation o f the l i n e s and c o e f f i c i e n t o f d e t e r m i n a t i o n s (r^) are given. The l i n e s from sham operated animals are a l s o p r e s e n t e d . The d e c o r t i c a t e s ' f o r c e d d i v e heart r a t e becomes lower with time a f t e r d e c o r t i c a t i o n , and becomes s i m i l a r t o t h a t 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 heart  r e g r e s s i o n r e l a t i o n s h i p s between d i v e  r a t e s and extent  operated  of d e c o r t i c a t i o n .  a n i m a l s t h e r e was  between t i m e  In t h e sham  no s i g n i f i c a n t r e l a t i o n s h i p  after  t h e sham o p e r a t i o n  and d i v e h e a r t  for the voluntary,  escape, and f o r c e d  dives.  (c)  Anatomical  Results  Sham o p e r a t e d anatomically  the cortex being  T h i s was c o n f i r m e d  f i g u r e 7).  The e x t e n t  ranging  Table 1 ) .  significantly  less  the  dimensions  all  decorticate  and  hindlimb  of c o r t i c a l lesioning  o f t h e damage v a r i e d among  o f t h e sham c o n t r o l s ,  o f t h e b r a i n s were s i m i l a r muskrats t h e o c c i p i t a l , regions  figures  8-10).  Muskrat  14.  regions  a p p e a r e d n o t t o be damaged.  be  The  frontal  The m e d i a l  perirhinal,  undamaged.  was although  (see t a b l e 1 ) . parietal,  regions  than  In  forelimb,  were damaged, a l t h o u g h  m u s k r a t s t h e damage was more e x t e n s i v e  insular,  o f c o r t e x removed  of the decorticate brains  than that  cortical  analysis  the decorticated  f r o m 22 t o 61 p e r c e n t  The w e i g h t  well  by h i s t o l o g i c a l  w h i c h a l l showed e v i d e n c e  muskrats, (see  a p p e a r e d t o be  f i g u r e 7). This c o n t r a s t s with  animals, (see  muskrat b r a i n s  undamaged, w i t h  vascularized. (see  rates  i n others  i n some (see  were damaged i n a l l b u t  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  and t e m p o r a l  The more  regions  lateral  a l s o appeared t o  F i g u r e 7. Cross s e c t i o n s o f sham operated and d e c o r t i c a t e muskrat b r a i n s . A) Cross s e c t i o n and c o r r e s p o n d i n g drawing o f b r a i n from sham operated Muskrat (M28) l o c a t e d at Bregma 0.0. B) Cross s e c t i o n and c o r r e s p o n d i n g drawing o f b r a i n from d e c o r t i c a t e Muskrat (M20) l o c a t e d at Bregma 0.0. Shaded areas o f the drawing correspond t o areas o f the cortex t h a t were removed. Refer t o Table 2 f o r a b b r e v i a t i o n s .  37 Table I.  B r a i n measurements and c o r t i c a l damage.  Muskrat  Brain Weight (g)  Ml 4 M20 M21 M25 M31 M33  4 . 62 3.75 3.93 3.71 3.87 3. 91 3.68  22 20 20 20 21 20 19  19 16 19 19 18 17 16  22 61 48 51 58 47 44  M28 M2 9 M30  4 .27 4.71 4.44  20 20 21  15 19 16  —  M27  Width (mm)  Length (mm)  Percentage Cortical Damage  --  The mean weight o f d e c o r t i c a t e b r a i n s was 3.93 + 0.12 g. The mean weight of sham operated b r a i n s was 4.47 + 0.13 g.  F i g u r e 8. S e r i a l b r a i n c r o s s s e c t i o n s from d e c o r t i c a t e Muskrat M14. D o r s a l view photograph and drawings o f s e r i a l c r o s s s e c t i o n s from Muskrat M14 t h a t had the l e a s t (22%) cortex removed. L i n e s across photograph correspond t o l o c a t i o n of c r o s s s e c t i o n s . Shaded areas of the drawings i n d i c a t e c o r t i c a l areas t h a t 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 t o Table 2 f o r a b b r e v i a t i o n s .  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 from d e c o r t i c a t e Muskrat M31. D o r s a l view photograph and drawings of s e r i a l c r o s s s e c t i o n s from Muskrat M31 t h a t had an average amount (47%) of c o r t e x removed. L i n e s across photograph correspond to l o c a t i o n of c r o s s s e c t i o n s . Shaded areas of the drawings i n d i c a t e c o r t i c a l areas t h a t 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 f o r  abbreviations.  41 Figure  9.  S e r i a l brain cross sections d e c o r t i c a t e Muskrat M31.  from  F i g u r e 10. S e r i a l b r a i n c r o s s s e c t i o n s from d e c o r t i c a t e Muskrat M20. D o r s a l view photograph and drawings o f s e r i a l c r o s s s e c t i o n s from Muskrat M20 t h a t had the most (61%) cortex removed. L i n e s across photograph correspond t o l o c a t i o n o f c r o s s s e c t i o n s . Shaded areas of the drawings i n d i c a t e c o r t i c a l areas t h a t 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 t o Table 2 f o r a b b r e v i a t i o n s .  44  Table I I . A b b r e v i a t i o n s used i n 7-10 • ac Aq cc eg CG CP DG DV3 ec fmi fm j IG LV OF RF SN  figures  a n t e r i o r commisure aquaduct corpus callosum cingulum c e n t r a l gray caudate putamen dentate gyrus dorsal t h i r d ventricle e x t e r n a l capsule f o r c e p s minor corpus callosum f o r c e p s major corpus callosum indusium griseum lateral ventricle olfactory tract rhinal fissure s e p t a l 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  t h e r e appeared t o be l i t t l e of the muskrats. interruption subcortical  i f any s u b c o r t i c a l  The p o s s i b i l i t y that  inspection damage t o any  t h e r e was an  of f i b r e t r a c t s between c o r t i c a l r e g i o n s and structures  was not  investigated.  46 DISCUSSION  Muskrats e x h i b i t e d a r a p i d b r a d y c a r d i a  (heart r a t e  d e c l i n e d by g r e a t e r than 55% o f the p r e - d i v e heart upon submergence i n a l l d i v e s . r e p o r t e d s i m i l a r decreases  rate)  Other r e s e a r c h e r s have  i n heart r a t e d u r i n g  both  r e s t r a i n e d and u n r e s t r a i n e d d i v i n g i n muskrat, mink vison,  and beaver Castor  1979;  G i l b e r t and Gofton  and Van V l i e t 1988;  canadensis,  Mustela  (Drummond and Jones  1982a,b; Jones et al. 1982; West  1986; Stephenson et al. 1988; Swain et al.  MacArthur and Karpan 1989). The  i n i t i a l b r a d y c a r d i a seen i n a l l d i v e s i n t h i s  was probably  a r e f l e x response caused by water s t i m u l a t i o n  of the n a s a l passages Bradycardia  study  ( c f . Drummond and Jones 1979).  seen d u r i n g v o l u n t a r y d i v e s when t h e animals  were d i v i n g o f t h e i r own v o l i t i o n and without  experimenter  i n t e r v e n t i o n was o f s i m i l a r magnitude t o t h e b r a d y c a r d i a seen d u r i n g f o r c e d d i v e s .  This i n d i c a t e s that bradycardia  i s not a response t o a s t r e s s f u l s i t u a t i o n , but t h a t i t occurs r e f l e x o g e n i c a l l y as a consequence o f t h e a c t u a l submersion. D i s t u r b i n g i n t a c t muskrats while they were b e i n g h e l d i n a h o l d i n g cage r e s u l t e d i n a 13% decrease MacArthur and Karpan  i n heart r a t e .  (1989) found a 38% "alarm"  i n muskrats i n the absence of submersion.  T h i s appears t o  be a c h a r a c t e r i s t i c response o f small mammals. s i t u a t i o n s t h e heart r a t e decreased  bradycardia  In s i m i l a r  by 12% i n opossum  47 Didelphis  marsupialis,  woodchucks Marmota  (Gabrielsen and Smith 1985), 27% i n monax,  (Smith and Woodruff 1980), 29% i n  chipmunks Tamias  striatus,  fawns Odocoileus  virginianus,  both r a b b i t s Sylvilagus aquaticus,  (Smith et al. 1981), 30% i n deer (Jacobson  floridanus,  1979), and 36% i n  and swamp r a b b i t s S.  (Smith and Sweet 1980, Causby and Smith 1981).  Swain et al. (1988) found t h a t beavers threatened  on land  " f r e e z e " , and heart r a t e decreases  situation,  by 57% i n t h i s  although the beavers would have probably water had i t been a v a i l a b l e .  escaped i n t o the  In t h i s study t h e 13% decrease  i n heart r a t e c o u l d be termed a f e a r b r a d y c a r d i a , however i t i s no where near as i n t e n s e as the b r a d y c a r d i a seen d u r i n g diving. Thus i n muskrats, although b r a d y c a r d i a occurs i n response t o both d i v i n g and t h r e a t e n i n g s i t u a t i o n s , the magnitude o f the heart r a t e d e c l i n e t o each i s v a s t l y different.  T h i s suggests  t h a t f e a r b r a d y c a r d i a and  submersion b r a d y c a r d i a are separate p h y s i o l o g i c a l responses, evoked by d i f f e r e n t s t a t e d t h a t although  situations. "withdrawal"  independent processes,  Gaunt and Gans (1969) and d i v i n g b r a d y c a r d i a a r e  they can occur s i m u l t a n e o u s l y .  b r a d y c a r d i a i s a p h y s i o l o g i c a l response t o 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 t h e cause o f the i n i t i a l b r a d y c a r d i a seen i n d i v i n g . In i n t a c t animals,  the t h r e e d i v e heart r a t e s were  separated throughout the d u r a t i o n o f t h e d i v e s .  With  i n c r e a s i n g l y s t r e s s f u l c o n d i t i o n s , t h e r e was a tendency  Fear  48 towards lower dive heart r a t e s , with v o l u n t a r y d i v e heart r a t e s being the h i g h e s t and  f o r c e d dive heart r a t e s the  lowest.  (1982b) found a s i m i l a r  G i l b e r t and Gofton  s i t u a t i o n i n the beaver with the b r a d y c a r d i a  i n forced dives  being much more i n t e n s e than i n u n r e s t r a i n e d d i v e s . Stephenson et al. surroundings  had  (1988) found t h a t mink i n novel lower d i v e heart r a t e s compared with  heart r a t e s when d i v e s were made i n f a m i l i a r  dive  surroundings.  In t u f t e d ducks, escape d i v e heart r a t e s were s i m i l a r t o spontaneous  (feeding) d i v e heart r a t e s , but heart  rates  d u r i n g i n v o l u n t a r y submergence were s i g n i f i c a n t l y  lower  (Stephenson et al.  1986).  v a r i e t y of animals,  Hence i t appears t h a t i n a  t h a t i n c r e a s i n g the s t r e s s of a d i v i n g  c o n d i t i o n r e s u l t s i n lower d i v e heart r a t e s . N a t u r a l l y o c c u r r i n g v o l u n t a r y d i v e s i n most small animals appear t o be short i n d u r a t i o n and a e r o b i c i n nature,  and do not show the complete c a r d i o v a s c u l a r  adjustments t h a t maximize oxygen c o n s e r v a t i o n al.  1980).  (Kooyman et  In c o n t r a s t , animals d u r i n g f o r c e d d i v e s have no  c o n t r o l of the d i v e d u r a t i o n , which p o s s i b l y c o u l d 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 . t h e r e f o r e would be t o t h e i r advantage to evoke metabolic c a r d i o v a s c u l a r adjustments v a s o c o n s t r i c t i o n and oxygen c o n s e r v a t i o n In the present  It and  (including increased peripheral  a lowered heart rate) t o maximize and  i n c r e a s e underwater endurance.  study  f o r c e d d i v e heart r a t e s were  s i g n i f i c a n t l y lower than those  of v o l u n t a r y d i v e s .  This  has  49 a l s o been observed i n redhead ducks 1986).  ( F u r i l l a and Jones  Stephenson et al. (1986) suggested t h a t the s t r e s s  of the d i v e c o n d i t i o n , which r e s u l t s i n lowered d i v e heart r a t e s , c o u l d be r e l a t e d t o the u n c e r t a i n t y of when s u r f a c e access w i l l next become a v a i l a b l e . In sham operated dive heart animals.  muskrats t h e r e was a s e p a r a t i o n of the  r a t e s , although  not a g r a d a t i o n as i n i n t a c t  Escape d i v e heart r a t e s i n shams were much lower  than escape d i v e heart  r a t e s i n i n t a c t animals,  significantly different Sham operated  and were not  from sham f o r c e d d i v e heart r a t e s .  animals had undergone a major s u r g i c a l  procedure, and may have been able t o remember t h i s . Muskrats  ( G i l b e r t and Gofton 1982a) and beavers  (Swain et  al.  1988) both d i v e i n t o water t o escape p o t e n t i a l danger.  The  sham operated  animals p o s s i b l y c o n s i d e r e d  f u r t h e r human  c o n t a c t a p o t e n t i a l t h r e a t t o t h e i r w e l l being, and attempted t o escape the danger by remaining as long as p o s s i b l e .  Sham operated  underwater f o r  animals e x h i b i t e d longer  d u r a t i o n escape d i v e s compared w i t h i n t a c t animals.  They  were a l s o much more a g g r e s s i v e towards and wary o f humans. Thus, the i n t e n s i f i e d escape d i v e b r a d y c a r d i a operated  i n the sham  animals may have been an e f f o r t t o maximize  underwater endurance. The operated  intense bradycardia  of 45 BPM e x h i b i t e d by sham  animals d u r i n g escape d i v e s was s i m i l a r t o the d i v e  heart r a t e s observed i n u n r e s t r a i n e d d i v i n g muskrats by Drummond and Jones  (1979) and Jones et a l . (1982).  Both  50 these  s t u d i e s found t h a t u n r e s t r a i n e d d i v i n g muskrats had  much lower heart r a t e than f o r c e d d i v e d animals. al.  (1982) concluded  a  Jones et  t h a t the a d d i t i o n a l s t r e s s of f o r c e d  d i v i n g reduced the a b i l i t y of animals to evoke c a r d i o v a s c u l a r d i v i n g adjustments.  Even though the  were u n r e s t r a i n e d , the p s y c h o l o g i c a l s t a t e of the was  not  fully  of the Jones  appreciated.  T h i s most l i k e l y was  animals  animals the cause  i n t e n s i f i e d d i v e heart r a t e s recorded by Drummond (1979) and  diving.  Jones et a l . (1982) d u r i n g  In whole animal u n a n e s t h e t i z e d  and  unrestrained  experiments, the  CNS  a r o u s a l s t a t e of the animal must be taken i n t o account, because t h i s can have an e f f e c t upon p h y s i o l o g i c a l responses. In c o n t r a s t with sham operated  animals,  decorticate  muskrats d i d not show a s e p a r a t i o n of d i v e heart r a t e s . t h r e e d i v e heart r a t e s were approximately  the same.  All  It  would appear t h a t an i n t a c t c e r e b r a l cortex i s necessary the d i f f e r e n t i a t i o n i n the d i v e heart r a t e s .  Since a l l  t h r e e d e c o r t i c a t e d i v e heart r a t e s were the same as v o l u n t a r y d i v e from the sham operated  animals,  the  has the e f f e c t of f u r t h e r lowering the heart r a t e , i n t e n s i f y i n g the b r a d y c a r d i a conditions  (escape and  the cortex and  during i n c r e a s i n g l y s t r e s s f u l  forced dives).  heart r a t e drop i n a d i v e may  be  Although the  i n i t i a t e d by  initial  nasal  r e c e p t o r s , the f i n a l adjustment of the d i v e heart r a t e i s dependant upon an i n t a c t The  for  cortex.  p a r t s of the cortex t h a t were removed, the  51 occipital  and p a r i e t a l r e g i o n s , have not been shown t o  be  d i r e c t l y i n v o l v e d i n c a r d i o v a s c u l a r c o n t r o l i n other animals. NTS mice  For example, no connections  terminate  i n these  (Saper 1982;  van  towards or from the  regions of the cortex i n r a t s der Kooy et al.  1984).  and  Cortical  areas  i n v o l v e d i n autonomic responses i n the r a t and mouse are i n s u l a r cortex  (Powell et al.  medial p r e f r o n t a l cortex al.  1987;  regions  the i n s u l a r and  Ruggiero et al.  (Buchanan et al.  Verberne et al. ( L o f v i n g 1961;  1985;  1988), and  1985;  muskrat  1987),  Verberne et  anterior cingulate  Burns and Wyss 1985).  In t h i s  study  c i n g u l a t e regions were not damaged at a l l ,  and not every muskrat had damage t o medial f r o n t a l One  the  (M14)  had no  regions.  f r o n t a l r e g i o n damage, and  yet  showed the same responses as the other d e c o r t i c a t e muskrats. Alternatively,  removal of c o r t i c a l r e g i o n s may  have a  g e n e r a l n o n - s p e c i f i c damaging e f f e c t t h a t i n t e r r u p t s passage of i n f o r m a t i o n  from the cortex t o the NTS,  thus t e m p o r a r i l y  e l i m i n a t i n g c o r t i c a l input t o the d i v e response. hypothesis  i s supported  by the apparent recovery  This of f u n c t i o n  over time t h a t made the f o r c e d d i v e response o f d e c o r t i c a t e muskrats s i m i l a r t o t h a t of sham operated  muskrats.  Perhaps  other c o r t i c a l or s u b c o r t i c a l regions were t a k i n g over t h i s f u n c t i o n of the o c c i p i t a l and p a r i e t a l r e g i o n s . t h a t should h e l p i n determining  Experiments  the v a l i d i t y of t h i s  idea  are c o n t r o l l e d l e s i o n i n g of s p e c i f i c c o r t i c a l areas, l e s i o n s of d i f f e r i n g s i z e s ,  l e s i o n i n g of animals of v a r y i n g  developmental ages, and t e s t i n g f o r the f o r c e d d i v e response  52 i n the same animal at v a r y i n g lengths  of time a f t e r  decortication. MacArthur and Karpan attenuates  (1989) found t h a t  dive bradycardia  i n muskrats.  evidence was found i n t h i s study.  exercise  Contradictory  I n t a c t animals e x e r c i s e d  v i g o r o u s l y i n f o r c e d d i v e s yet had a lower heart  r a t e than  i n escape d i v e s when they r e s t e d underneath the screens. Furthermore, i n sham operated  and d e c o r t i c a t e animals,  escape and f o r c e d dive heart  r a t e s 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  c o n c l u s i o n drawn from t h i s i s t h a t underwater a c t i v i t y does not  i n f l u e n c e dive heart  r a t e s i n muskrats.  Although the response was v a r i a b l e , t r a p p i n g muskrats underwater r e s u l t e d i n a decrease i n heart  rate.  c o n t r a s t s with t r a p p i n g t u f t e d ducks where heart immediately dropped t o l e v e l s recorded  during  This r a t e always  involuntary  submersion  (Stephenson et al. 1986).  d i v e heart  r a t e i n d i c a t e s p o s i b l e c o r t i c a l i n f l u e n c e upon  heart  This a l t e r a t i o n i n  r a t e d u r i n g the d i v e . The  heart  r a t e of muskrat and beaver are h i g h e r  during  a c t i v e behaviour  (grooming and swimming) than d u r i n g l e s s  a c t i v e behaviour  ( r e s t i n g and s l e e p i n g )  1982b; Swain et a l . 1988). decorticate,  ( G i l b e r t and Gofton  T h i s was a l s o found i n i n t a c t ,  and sham operated  animals i n t h i s  However, an i n t e r e s t i n g q u e s t i o n  i s why i n sham  animals t h e i r r e s t i n g and a c t i v e heart lower than i n i n t a c t animals.  study. operated  r a t e s were so much  Apparently  the e f f e c t s of  53 surgery  r e s u l t e d i n a lowered r e s t i n g heart  The  predive  voluntary  heart  than t h a t of t h e i r a c t i v e heart seconds before  voluntary  r a t e of muskrats i s higher rate.  Approximately 30  d i v e s , heart  r a t e s o f muskrats  start to increase  from the a c t i v e heart  voluntary  heart  predive  MacArthur and Karpan  rate.  rate.  (1989).  r a t e t o the  T h i s t r e n d was a l s o seen by B u t l e r and Woakes (1979) found  i n t u f t e d and pochard ducks t h a t approximately 5 seconds before  the f i r s t  tachycardia had  dive o f a d i v i n g bout t h e r e  i s both a  and h y p e r v e n t i l a t i o n , and concluded that  the e f f e c t of l o a d i n g oxygen s t o r e s b e f o r e  a d i v i n g bout  ( B u t l e r and Woakes 1979).  The a c t i v e heart  the s t a r t o f  P o s s i b l y oxygen  l o a d i n g accompanies the a n t i c i p a t o r y p r e d i v e muskrats.  this  tachycardia i n  r a t e o f muskrats was s i m i l a r t o  t h a t o f escape and f o r c e d p r e d i v e  heart  rates.  B u t l e r and  Woakes (1979) found no a n t i c i p a t o r y "increase i n heart in  f o r c e d d i v e d ducks.  animals entered preparatory  rate  Perhaps i n these c o n d i t i o n s the  the water before  being  able t o engage i n a  tachycardia.  In c o n c l u s i o n ,  t h i s i s the f i r s t  study t o date t h a t has  i n v e s t i g a t e d the suprabulbar mechanisms i n v o l v e d i n the dive response o f spontaneously behaving animals. studies, e l e c t r i c a l stimulation of s p e c i f i c  In previous suprabulbar  b r a i n areas has r e s u l t e d i n only p a r t i a l m a n i f e s t a t i o n of cardiovascular  and r e s p i r a t o r y d i v i n g adjustments (cf.  B u t l e r and Jones 1982).  T h i s study p r o v i d e s  positive  evidence f o r c o r t i c a l involvement i n the d i v e response of  muskrats, and  i t e l i m i n a t e s the c o n t e n t i o n t h a t  bradycardia i s solely  fear-induced.  55 REFERENCES Anderson H . T . 1963 F a c t o r s determining the c i r c u l a t o r y adjustments to d i v i n g I . Water immersion. Acta P h y s i o l o g i c a S c a n d i n a v i c a 58:173-185 Anderson H . 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Sweet 1980 E f f e c t o f a t r o p i n e on the onset o f f e a r b r a d y c a r d i a i n E a s t e r n C o t t o n t a i l Rabbits, S v l v i l a g u s f l o r i d a n u s . Comparative B i o c h e m i s t r y and P h y s i o l o g y 66C:239-241  59 Smith E.N. and W. Tobey 1983 Heart r a t e response t o f o r c e d and v o l u n t a r y d i v i n g i n Swamp Rabbit, S y l v i l a g u s aquaticus. P h y s i o l o g i c a l Zoology 56:632-638 Smith E.N. and R.A. Woodruff 1980 Fear b r a d y c a r d i a i n f r e e - r a n g i n g woodchucks, Marmota monax. J o u r n a l of Mammalogy 61:750-753 Spyer K.M. 1982 C e n t r a l nervous i n t e g r a t i o n of c a r d i o v a s c u l a r c o n t r o l . J o u r n a l of Experimental B i o l o g y 100:109-128 Spyer K.M. 1984 C e n t r a l c o n t r o l of the c a r d i o v a s c u l a r system. In: Recent Advances i n P h y s i o l o g y (ed. P.F.Baker), C h u r c h i l l L i v i n g s t o n e , New York pl63-200 Stephenson R., P.J. 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L o u i s 1987 Medial p r e f r o n t a l c o r t i c a l l e s i o n s modulate b a r o r e f l e x s e n s i t i v i t y i n the r a t . B r a i n Research 426:243-249 West N.H. and B.N. Van V l i e t 1986 F a c t o r s i n f l u e n c i n g the onset and maintenance of b r a d y c a r d i a i n Mink. P h y s i o l o g i c a l Zoology 59:451-463 Woakes A . J . and P.J. B u t l e r 1983 Swimming and d i v i n g i n T u f t e d Ducks, Avthva f u l i g u l a , with p a r t i c u l a r r e f e r e n c e t o heart r a t e and gas exchange. J o u r n a l of E x p e r i m e n t a l B i o l o g y 107:311-329 Wolf S. 1978 P s y c h o l o g i c a l i n f l u e n c e s on the d i v e r e f l e x i n man. In: Neural Mechanisms i n C a r d i a c Arrhythmias (eds. P.J.Schwartz, A.M.Brown, A . M a l l i a n i , and A . Z a n c h e t t i ) , Raven Press, New York p237-250 Zapol W.M., G.C. L i g g i n s , R.C. Schneider, J . Q v i s t , M.T. Snider, R.K. Creasy, and P.W. Hochachka 1979 Regional b l o o d flow d u r i n g simulated d i v i n g i n the conscious Weddell S e a l . J o u r n a l of A p p l i e d P h y s i o l o g y 47:968-973 Z i l l e s K. and A. Wree 1985 Cortex: a r e a l and laminar s t r u c t u r e . In: The Rat Nervous System, v o l 1 (ed. G.Paxinos), Academic Press, Toronto p375-415  61 Appendix 1 Dive heart r a t e s from i n t a c t muskrats DIVE TIME (s) Predive 5 10 15 20 25 30 35 40 45 50 55 60 Postdive  Voluntary  Forced  Escape  MEAN  SEM  N  MEAN  SEM  N  MEAN  SEM  N  297 130 113 118 105 102 111 112 145  13 9 8 8 15 12 15 10 21  8 8 8 8 7 6 5 4 2  274 95 95 91 90 84 93 48 62 48 35 68 61 290  17 18 18 13 21 19 33 10 6 24 10  7 7 7 7 5 5 5 4 4 2 2 1 1 7  273 74 63 57 58 54 56 54 56 57 55 54 58 289  17 7 6 4 4 3 4 4 4 5 2 3 4 14  7 7 7 7 7 7 7 7 7 7 7 7 7 7  303-  13  -8  21  Grand mean heart r a t e v a l u e s and standard e r r o r of the mean from N a n i m a l s . Some muskrats performed s h o r t e r d u r a t i o n v o l u n t a r y and escape d i v e s r e s u l t i n g i n d e c r e a s i n g N numbers i n the longer d u r a t i o n u n r e s t r a i n e d d i v e s .  62 Appendix 2 Dive heart r a t e s from sham operated muskrats DIVE TIME (s) Predive  5  10 15  20 25 30 35 40 45 50 55 60  Postdive  Voluntary  Forced  Escape  MEAN  SEM  N  MEAN  SEM  N  MEAN  SEM  N  274 109 113 -  11 5 -  3 3 1 -  248 44 46 38 37 39 37 42 41 39 39 34 38 233  21 3 3 8 6 7 3 3 5 4 5 1 4 11  3 3 3 3 3 3 3 3 2 2 2 2 2 3  260 52 55 42 42 47 40 44 49 48 48 45 45 272  8 4 5 4 3 8 2 10 4 6 6 2  3 3 3 3 3 3 3 3 3 3 3 3 3 3  269-  --  ---- 4 3  -  8  11  Grand mean h e a r t r a t e v a l u e s and standard e r r o r o f t h e mean from N animals. A l l sham operated muskrats performed s h o r t d u r a t i o n v o l u n t a r y d i v e s , w h i l e many escape d i v e s l a s t e d over 2 minutes.  63 Appendix 3 Dive heart r a t e s from d e c o r t i c a t e DIVE TIME (s) Predive 5  10 15  20 25  30 35 40 45 50 55 60 Postdive  Voluntary  muskrats Forced  Escape  MEAN  SEM  N  MEAN  SEM  N  MEAN  SEM  N  295 106 101 109 117  3 8 6 8  7 7 6 2 1  246 86 84 80 74 81 125 52  7 9 8 6 5 13  7 7 7  263 80 75 79 78 83 71 73 78 77 82 86 82 271  12 10 12 12 15 18 11 10 11 11 10 15 11 10  6 6 6 6 6 6 6 6 6 6 6 6 6 6  285-  -3  -7  274  -9  5  3 4 1 1  -7  Grand mean heart r a t e v a l u e s and standard e r r o r of the mean from N a n i m a l s . Some muskrats performed s h o r t e r d u r a t i o n v o l u n t a r y and escape d i v e s r e s u l t i n g i n d e c r e a s i n g N numbers i n the longer d u r a t i o n u n r e s t r a i n e d d i v e s .  

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