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Spontaneous electrical activity of the spinal cord
S P O N T A N E O U S E L E C T R I C A L A C T I V I T Y OF T H E SPINAL CORD J. TEN CATE Physiological Laboratory of the University ot Amsierdam, The Nelherlands
Although the reaction potentmls of the recision on the boundary of the medulla spinal cord have been thoroughly investigated oblonga(a, definite electrical activity of the by a number of workers, including Gasser spinal cord could always be registered As and Graham (1933). Hughes, McCough and the reflex activity disappeared the spontaStewart (1937) and Bremer (1941), only neous electrical activity also faded out rapivery scanty information as to the spontaneous dly The curves (EChG) thus obtained electrical activity of the spinal cord ~s to showed slow waves of the type of Berger's be found m the literature. ,~-waves and also fast waves resembling flAfter the wellknown experiments of Adrian waves The voltage of the potential changes and Buytendyk ( 1931 ), in which spontaneous in the spinal cord was determined from the rhythmic potentml fluctuations were re- calibration values, which are qlven on the gistered from the isolated brain-stem of the curves m ~ V (fig 5C) goldfish, Gerard and Young (1937) studied The spontaneous electrical activity of the the spontaneous electrical activity of the isolated spinal cord of warm-blooded ammedulla oblongata and spinal cord These reals was studied (m cats) by G P M workers, however, merely demonstrated the Horsten m his thesis For th~s purpose two existence of such actiwty, but did not study series of investigations were carried out In it further Bremer (19ql) also gives a de- the first the caudal part of the spinal cord scription of the spontaneous electrical activity was isolated bv a transverse incision at the of the spinal cord as being characterized by level of the 10th thoracic segment. About irregular frequencies with a very low voltage 10 days after this operation the EChG of During the last five years we have made a the caudal part of the cord was registered specml study of the spontaneous electrical under Pentothal or ether anaesthesia. It activity of the spinal cord and of the various transpired, however, that the EChG pattern factors by which this actlwty is influenced was affected by the anaesthetics A second The first investigation (with W G W a l - series of experiments was then started, m ter and J ] Koopman) was concerned with which the animals were first decerebrated the spontaneous electrical achv~ty of the under ether anaesthesia, afte~ which the spinal cord m frogs The electrochordogram spinal cord was isolated from the brain by ( E C h G ) was led off either directly from the transverse section at the level of the first spinal cord or with the electrodes placed on cervical segment The registration of the the vertebrae after removal of the dorsal spontaneous electrical activity of the isolated muscles It was found that the heart action portion of the cord was done after a certain potentials interfered with registration of the lapse of time, when the effect of the ether spontaneous electrical achwty of the spinal had worn off cord, the heart was therefore extirpated and As can be seen in figures 1 and 5C, the it was found that the reflex and spontaneous spontaneous electrical activity of the spinal electrical activ~tles of the spinal cord survived cord was very marked and showed a certain this operatmn for about 20 minutes (these resemblance to that seen in frogs In addmon experiments were clone m the summer to slow waves, corresponding to the a- and months). 8-waves of the electroencephalogram there In these experiments, m which the cord were also numerous fast waves which corwas separated from the brain by a transverse responded to the fl-waves of the EEG. The l 445 ]
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a m p h t u d e of all w a v e s w a s a l w a y s g r e a t e r t h a n t h a t f o u n d w i t h frogs, the s e n s m w t y of the r e c o r d m 9 i n s t r u m e n t b e i n g t h e s a m e m b o t h cases
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also r e m a i n e d c o m p a r a t i v e l y h v e l y A 9 l a n c e at g r a p h 3 A w d l suffice t o s h o w t h a t the s p o n t a n e o u s electmcal a c t l w t y o f t h e i s o l a t e d s p i n a l s e g m e n t d i f f e r s from t h a t o f the c o m pletely intact spinal cord Pamcularly noticea b l e is t h e p r e d o m i n a n c e o f s l o w e r f r e q u e n cms, a l t h o u g h f a s t e r f r e q u e n c m s o f t h e at y p e a n d also fast B - w a v e s a r e stdl p r e s e n t .
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A
Fig 1 Spontaneous electrical activity of the spinal cord which has been isolated, in unanaesthetized, previously decerebrated cat With Walter and Koopman a study of the s p o n t a n e o u s electmcal a c t l v l t y o f a s i n g l e i s o l a t e d s p i n a l s e g m e n t --- t h e s e c o n d , w h i c h i n n e r v a t e s t h e f o r e - h m b s - - m f r o g s (fig. 2A), w a s c a m e d o u t A s l o n g a s t h e r e f l e x a c t l w t y o f t h e i s o l a t e d s e g m e n t w a s still present, the spontaneous electrical actlwty
B
!/.,v 2&L.~ .2~ . . . . r. _
C
2~
D
Fig 2 A Spontaneous electrmal acuv~ty of one isolated segment of a frog Only the 2nd segment of the spinal cord left intact, the rest removed Brain also removed Reflexes 0ood B Same preparation as m A Both spinal nerves sup"~vmo the foreleos severed Immedtatly after re0istertn 0 curve 2
Fig 3 A Spontaneous electmcal acttvtty of the spmal cord of a frog Spinal cord and brain intact Except for the nerves supplying the forelegs, all nerve roots severed B Same preparation as m A Nerves supplying forelegs severed, bram mtact C Same preparation as m A Brain removed D Cahbration-hne with both gelatin electrodes (20 per cent gelatm m Rm0er's solution) placed together
ELECTRICAL ACTIVITY OF SPINAL CORD T h e low frequencies are probably to be reoarded as signs of damage to the cord segment in the process of isolation. Notwithstanding this, the experiments show that even a completely isolated segment of the spinal cord is still capable of maintaining a fair degree of spontaneous electrical activity While an isolated spinal segment that is connected to the forelimbs via the spinal roots still shows a quite considerable electrical activity, this activity dwindles to a great extent if the connection with the periphery is interrupted by section of the spinal roots (fig 2B). T h e same pattern was seen in the E C h G s taken from a spinal cord after section of all the spinal nerves. In the experiments with W a l t e r and Koopman, we first isolated the cord from the brain. After the E C h G of this spinal cord had been recorded, we severed all the spinal nerves close to the vertebral column on both sides In every case the spinal cord completely isolated in this manner showed only a very slight spontaneous electrical activity. T h a t this decrease of electrical activity was not due to changes in the circulation of blood in the spinal cord is proved by the experiments in which the heart was removed on account of the interference of ~ts action potentials with the E C h G registration. Shock phenomena in the frog are minimal and of very short duration, so that the decrease cannot be ascribed to the effects of shock either Besides this, the results were the same whether we took the E C h G immediately after section of the spinal roots or 15 min. later. It is worth while to draw attention here once more to the following fact we were able to ascertain that the spontaneous electrical act,vity of the isolated spinal cord is still comparatively hvely so long as the cord stdl remains connected, through a few spinal nerves, with the fore- and hmd-hmbs W h e n these connections are severed, however, the activity becomes minimal Both the lsoJated spinal segment and the completely isolated cord show a defimte spontaneous acttv,ty as long as they remain
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m connection, through the spinal nerves, with the periphery J , e , with the muscles and the skin. A totally isolated spinal cord that has all its spinal nerves severed and that is isolated from the brain, shows only a feeble electrical activity. This electrical actwtty, which is produced by the completely spontaneous activity of the nerve cells, must be regarded as the t r u e spontaneous electrical activity of the spinal cord. It is observed only when the spinal cord Is totally isolated from the brain and from the periphery (fig 3A, B and C) In each experiment the zero-hne was drawn first, thc two electrodes being placed one against the other (fig. 3D) Similar curves were registered after disappearance of electrical activity in the cord of the frog 30 or more minutes after the heart had been removed T he grid-electrode was placed on the cord, the ground-electrode on the dorsal skin on the an,mal's back at a dlstance of 2-4 cm from the former T he stimuli which are transmitted from the periphery via the afferent nerves to the cord maintain the spontaneous electrical activity of thin organ at a much higher level, which is shown chmfly by the much greater amphtude of the waves. These observations indicate the ex,stence of a continuous interaction between the spinal cord and the muscles and skin, even when all the organs ment,oned are apparently in a state of complete rest T h e spinal cord is continually receiving propmo- and exteroceptive stimuli from the peripheral organs and, in its turn, ,s continually sending impulses to the periphery This had already been pointed out by Brondgeest (1860) and later by Sherrmgton and Llddell (1925), who ascribed reflex muscle tone to such an interact,on between spinal cord and muscles. Acccordmg to Ozono de AlmeMa and Pieron (1924) and Bremer and Moldaver (193q). the afferent stlmuh transmitted from the skin to the spinal cord also play an appreciable part in thin respect Horsten described a s,mdar action of the periphery on the electrical activity of the
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spinal c o r d an cats In h~s e x p e r i m e n t s , the ~pmal c o r d of p r e v m u s l y d e c e r e b r a t e d cats w a s s e v e r e d t r a n s v e r s e l y at the level of the 12th t h o l a c l c s e g m e n t T h e e l e c t r i c a l act~wty of the i s o l a t e d c a u d a l p a r t of the s p i n a l c o r d v,a~ then re q~stered, a f t e r w h i c h b o t h sciatic n e r v e s were cut T h e a m p h t u d e of the s l o w a n d fa~t w a v e s ot the E C h G then d e c r e a s e d c o n s M e r a b l y Stdl s t r o n g e r e w d e n c e w a s p r o vMed by a n o t h e r of H o r s t e n ' s e x p e n m e n t ~ T h e l u m b o - s a c r a l p a r t of the s p i n a l c o r d of cats ,~a~ ~solated from the hLqher p a r t s of the centrM n e r v o u s qystem a b o u t 10 d a w a f t e r th~s o p e r a h o n the s p o n t a n e o u s electrical a c t i v i t y of the ~solated cord ~ a s r e q ~ t e r e d a f t e r c o m p l e t e paralys~s of the muscle~ b~ mean~ of D - t u b o c u r a r m e chloride The muscle tone of the h m d - h m b q w a s a b o h s h e d a n d the s p o n t a n e o u s electrical a c t i v i t y of thc ~ o l a t e d s p i n a l c o r d wa~ ver~ sh,qht W h e n h o w e v e r one of the h m d - h m b s h a d been sub)ected for ~ome t~me to p a s s w e flexion which )r'cren~ed the n u m b e r ot propr,ocept~ve H~-
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pulses, the s p o n t a n e o u s e l e c t r i c a l a c t w a t y of the s a m e p o r h o n of s p i n a l c o r d i n c r e a s e d 9 r e a t l y A c o n s a d e r a b l e i n c r e a s e m the n u m b e r of fast w a v e s w a s o b s e r v e d on e v e r y occasaon ( h 9 4 A a n d B) T o 9 a m a b e t t e r u n d e r s t a n d m 9 o f the anfluence of e x t e r o - a n d p r o p n o c e p t w e stlmuh on the s p o n t a n e o u s e l e c t r i c a l a c t w l t y of the spinal c o r d e x p e r i m e n t s w e r e c a r r i e d out with H o r s t e n a n d K o o p m a n , on froqs an w h i c h the e f f e c t of s t r e t c h m 9 of m u s c l e s a n d skin of the h i n d h m b s on the E C h G w a s i n v e s t i g a t e d F o r th~s p u r p o s e x~e h r s t t o o k the E C h G ot a fro,q t y m q u n d i s t u r b e d on a cork slab T h e n we took an E C h G w i t h the fro9 in a h a n q m 9 po,,~tion a n d with a 20 cj w e i g h t
A
B
;o C
Fig 4 A Soontaneous electrical actwlty of the caudal part of the spinal cord of a cat x~h~ch has been severed at the 10th dorsal segment, re91stered 10 days after the operation under ether anaesthesm and complete muscular paral 3 sis by mlectlon of D-tubocurarme chloride B The same cat after passive movements had been executed for some time v. lth one hind leg
F10 5 A Spontaneous electrical activity of the spinal cord o) a frog lym,j horizontally on a cork slab B Same frog as in A in hanging position with a 20 0 weight suspended from each hind leg C Spontaneous electrical acn~lty of the isolated spinal cord of a fro 0 D The same spinal frog as ~n C but after the frog had been skmned
ELECTRICAL ACTIVITY O Y SPINAL CORD suspended from each of its hind-legs W e found that stretchm 9 of the h,.nd-hmbs resuited m an apprecmble increase of the spontaneous electmcal activity of the cord, with a preferentml increase of the fast waves, more rarely a shght increase of the slow waves was also observed (rio 5 A and B) T o ascertain what part of the shmulatmn of spontaneous electrical actlvltv of the spinal cord ~s due to the exterocept~ve and what part to the propmocepuve shmull, we also carried out the following expemments F~rst we investigated the effect of ehmmatmn of exterocephve stlmuh The skin of the hind hmbs and the hinder part of the trunk of a frog was peeled off and the E C h G of the caudal part of the cord (severed transversely at the level of the 5th or 6th segment) was registered before and after this operation In all expemments we found the spontaneous electmcal achvlty of the molated caudal part of the cord to be apprecmbly decreased after the skin had been peeled off Partrcularly stroking was the dlmmutlon of amphtude of both fast and slow waves (fig 5C and D) W e then ehmlnated proprloceptlve shmuh (in frogs) by the mlectmn of curare, leading to total paralysts of all muscles In all expemments we found the spontaneous electmcal actwlty of the isolated caudal part of the spinal cord to be conmderably decreased when thin complete muscular paralyms was estabhshed These expemments on the ehmmatmn of exterocephve and also of propmocept~ve snmuh point unmistakably to the conclusmn that these st~muh, which are transmitted from the pemphery to the spinal cord, have an ~mportant influence on the spontaneous electmcal achwty of the organ m questmn The afferent conduction of extero- and propmoceptlve shmuh is not the only thing which maintains the true spontaneous electmcal achvlty of the spinal cord at a high level Th e hl,qher centres of the brain also play their part m this respect, as shown by the expemments of Koopman, W a l t e r and myself on frogs W e were able to observe
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that the spontaneous electmcal activity o[ the spinal cord, whxch could receive no shmuh from the pemphery because all the spinal nerves were severed, diminished appreciably when the cord was separated ham brain by a transverse mc~smn at the boundary of the medulla oblongata Horsten's expemments with decerebrated cats also point to an indubitable influence of the brain on the spontaneous electmcal activity of the spinal cord After decerebratmn, the cats showed a particularly hvely electmcal acuvlty of the spinal cord V e r y fast waves of relatwely large amphtude were registered Thin shll remained unchanged after mlectlon of D-tubocurarme chlomde to ehmmate the actton potentials of muscles Thts pronounced electmcal achvlty of the spinal cord indicates a state of increased exc~tatton of the motor antemor-horn cells, which leads to increase of muscular tone after the braking actmn of the nucleus ruber has been ehmmated and the nucleus of Delters and the substantla ret~culams have acqmred an excessive influence over the motor antemor-horn cells (fig 6A) W h e n the effects of the above-mentmned tone-producm 9 centres on the spinal cord are ehmlnated by a transverse sechon through the cervical part of the cord, the E C h G changes at the same t~me as the muscular mfldlty disappears T he fast waves decrease m number and the slow waves become more numerous (compare hgure 1). T h e amphtude of the waves also becomes smaller Horsten also studied the effect of the motor cortex of the cerebral hemispheres on the spontaneous electmcal achvlty of the spinal cord His observations agreed with those of W e e d (1914), Logan (1925), Bard and W o o l s e y (1933) and ten Care (1940) m that he also noted an increase of tone of the flexors after b~lateral exhrpatlon of the motor cortex, this pomtm 9 to an augmented state of stlmulatmn of the motor anteriorhorn cells. In correspondence to these observatrons, an increase of fast waves was seen m the E C h G of cats after bdateral extlrpat~on of the motor cortex Thin points to shght de-mhlb~tmn of the motor cells
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with increase of thmr excltabdlty (fig and C)
6B
A
C
Since anaesthetics were used m most of the expemments on cats, H o r s t e n also stud~ed the effects of ether and Pentothal on the electmcal act~wty of the spinal cord T h e s e experiments showed that m intact cats under ether, low frequencies are chiefly m evidence m the E C h G In cats a n a e s t h e u s e d with the barbltumc acid derivative Pentothal, on the other hand, a defimte increase of fast w a v e s was seen In this w a y H o r s t e n was able to show that the E C h G pattern of the normal cat is dependent to a high degree on the anaesthetic used In other expemments H o r s t e n ascertained that th~s &fference between the effect of ether and that of Pentothal on the spontaneous electmcal activity of the spinal cord is manifested only m a m m a l s m whtch the spinal cord is stdl m connectmn wtth the brain. W h e n the two anaesthetics m questmn were administered to cats whose lumbosacral medulla had been isolated a few d a y s prewously, their effects on the spontaneous electmcal act~wty of the isolated portmn of the spinal cord were found to be ldentlca! T h e E C h G pattern was the same whether ether or Pentothal was administered It thus appears that the brain Is responstble for the difference between the effects of the two anaesthetics on the electrical actlwty of the spinal cord (fig. 6 B and D ) SUMMARY
D
F~g 6 A Electrical actlvfly of the spinal cord of a decerebrated cat (paralysed with D-tubocuramne chloride) shortly after the decerebration B EChG of a cat under ether anaesthesia (compare fig 1 ) C EChG of the same cat as in B but after extlrpatmn of the motor cortex D EChG of a normal cat under Pentothal anaesthesia
1 T h e isolated spinal cord of frogs and cats shows spontaneous electmcal activity which can be re91stered without difficulty. In the electrochordogram ~t ~s possible to d l s t m g m s h slow and fast waves 2 A single isolated segment of the frog's spinal cord also shows spontaneous electmcal actwlty 3 T h e spontaneous electrical actlwty is maintained at a relatively high level by stlmuh which are transmitted from the skin and muscles to the spinal cord After sectlon of all the spinal nerves, p e e h n g - o f f of the skin and ehmmatlon of propmoceptlve stlmuh by mlectlon of curare, the spontaneous electrical activity dlmlmshes considerably
ELECTRICAL ACTIVITY OF SPINAL CORD 4. T h e s p o n t a n e o u s e l e c t r i c a l a c t i v i t y o f t h e s p i n a l c o r d is a l s o i n f l u e n c e d b y t h e brain Both the nuclm of the brain stem and the motor cortex of the cerebral hemispheres p l a y a n ~ m p o r t a n t p a r t m th~s r e s p e c t REFERENCES ADRIAN, E D and BHYTENDI.IK, F J J Potential changes m isolated brain stem of goldfish 1. Phystol, 1931, 71 121-135 BREMEn, F L'actlvlte electr~que ¢ spontanee • de la moelle epmlere Arch mternat Phystot, 1941, 51 51-84 BnEMER, F et MOLDAVEn, J Reflectlwte cutanee et tonus postural chez les Anoures C R Soc Btol, Paris, 1934, 115 418-422 BRONDGEEST, P Q Onderzoekmgen over den tonus der wfllekeur~ge sp~e ren Dissertation. LImvers~ty of Utrecht, 1860 GASSER, H S and GRAHAM, H T Potentials produced m spinal cord by stlmulatmn of dorsal roots Amer ] PhysmI, 1933, 103 303-320 GERARD, R W and YOUNG, J Z Electrical activity of central nervous system of frog Proc Roy. Soc, 1937, B 122 343-352 HUGHES, J, MCCOUGH, G P and STEWART, W B. Cord potentmls m the spinal cat Amer ] Phgstol, 1937, 118 411-421
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HORSTEN, G P M L acuvite electnque spontanee de la moelle epmiere des mammlferes Arch mternat Phys~ol, 1947 55 304-306 HORSTEN, G P M Een onderzoek naar de spontane electrlsche actlvltelt van her zoogdierruggemerg Dissertation University of Amsterdam, 1948 HORSTEN, G P M L'achvlte electnque de la moelle epmlere sous narcose ~ 1'ether et au Pentothal Arch let Pharmacodgn Ther, 1948, 77 212218 HORSTEN G P M L'mfluence des parties superleures de l encephale sur l'actlvlte electrique spontanee de la moelle epmiere Arch mternat Phystol, 1948, 56 117-129 OZORIO DE ALMEIDA, M et PmRON, H Achon de la peau sur l etat general du systeme nerveux chez la grenoudle C R Soc Btol, Paris, 199.4, 90 422-425 TEN CATE J Lacttvtte elecmque spontanee des differentes parties du systeme nerveux central J Phgstol, 1949 41 161-172 TEN CATE, J, WALTER, W G and KOOPMAN L J Electrical activity m frog spinal cord ] Neurophy~tol, 1947, 10 223-233 TEN CATE, J, HORSTEN, G P M e t KOOPMAN, L ] Influence des organes pGrlpherlques sur I acttvlte elecmque de la moelle dpmlere Arch tnternat Phgstol, 1947, 55 51-58
Reference TEN CATE, J Spontaneous electrical activity of the spinal cord 445-451
EEG Chn Neurophysmt, 19fi0, 2
Although the reaction potentmls of the recision on the boundary of the medulla spinal cord have been thoroughly investigated oblonga(a, definite electrical activity of the by a number of workers, including Gasser spinal cord could always be registered As and Graham (1933). Hughes, McCough and the reflex activity disappeared the spontaStewart (1937) and Bremer (1941), only neous electrical activity also faded out rapivery scanty information as to the spontaneous dly The curves (EChG) thus obtained electrical activity of the spinal cord ~s to showed slow waves of the type of Berger's be found m the literature. ,~-waves and also fast waves resembling flAfter the wellknown experiments of Adrian waves The voltage of the potential changes and Buytendyk ( 1931 ), in which spontaneous in the spinal cord was determined from the rhythmic potentml fluctuations were re- calibration values, which are qlven on the gistered from the isolated brain-stem of the curves m ~ V (fig 5C) goldfish, Gerard and Young (1937) studied The spontaneous electrical activity of the the spontaneous electrical activity of the isolated spinal cord of warm-blooded ammedulla oblongata and spinal cord These reals was studied (m cats) by G P M workers, however, merely demonstrated the Horsten m his thesis For th~s purpose two existence of such actiwty, but did not study series of investigations were carried out In it further Bremer (19ql) also gives a de- the first the caudal part of the spinal cord scription of the spontaneous electrical activity was isolated bv a transverse incision at the of the spinal cord as being characterized by level of the 10th thoracic segment. About irregular frequencies with a very low voltage 10 days after this operation the EChG of During the last five years we have made a the caudal part of the cord was registered specml study of the spontaneous electrical under Pentothal or ether anaesthesia. It activity of the spinal cord and of the various transpired, however, that the EChG pattern factors by which this actlwty is influenced was affected by the anaesthetics A second The first investigation (with W G W a l - series of experiments was then started, m ter and J ] Koopman) was concerned with which the animals were first decerebrated the spontaneous electrical achv~ty of the under ether anaesthesia, afte~ which the spinal cord m frogs The electrochordogram spinal cord was isolated from the brain by ( E C h G ) was led off either directly from the transverse section at the level of the first spinal cord or with the electrodes placed on cervical segment The registration of the the vertebrae after removal of the dorsal spontaneous electrical activity of the isolated muscles It was found that the heart action portion of the cord was done after a certain potentials interfered with registration of the lapse of time, when the effect of the ether spontaneous electrical achwty of the spinal had worn off cord, the heart was therefore extirpated and As can be seen in figures 1 and 5C, the it was found that the reflex and spontaneous spontaneous electrical activity of the spinal electrical activ~tles of the spinal cord survived cord was very marked and showed a certain this operatmn for about 20 minutes (these resemblance to that seen in frogs In addmon experiments were clone m the summer to slow waves, corresponding to the a- and months). 8-waves of the electroencephalogram there In these experiments, m which the cord were also numerous fast waves which corwas separated from the brain by a transverse responded to the fl-waves of the EEG. The l 445 ]
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a m p h t u d e of all w a v e s w a s a l w a y s g r e a t e r t h a n t h a t f o u n d w i t h frogs, the s e n s m w t y of the r e c o r d m 9 i n s t r u m e n t b e i n g t h e s a m e m b o t h cases
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also r e m a i n e d c o m p a r a t i v e l y h v e l y A 9 l a n c e at g r a p h 3 A w d l suffice t o s h o w t h a t the s p o n t a n e o u s electmcal a c t l w t y o f t h e i s o l a t e d s p i n a l s e g m e n t d i f f e r s from t h a t o f the c o m pletely intact spinal cord Pamcularly noticea b l e is t h e p r e d o m i n a n c e o f s l o w e r f r e q u e n cms, a l t h o u g h f a s t e r f r e q u e n c m s o f t h e at y p e a n d also fast B - w a v e s a r e stdl p r e s e n t .
II
A
Fig 1 Spontaneous electrical activity of the spinal cord which has been isolated, in unanaesthetized, previously decerebrated cat With Walter and Koopman a study of the s p o n t a n e o u s electmcal a c t l v l t y o f a s i n g l e i s o l a t e d s p i n a l s e g m e n t --- t h e s e c o n d , w h i c h i n n e r v a t e s t h e f o r e - h m b s - - m f r o g s (fig. 2A), w a s c a m e d o u t A s l o n g a s t h e r e f l e x a c t l w t y o f t h e i s o l a t e d s e g m e n t w a s still present, the spontaneous electrical actlwty
B
!/.,v 2&L.~ .2~ . . . . r. _
C
2~
D
Fig 2 A Spontaneous electrmal acuv~ty of one isolated segment of a frog Only the 2nd segment of the spinal cord left intact, the rest removed Brain also removed Reflexes 0ood B Same preparation as m A Both spinal nerves sup"~vmo the foreleos severed Immedtatly after re0istertn 0 curve 2
Fig 3 A Spontaneous electmcal acttvtty of the spmal cord of a frog Spinal cord and brain intact Except for the nerves supplying the forelegs, all nerve roots severed B Same preparation as m A Nerves supplying forelegs severed, bram mtact C Same preparation as m A Brain removed D Cahbration-hne with both gelatin electrodes (20 per cent gelatm m Rm0er's solution) placed together
ELECTRICAL ACTIVITY OF SPINAL CORD T h e low frequencies are probably to be reoarded as signs of damage to the cord segment in the process of isolation. Notwithstanding this, the experiments show that even a completely isolated segment of the spinal cord is still capable of maintaining a fair degree of spontaneous electrical activity While an isolated spinal segment that is connected to the forelimbs via the spinal roots still shows a quite considerable electrical activity, this activity dwindles to a great extent if the connection with the periphery is interrupted by section of the spinal roots (fig 2B). T h e same pattern was seen in the E C h G s taken from a spinal cord after section of all the spinal nerves. In the experiments with W a l t e r and Koopman, we first isolated the cord from the brain. After the E C h G of this spinal cord had been recorded, we severed all the spinal nerves close to the vertebral column on both sides In every case the spinal cord completely isolated in this manner showed only a very slight spontaneous electrical activity. T h a t this decrease of electrical activity was not due to changes in the circulation of blood in the spinal cord is proved by the experiments in which the heart was removed on account of the interference of ~ts action potentials with the E C h G registration. Shock phenomena in the frog are minimal and of very short duration, so that the decrease cannot be ascribed to the effects of shock either Besides this, the results were the same whether we took the E C h G immediately after section of the spinal roots or 15 min. later. It is worth while to draw attention here once more to the following fact we were able to ascertain that the spontaneous electrical act,vity of the isolated spinal cord is still comparatively hvely so long as the cord stdl remains connected, through a few spinal nerves, with the fore- and hmd-hmbs W h e n these connections are severed, however, the activity becomes minimal Both the lsoJated spinal segment and the completely isolated cord show a defimte spontaneous acttv,ty as long as they remain
447
m connection, through the spinal nerves, with the periphery J , e , with the muscles and the skin. A totally isolated spinal cord that has all its spinal nerves severed and that is isolated from the brain, shows only a feeble electrical activity. This electrical actwtty, which is produced by the completely spontaneous activity of the nerve cells, must be regarded as the t r u e spontaneous electrical activity of the spinal cord. It is observed only when the spinal cord Is totally isolated from the brain and from the periphery (fig 3A, B and C) In each experiment the zero-hne was drawn first, thc two electrodes being placed one against the other (fig. 3D) Similar curves were registered after disappearance of electrical activity in the cord of the frog 30 or more minutes after the heart had been removed T he grid-electrode was placed on the cord, the ground-electrode on the dorsal skin on the an,mal's back at a dlstance of 2-4 cm from the former T he stimuli which are transmitted from the periphery via the afferent nerves to the cord maintain the spontaneous electrical activity of thin organ at a much higher level, which is shown chmfly by the much greater amphtude of the waves. These observations indicate the ex,stence of a continuous interaction between the spinal cord and the muscles and skin, even when all the organs ment,oned are apparently in a state of complete rest T h e spinal cord is continually receiving propmo- and exteroceptive stimuli from the peripheral organs and, in its turn, ,s continually sending impulses to the periphery This had already been pointed out by Brondgeest (1860) and later by Sherrmgton and Llddell (1925), who ascribed reflex muscle tone to such an interact,on between spinal cord and muscles. Acccordmg to Ozono de AlmeMa and Pieron (1924) and Bremer and Moldaver (193q). the afferent stlmuh transmitted from the skin to the spinal cord also play an appreciable part in thin respect Horsten described a s,mdar action of the periphery on the electrical activity of the
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spinal c o r d an cats In h~s e x p e r i m e n t s , the ~pmal c o r d of p r e v m u s l y d e c e r e b r a t e d cats w a s s e v e r e d t r a n s v e r s e l y at the level of the 12th t h o l a c l c s e g m e n t T h e e l e c t r i c a l act~wty of the i s o l a t e d c a u d a l p a r t of the s p i n a l c o r d v,a~ then re q~stered, a f t e r w h i c h b o t h sciatic n e r v e s were cut T h e a m p h t u d e of the s l o w a n d fa~t w a v e s ot the E C h G then d e c r e a s e d c o n s M e r a b l y Stdl s t r o n g e r e w d e n c e w a s p r o vMed by a n o t h e r of H o r s t e n ' s e x p e n m e n t ~ T h e l u m b o - s a c r a l p a r t of the s p i n a l c o r d of cats ,~a~ ~solated from the hLqher p a r t s of the centrM n e r v o u s qystem a b o u t 10 d a w a f t e r th~s o p e r a h o n the s p o n t a n e o u s electrical a c t i v i t y of the ~solated cord ~ a s r e q ~ t e r e d a f t e r c o m p l e t e paralys~s of the muscle~ b~ mean~ of D - t u b o c u r a r m e chloride The muscle tone of the h m d - h m b q w a s a b o h s h e d a n d the s p o n t a n e o u s electrical a c t i v i t y of thc ~ o l a t e d s p i n a l c o r d wa~ ver~ sh,qht W h e n h o w e v e r one of the h m d - h m b s h a d been sub)ected for ~ome t~me to p a s s w e flexion which )r'cren~ed the n u m b e r ot propr,ocept~ve H~-
CATE
pulses, the s p o n t a n e o u s e l e c t r i c a l a c t w a t y of the s a m e p o r h o n of s p i n a l c o r d i n c r e a s e d 9 r e a t l y A c o n s a d e r a b l e i n c r e a s e m the n u m b e r of fast w a v e s w a s o b s e r v e d on e v e r y occasaon ( h 9 4 A a n d B) T o 9 a m a b e t t e r u n d e r s t a n d m 9 o f the anfluence of e x t e r o - a n d p r o p n o c e p t w e stlmuh on the s p o n t a n e o u s e l e c t r i c a l a c t w l t y of the spinal c o r d e x p e r i m e n t s w e r e c a r r i e d out with H o r s t e n a n d K o o p m a n , on froqs an w h i c h the e f f e c t of s t r e t c h m 9 of m u s c l e s a n d skin of the h i n d h m b s on the E C h G w a s i n v e s t i g a t e d F o r th~s p u r p o s e x~e h r s t t o o k the E C h G ot a fro,q t y m q u n d i s t u r b e d on a cork slab T h e n we took an E C h G w i t h the fro9 in a h a n q m 9 po,,~tion a n d with a 20 cj w e i g h t
A
B
;o C
Fig 4 A Soontaneous electrical actwlty of the caudal part of the spinal cord of a cat x~h~ch has been severed at the 10th dorsal segment, re91stered 10 days after the operation under ether anaesthesm and complete muscular paral 3 sis by mlectlon of D-tubocurarme chloride B The same cat after passive movements had been executed for some time v. lth one hind leg
F10 5 A Spontaneous electrical activity of the spinal cord o) a frog lym,j horizontally on a cork slab B Same frog as in A in hanging position with a 20 0 weight suspended from each hind leg C Spontaneous electrical acn~lty of the isolated spinal cord of a fro 0 D The same spinal frog as ~n C but after the frog had been skmned
ELECTRICAL ACTIVITY O Y SPINAL CORD suspended from each of its hind-legs W e found that stretchm 9 of the h,.nd-hmbs resuited m an apprecmble increase of the spontaneous electmcal activity of the cord, with a preferentml increase of the fast waves, more rarely a shght increase of the slow waves was also observed (rio 5 A and B) T o ascertain what part of the shmulatmn of spontaneous electrical actlvltv of the spinal cord ~s due to the exterocept~ve and what part to the propmocepuve shmull, we also carried out the following expemments F~rst we investigated the effect of ehmmatmn of exterocephve stlmuh The skin of the hind hmbs and the hinder part of the trunk of a frog was peeled off and the E C h G of the caudal part of the cord (severed transversely at the level of the 5th or 6th segment) was registered before and after this operation In all expemments we found the spontaneous electmcal achvlty of the molated caudal part of the cord to be apprecmbly decreased after the skin had been peeled off Partrcularly stroking was the dlmmutlon of amphtude of both fast and slow waves (fig 5C and D) W e then ehmlnated proprloceptlve shmuh (in frogs) by the mlectmn of curare, leading to total paralysts of all muscles In all expemments we found the spontaneous electmcal actwlty of the isolated caudal part of the spinal cord to be conmderably decreased when thin complete muscular paralyms was estabhshed These expemments on the ehmmatmn of exterocephve and also of propmocept~ve snmuh point unmistakably to the conclusmn that these st~muh, which are transmitted from the pemphery to the spinal cord, have an ~mportant influence on the spontaneous electmcal achwty of the organ m questmn The afferent conduction of extero- and propmoceptlve shmuh is not the only thing which maintains the true spontaneous electmcal achvlty of the spinal cord at a high level Th e hl,qher centres of the brain also play their part m this respect, as shown by the expemments of Koopman, W a l t e r and myself on frogs W e were able to observe
449
that the spontaneous electmcal activity o[ the spinal cord, whxch could receive no shmuh from the pemphery because all the spinal nerves were severed, diminished appreciably when the cord was separated ham brain by a transverse mc~smn at the boundary of the medulla oblongata Horsten's expemments with decerebrated cats also point to an indubitable influence of the brain on the spontaneous electmcal activity of the spinal cord After decerebratmn, the cats showed a particularly hvely electmcal acuvlty of the spinal cord V e r y fast waves of relatwely large amphtude were registered Thin shll remained unchanged after mlectlon of D-tubocurarme chlomde to ehmmate the actton potentials of muscles Thts pronounced electmcal achvlty of the spinal cord indicates a state of increased exc~tatton of the motor antemor-horn cells, which leads to increase of muscular tone after the braking actmn of the nucleus ruber has been ehmmated and the nucleus of Delters and the substantla ret~culams have acqmred an excessive influence over the motor antemor-horn cells (fig 6A) W h e n the effects of the above-mentmned tone-producm 9 centres on the spinal cord are ehmlnated by a transverse sechon through the cervical part of the cord, the E C h G changes at the same t~me as the muscular mfldlty disappears T he fast waves decrease m number and the slow waves become more numerous (compare hgure 1). T h e amphtude of the waves also becomes smaller Horsten also studied the effect of the motor cortex of the cerebral hemispheres on the spontaneous electmcal achvlty of the spinal cord His observations agreed with those of W e e d (1914), Logan (1925), Bard and W o o l s e y (1933) and ten Care (1940) m that he also noted an increase of tone of the flexors after b~lateral exhrpatlon of the motor cortex, this pomtm 9 to an augmented state of stlmulatmn of the motor anteriorhorn cells. In correspondence to these observatrons, an increase of fast waves was seen m the E C h G of cats after bdateral extlrpat~on of the motor cortex Thin points to shght de-mhlb~tmn of the motor cells
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with increase of thmr excltabdlty (fig and C)
6B
A
C
Since anaesthetics were used m most of the expemments on cats, H o r s t e n also stud~ed the effects of ether and Pentothal on the electmcal act~wty of the spinal cord T h e s e experiments showed that m intact cats under ether, low frequencies are chiefly m evidence m the E C h G In cats a n a e s t h e u s e d with the barbltumc acid derivative Pentothal, on the other hand, a defimte increase of fast w a v e s was seen In this w a y H o r s t e n was able to show that the E C h G pattern of the normal cat is dependent to a high degree on the anaesthetic used In other expemments H o r s t e n ascertained that th~s &fference between the effect of ether and that of Pentothal on the spontaneous electmcal activity of the spinal cord is manifested only m a m m a l s m whtch the spinal cord is stdl m connectmn wtth the brain. W h e n the two anaesthetics m questmn were administered to cats whose lumbosacral medulla had been isolated a few d a y s prewously, their effects on the spontaneous electmcal act~wty of the isolated portmn of the spinal cord were found to be ldentlca! T h e E C h G pattern was the same whether ether or Pentothal was administered It thus appears that the brain Is responstble for the difference between the effects of the two anaesthetics on the electrical actlwty of the spinal cord (fig. 6 B and D ) SUMMARY
D
F~g 6 A Electrical actlvfly of the spinal cord of a decerebrated cat (paralysed with D-tubocuramne chloride) shortly after the decerebration B EChG of a cat under ether anaesthesia (compare fig 1 ) C EChG of the same cat as in B but after extlrpatmn of the motor cortex D EChG of a normal cat under Pentothal anaesthesia
1 T h e isolated spinal cord of frogs and cats shows spontaneous electmcal activity which can be re91stered without difficulty. In the electrochordogram ~t ~s possible to d l s t m g m s h slow and fast waves 2 A single isolated segment of the frog's spinal cord also shows spontaneous electmcal actwlty 3 T h e spontaneous electrical actlwty is maintained at a relatively high level by stlmuh which are transmitted from the skin and muscles to the spinal cord After sectlon of all the spinal nerves, p e e h n g - o f f of the skin and ehmmatlon of propmoceptlve stlmuh by mlectlon of curare, the spontaneous electrical activity dlmlmshes considerably
ELECTRICAL ACTIVITY OF SPINAL CORD 4. T h e s p o n t a n e o u s e l e c t r i c a l a c t i v i t y o f t h e s p i n a l c o r d is a l s o i n f l u e n c e d b y t h e brain Both the nuclm of the brain stem and the motor cortex of the cerebral hemispheres p l a y a n ~ m p o r t a n t p a r t m th~s r e s p e c t REFERENCES ADRIAN, E D and BHYTENDI.IK, F J J Potential changes m isolated brain stem of goldfish 1. Phystol, 1931, 71 121-135 BREMEn, F L'actlvlte electr~que ¢ spontanee • de la moelle epmlere Arch mternat Phystot, 1941, 51 51-84 BnEMER, F et MOLDAVEn, J Reflectlwte cutanee et tonus postural chez les Anoures C R Soc Btol, Paris, 1934, 115 418-422 BRONDGEEST, P Q Onderzoekmgen over den tonus der wfllekeur~ge sp~e ren Dissertation. LImvers~ty of Utrecht, 1860 GASSER, H S and GRAHAM, H T Potentials produced m spinal cord by stlmulatmn of dorsal roots Amer ] PhysmI, 1933, 103 303-320 GERARD, R W and YOUNG, J Z Electrical activity of central nervous system of frog Proc Roy. Soc, 1937, B 122 343-352 HUGHES, J, MCCOUGH, G P and STEWART, W B. Cord potentmls m the spinal cat Amer ] Phgstol, 1937, 118 411-421
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HORSTEN, G P M L acuvite electnque spontanee de la moelle epmiere des mammlferes Arch mternat Phys~ol, 1947 55 304-306 HORSTEN, G P M Een onderzoek naar de spontane electrlsche actlvltelt van her zoogdierruggemerg Dissertation University of Amsterdam, 1948 HORSTEN, G P M L'achvlte electnque de la moelle epmlere sous narcose ~ 1'ether et au Pentothal Arch let Pharmacodgn Ther, 1948, 77 212218 HORSTEN G P M L'mfluence des parties superleures de l encephale sur l'actlvlte electrique spontanee de la moelle epmiere Arch mternat Phystol, 1948, 56 117-129 OZORIO DE ALMEIDA, M et PmRON, H Achon de la peau sur l etat general du systeme nerveux chez la grenoudle C R Soc Btol, Paris, 199.4, 90 422-425 TEN CATE J Lacttvtte elecmque spontanee des differentes parties du systeme nerveux central J Phgstol, 1949 41 161-172 TEN CATE, J, WALTER, W G and KOOPMAN L J Electrical activity m frog spinal cord ] Neurophy~tol, 1947, 10 223-233 TEN CATE, J, HORSTEN, G P M e t KOOPMAN, L ] Influence des organes pGrlpherlques sur I acttvlte elecmque de la moelle dpmlere Arch tnternat Phgstol, 1947, 55 51-58
Reference TEN CATE, J Spontaneous electrical activity of the spinal cord 445-451
EEG Chn Neurophysmt, 19fi0, 2