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Excitability cycle of the visual cortex during sleep and wakefulness
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ELECTROENCEPHALOORAPHY AND CLINICAl. NEUROPHYSIOLDGY
E X C I T A B I L I T Y CYCLE O F T H E V I S U A L C O R T E X D U R I N G SLEEP A N D W A K E F U L N E S S 1 MARIe PALESTINI2, MARIe PISANO, GUIDO ROSADINI AND GIAN FRANCe ROSS1 Clinica Neurochirurgica dell'Universitd di Genova, Genoa (Italy)
(Accepted for publication: December 29, 1964) INTRODUCTION
The present research is part of a study of the excitability of the cerebral cortex of intact unanesthetized cats, during physiological changes in the degree of alertness: wakefulness and sleep. The excitability of the visual cortex was examined in the experiments reported below. As is well known, an electrical change of definite morphology and latency can be elicited by a volley of afferent impulses in almost all the structures of the brain (evoked potential). The interpretation of the neural mechanisms responsible for the genesis of such a potential is far from being satisfactory (Chang 1959); however, the changes in its amplitude are commonly considered to reflect changes in the functional condi. tions of the structure from which it is recorded. In previous researches we have shown that the amplitude of the late post-synaptic components (4th surface positive wave and 5th surface negative wave) of the electrical potential evoked in the visual cortex of the cat by a single electrical stimulus applied to the optic radiations is definitely influenced by the degree of alertness (Palestini et al. 1964; Rossi et al. 1965). Two stag~.~ of sleep of different depths can be recognized in the cat (see Rossi 1963, 1964 for references): a stage of light sleep, electroencephalographically characterized by slow, high voltage rhythms ("synchronized" sleep) and a stage of deep sleep, accompanied by fast, low voltage electroencephalographic activity ("desynchronized" sleep, with x The research was supported by "Consiglio Nazionale delle Ricerche (lmpresa di Elettrofisiologia) '° and Office of Scientific Research OAR through the European Office, Aerospace Research, United States Air Force (Grant AF EOAR 64-11). A preliminary note was published in Boll Soc. ital. Biol. sper., 1964, 39: 1662-1664. Present address: Centre de Psiquiatria Experimental, Universidad de Chile, Santiago de Chile.
electrocortical rhythms quite similar to those recorded during wakefulness), by complete muscular relaxation, marked blood pressure fall and typical rapid movements of the eyes. The amplitude of the cortical potentials evoked by a volley of impulses coming from the optic radiations was found to be definitely larger during sleep than during wakefulness; no constant or significant difference between the two phases of sleep was observed (Palestini et ai. 1964; Rossi et al. 1965). Similar results were obtained almost simultaneously by Cordeau (1965). Walsh and Cordeau (1964) anc~ Favale et al. (1964), though in the experiments of the last authors the amplitude of the potentials evoked during desynchronized sleep seemed very inconstant. These findings seemed to indicate that the cortical excitability is higher during sleep than during wakefulness. By recording the cortical electrical activity of cats through nonpolarizable electrodes connected with direct coupled differential amplifiers, Arduini et al. 0957) reported the appearance of a marked, long-lasting, surface negative potential shift during arousal from sleep. Caspers (1961, 1962, 1965) confirmed the phenomenon in intact unanesthetized rats; in addition, he made the interesting observation that sleep is accompanied by a surface-positive shift of the cortical electrical activity and that the amplitude of this shift is related to the depth of sleep. According to very recent findings of Wurtz et al. (1964) in the normal cat, the DC cortical potential, though negative at the moment of arousal from sleep, becomes positive during the wakeful state; a similar positive polarization is present during desynchronized sleep, while synchronized sleep is characterized by negative cortical polarization. We do not want to comment uponthe difference between the results of Caspers and ~-rWurtz and Eiectroeneeph. clin. NeurophysioL, 1965, 19:276--283
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coworkers. What matters is that, independent of their sign, these variations in the polarization of the cerebral cortex might have an influence on the amplitude of the electro-cortical responses to corticipetal impulses. As our hypothesis on the behavior of cortical excitability during sleep and wakefulness was based on the study of amplitude variations of the cortical evoked potentials, new experiments had to be performed to check its validity. In the present research, instead of comparing the amplitudes of cortical potentials evoked during the two stages of sleep and during wakefulness, we compared the so-called cortical "recovery cycle" in the three different conditions. With this technique the degree of excitability of the cortical neurons is given by the behavior of their refractoriness or depression following their activation by corticipetal impulses (Chang 1959). The phenomenon is expressed by the ratio between the amplitudes of two potentials evoked in the cortex by volleys of afferent impulses elicited by two identical stimuli, one following on the other in rapid succession, but with a variable interval. A phenomenon, therefore, that cannot be affected by the enduring changes in the polarization of the cerebral cortex described above.
CA). Screw electrodes fixed in the skull and steel wires passed through the posterior cervical muscles were connected with an ink-writing electroencephalograph (Battaglia-Rangoni M.10) and used for continuous monitoring of the electroencephalographic and electromyographic activity. The experimental sessions started at least two days after surgery and were repeated for several days. The cat was kept in a dark, relatively sound-proof cage. The variations of wakefulness and of the two phases of sleep were revealed by the electroencephalographic patterns and by the electrical activity of the posterior cervical muscles. RESULTS
I. Criteria followed for the evaluation o f the excitability level of the visual cortex Paired stimuli (SI and $2) of equal intensity and duration were applied to the optic radiations every 3-4 sec. The interval between S I and $2 ranged from 50 to 750 msec; the following intervals were usually employed: 50, 100, 150, 200, 250, 300, 350, 400, 450, 500 and 750 msec. Each pair l!0
RI
MATERIAL AND METHODS
Ten adult cats were used. The electrode implantation was performed under barbiturate anesthesia and with an aseptic technique similar to that previously described (Pisano et al. 1962; Palestini et al. 1964; Rossi et al. 1965). The optic radiations were bipolarly stimulated through copper electrodes, having the extremities electrolytically platinized, and implanted with the stereotaxic ipstrument. The locations ofthese electrodes were checked ph~,siologically during the operation and anatomically after the death of the animal. Paired impulses from 0.03 to 0.1 msec duration were used (Tektronix 161 and 162). Their intensity was arbitrarily fixed at a level 50% higher thail the lowest capable of constantly evoking a cortical response during relaxed wakefulness. Silver electrodes for recording were placed on the dura overlying the visual cortical area. The cortical responses were amplified (Grass P5), recorded on a cathode ray oscilloscope (Tektronix 502) and photographed (Grass
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iecovew cycle of the visual ~,oriicalresponse(11~)to optic
radiation stimulation in ,t typical experiment. I I is the control response (100~). Ordinates: amplitude of the tested response R2 relative to the amplitude of the control response RI in percentage units. Abscissae: intervals in msec between the stimuli SI and $2 evoking the responses RI and R2. Electroenceph. olin. Neurophysiol., 1965, 19:276-283
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of stimuli was applied 50 times during each one of the three conditions examined: wakefulness, sleep with electroencephalographic synchronization 0ight sleep) and sleep with electroencephalographic desynchronization (deep sleep). About 1650 pairs of stimuli were therefore employed in each experimental session. The reasons which necessitated such a large number of stimuli were reported and discussed els~,~where (Pisano et ai. 1962; Palestini et al. 1964; Rossi et al. 1965). The amplitudes of the two responses RI and R2 evoked in the visual cortex by each pair of radiation stimuli were measured between the peaks of the largest positive (C4) and negative (C5) deflections. The mean amplitudes of RI and of R2 were then calculated for each group of 50 pairs of responses to stimuli at a given interval. Finally, the ratio between the mean amplitudes of the two respon-
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ses to the two stimuli(mR2/mRl) was evaluated. As was expected, with the shortest intervals between SI and $2 the ratio mR2/mRl was less than 1 ; this was taken as an indication that the impulses arising from the second stimulus of ehe pair reached a subresponsive visual cortex. The progressiveincrease of the interval between S 1and $2 was followed by a parallel increase of the ratio mR2/mR 1, ascribed to the progressive recovery of cortical excitability. Finally, the ratio mR2/m R1 became equal to 1; the excitability of the cortical neurons at the moment they were activated by the second stimulus was considered to be completely recovered, being of the same magnitude as at the moment of the first stimulus. No attempt was made to study the cortical recovery cycle by employing S 1-$2 intervals of less than 50 msec.
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Fig. 2 Responses of the visual cortex to 5 pairs of identical stimuli applied to the optic radiations during synchronized sleep (LS), desynchronized sleep (DS) and wakefulness(W). The mean of the ratios between the 5, second (R2)'and the 5 first (RI) responses (m R2/RI) is similar during synchronized and desynchronizedsleep and higher during the two forms of sleep than during wakefuln--~s.Note the great fluctuationsin amplitude of the evoked potentials during synchronizedsleep and its relative stabilityduring desynchronizedsleepand wakefulness. Electroenceph. clin. Neurophysioi., 1965, 19:276-283
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CORTICAL EXCITABILITY DURING SLEEP
2. Changes in the excitability o f the visual cortex during wakefulness and the two stages ~,j"'~-'-~,¢e_pThe results of a typical experiment are illustrated in Fig. 1. In this and in the following figures the ratio mR2]mRl is given in percentage terms, RI being equal to 100. As can be seen in the figure, the excitability cycle during wakefulness is different from that recorded during sleep; on the contrary, it has a similar behavior during the synchronized (light) and during the desynchronized (deep) phases of sleep. The excitability cycle during wakefulness differs in the two following respects from those during the two forms of sleep: (a) the duration of the interval S 1-$2 necessary for complete recovery (mR2/mRl = 1) or, in other words, the duration of the period of subexcitability following RI, is longer during wakefulness than during both synchronized and desynchronized sleep; during wakefulness the amplitude of mR2 has not yet reached that of mR l when the interval S 1-$2 is long enough for complete recovery during sleep 050 msec); (b) the degree of depression of cortical excitability (revealed by the low level of R2) is greater during wakefulness than during sleep; the curve expressing the cortical excitability cycle during wakefulness is always below that expressing sleep and does not meet it with the intervals SI-$2 used (Fig. 3).
In the case illustrated in Fig. 1 the cortical recovery time is slightly shorterduringdesynchronized sleep than during synchronized sleep. Such a difference, however, was not present in all cats; in most experiments the two phases of sleep were characterized by similar excitability cycles (Fig. 3) and in one case a quicker recovery was found during synchronized sleep. Another typical finding is illustrated in Fig. 2, namely the great fluctuation of individual R2/RI ratios during synchronized sleep; a difference of 300% could be found.The value of the R2/KI ratio is definitely more uniform though not absolutely stable during both deep sleep and wakefulness. Fig. 3 gives the averaged results of all our experiments. The longer duration and greater degree of cortical depression during wakefulness than during both forms of sleep, illustrated in the first figure, is evident also here and seems to be a constant phenonienon. No relevant differences can be found between the two phases ofsleep. DISCUSSION
Depression of the excitability of the visual cortical neurons occurs following their activation by a volley of afferent impulses. Such a depression is of greater degree and longer duration during wakefulness than during both light sleep (EEG synchronization) and deep sleep (EEG desynchronization). This agrees with the findings Meon of oll e x p e r i m e n t s of Evarts et al. (1960) obtained with a technique 120 similar to the one here described but limited to R1 the study of wakefulness and of sleep with synchnmized EEG activity. As said at the beginning, the present research ¢/~i./" '80 was undertaken with the aim of checking the interpretation given to our previous work on the ~J 0 changes in amplitude of visual cortical responses 6~ & to single shocks to the lateral geniculate radiaR2 .s tions. The results support such an interpretation: g 4o the excitability of the visual cortex is higher durIk~t tam u - ing sleep than during wakefulness. deep sleep . . . . . . 20 Our results cannot disprove the hypothesis wokefulrm~ . . . . . . that changes of polarization of the cerebral cor(Intervol S l - $2) tex during sleep and wakefulness (Arduini et al. i I i I I I 50 150 2 5 0 3 5 0 4 5 0 550 rnsec 1957: Caspers 1961, 1962, 1965; Wurtz et al. Fig. 3 1964) influence the amplitude of evoked cortical Recovery cycle of the visual cortical response to optic potentials. However, they show that the variaradiation stimulation. Averagedresultsin 10cats. See Fig. tions in amplitude of the cortical response are I for explanation. •
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not exclusively due to different cortical potential gradients. In fact, the latter might perhaps influence the amplitude of a single evoked potential, but could not affect the ratio R2/RI studied in the present experiments. It is likely, therefore, that the changes in amplitude of the electrical potentials evoked in the visual cortex by stimulation of the optic radiations during sleep and wakefulness are due, at least in part, to corresponding differences in neuronal recruitment. The possible neural processes in the cerebral cortex underlying the changes in amplitude of the single cortical evoked potentials during physiological sleep and wakefulness have already been discussed at length by us (Palestini et al. 1964; Rossi et al. 1965) and by others (Evarts etal. 1960; at~,,.,! u . vt~t.J.tw . . .~11.. E 4 $~. lit ~,T~~ t 3 J , Llo,:A. , . ~ c'q. P~ , Cordeau 1965; see Bremer 1961 and Zanchetti 1962 for the literature on acute preparations). One may assume that the same processes are responsible for the changes in amplitude of the two cortical responses RI and R2. Whatever the nature of these neural mechanisms, the following remarks can be made. 1. The excitability of the visual cortical neurons activated by radiation impulses seems to be related to the two basic physiological conditions of vigilance: sleep and wakefulness. However, the level of the cortical excitability is similar during the two phases of sleep. The best known and generally accepted mechanism of sleep, at least in the cat, is the functional depression of the brain-stem reticular activating structures (see Rossi 1963, 1964, for references). It is likely that the depression of the activating system is: (a) present during all forms of physiological sleep and (b) the main neural event distinguishing sleep from wakefulness. The depression of the activating system, therefore, seems to parallel the changes in visual cortical excitability found in the present research. A causal relationship between the two phenomena might be suggested and seems supported by experimental findings obtained in acute preparations (see Bremer 1961 for references). During wakefulness the reticular activating system would have a depressing influence on visual cortical excitability; the increased excitability observed during both synchronized and desynchronized sleep would be due to release from depression.
The existence of inhibitory phenomena in the cerebral cortex during arousal seems supported by some results of micro-electrode work (Whitlock et al. 1953; Jasper 1958). However, other researches have shown that the level of activity of cortical neurons during wakefulness is similar to that recorded during sleep with EEG desynchronization and higher than that recorded during sleep with EEG synchronization (Evarts 1962, 1964; Arduini et al. 1963). We pointed out previously (Rossi et al. 1965) that the latter findings seem in contrast with the occurrence of inhibition during wakefulness. An attempt at interpretation of this apparent contrast was made recently by Evarts (1964) on the basis of the results obtained by analysing rate and temporal patterns of discharge of pyramidal tract neurons in the monkey; he suggested that during sleep with EEG synchronization the reduction of the inhibitory phenomena may be associated with a reduction of "excitatory drive". We do not know whether such an interpretation might be applicable to the behavior of the neurons of the visual cortex of the cat as well. However, the hypothesis of disinhibition during sleep would well explain our results. 2. The mean excitability levels (i.e. the mean of several R2/R1 ratios)are similar during the two forms of sleep. However, the value of the single R2/R1 ratio is very fluctuating during synchronized sleep and relatively stable during desynchronized sleep (Fig. 2). This seems to be the only difference that our experiments could show between the two phases of sleep. Since the cortical excitability is stable also during wakefulness, the phenomenon seems related to the patterns of electro-cortical activity as recorded in the EEG. The hypothesis has been made above that an ascending influence from the b,'ain-stem activating structures during wakefulness depresses the visual cortical excitability. It is well know that such an influence is responsible for the desynchronization of the electro-cortical rhythms characterizing wakefulness (see Rossi and Zanchetti 1957 for references); it is possible that this influence is also responsible for the stability of the co~ ~cal excitability cycle. According to the same hypo~ ~ -sis, at the beginnh, g of sleep the visual cortical excitability increases as a consequence of the reduction or suppression of the ascending Electroenceph. clin. Neurophysiol., 1965, 19:276-283
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CORTICAL EXCITABILITY DURING SLEEP
flow of reticular impulses. The reticular structures have a restraining influence on the thalamic synchronizing pacemaker; their depression, therefore, is followed by release of this pacemaker and synchronization of the electro-cortical rhythms (see Rossi and Zanchetti 1957 for references). It is possible that the large fluctuations of the visual conical excitability cycle observed during synchronized sleep are due to the varying activity of the synchronizing thalamo-cortical circuits. In the foregoing the persistence of the functional depression of the activating systems after the transition from synchronized to desynchronized sleep has been considered to be responsible tbr the persistence of the high cortical excitability. The occurrence of desynchronization in the second phase of sleep seems to be due to hypnogenic impulses ascending from the brainstem (see Rossi 1963, 1964 for references). It is possible that the same hypnogenic brain-stem influence has a stabilizing effect on cortical excitability and keeps it at a high level. As stated above, our results show that the excitability of the visual cortex is more stable during the desynchronized phase of sleep than during the synchronized one. That does not mean, however, that the cortical excitability during desynchronized sleep is absolutely stable. We know that phasic changes in cortical activity are present during desynchronized sleep (Evarts 1962, 1964; Mouret etal. 1963: Marchiafava and Pompeiano 1964), chiefly in coincidence with episodes of typical eye movements. We have no evidence of a possible relation between these changes and the behavior of cortical excitability. 3. The study ofthe recovery cycle asa means of investigating central nervous system excitability during physiological sleep and wakefulness has been applied so far only to the visual area of the cerebral cortex 1. However, several researches have been performed in intact unanesthetized cats on the changes in amplitude of single potenI When this paper was ready for publication, Dr. Allison informed us of his study of the recovery 6ycle of the somatic sensory cortex (Allison, T. Cortical and subcortical evoked responses to central stimuli during wakefulness and sleep. Eleetroenceph. clin. Neurophysiol., 1965, 18: 13 I - i 39). His results are in good agreement with those reported here.
tials evoked in other cortical areas and in thalamic nuclei (Pisano et al. 1962; Favale et al. 1963; Favale and Manfredi 1963; Okuma and Fujimori 1963; Frommer and Galambos 1964; Palestini et al. 1964; Cordeau 1965; Rossiet aL 1965) or on the variations of the threshold of electrical cortical stimulation (Hodes 1964). The results of these researches indicate that: (a) the excitability changes of the sensori-motor cortex during wakefulness and the two phases of sleep are to some extent different from those observed in the visual corticol area; (b) the excitability changes of the thalam~ relay nucki ventro-postero-lateralis and lateral geniculate, though similar for the two nuclei, are definitely different from those observed at the cortical level (highest excitability during desynchronized sleep and lowest excitability during synchronized sleep). These findings emphasize the limitations of our results and of their implication for the nature of sleep and arousal mechanisms. SUMMARY
The excitability cycle of the visual cortex of intact unanesthetized cats was studied during the states of wakefulness, sleep with EEG synchronization and sleep with EEG dcsynchronization. The study was made by analysing the relative amplitudes of the two potentials evoked in the visual cortical area by two identical stimuli to the optic radiations, separated by a variable time interval. The excitability of the visual cortical neurons is higher during sleep than during wakefulness; no significant differences are found between the two phases of sleep. The phenomenon is tentatively interpreted by assuming that during sleep the cerebral cortex is released from an inhibitory influence exerted by the reticular activating system. The fluctuations of cortical excitability during synchronized sleep might be due to the varying activity of the synchronizing thalamo-cortical circuits; its relative stability during desynchronized sleep might be ascribed to an ascending hypnogenic brainstem influence. Different cortical areas might show different excitability changes during sleep and wakefulness; the excitability changes ofthe thalamus seem to be partially different from those of the cerebral cortex. Electroenceph. clin. Neurophysiol., 1965, 19:276-283
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CYCLED'EXCITABILIT~DU CORTEXVISUELPENDANT LE SOMMEILET LA VEILLE
Les a u t e u r s 6 t u d i e n t le cycle d'excitabilit6 du cortex visuel chez le chat intact n o n anesth~si6, au ~cours des ~tats de veille, de sommeil avec synchronisation E E G et de sommeil avec d~synchronisation EEG. lls proc~dent ~ l'analyse des amplitudes relatives des deux potentiels 6voqu6s dans l'aire corticale visuelle par deux stimulations identiques appliqu6es aux radiations optiques et s6par~es par des intervalles de temps variables. L'excitabilit6 des neurones du cortex visuel est plus ~lev~e au c~urs du sommeil que pendant l'~tat de veille; il n'a pas 6t6 trouv6 de diff6rences significatives entre les deux phases de sommeil. Les auteurs tentent d'interpr~ter ce ph~nom~ne en ~mettant l'hypoth~se que durant le sommeil le cortex c~r6bral est lib6r~ d ' u n e influence inhibitrice exerc~e par le syst~me r6ticulaire activateur. Les fluctuations de l'excitabilit6 corticale pendant le sommeil synchronis6 pourraient ~tre dues ~t i'activit~ oscillante des circuits de synchronisation thalamo-corticaux; sa stabilit6 relative pendant le sommeil d6synchronis6 pourrait ~tre attribute ~ une influence ascendante hypnog~ne du tronc c6r~bral. Des aires corticales diff~rentes pourraient montrer des modifications diff~rentes d'excitabilit~ au cours du sommeil et de la veille; les ehangements d'excitabilit6 du thalamus paraissent diff~rer en partie de ceux du cortex c~r~bral. REFERENCES ARDUINI, A., BERLUCCHI,G. and STRATA,P. Pyramidal activity during sleep and wakefulness. Arch. ital. Biol,, 1963,101: 530-544. ARDUnq~,A., MANCtA,M. and MECHELSE,K. Slow potential changes elicited in the cerebral cortex by sensory reticular stimulations. Arch. itaL Biol., 1957, 95: 127138. BREMER, F. Neurogenic factors influencing the evoked potentials of the cerebral cortex. Sensory communication. M.I.T. and Wiley, New York, 1961: 675-698. CASPEr, H. Changes of cortical D.C. potentials in the sleep-wakefulness cycle. In G. E. W. WOLS~t,mOLMe and M. O'CoNNoR (Eds.), The nature of sleep. Churchill, London, l ~ i . 237-253. CASper, H. Die Vertinderungen der corticale Gleichspannung und ihre Beziehungen zur senso-motoriscnen Aktivittit (Verhalten) bei Weckreizungen am freibeweglichen Tier. Proc. int. Union. physiol. Sci., 22rid Congr. Leyden, 1962,1: 443-447.
CASPERS, H. Shifts of cortical steady potential during various stages of sleep. In M. $OUVL,r (Ed.), Aspects anatomo-fonctionneis de "la physiologie du sommeiL Coll. int. Centre Nat. Recherche Sci., Lyon, 1965. CHANG, H. T. The evoked potentials. In J. FIELD et al. (EAs.), Handbook of physiology, Sect. 1. Amer. Physiol. Sot., Washington, 1959,1: 229-313. CORDEAU,J. P. Vagiatious de la transmission des messages sensoriels en fonction des diff~rents ~tats d'~veil et de sommeil. In M. JOUVL~ (Ed.), Aspects a n a t o m o fonctimtnels de la physiologie du sommeiL Coll. int. Centre Nat. Recherche Sci., Lyon, 1965. EVARTS,E. V. Activity in neurons in visual cortex of the cat during sleep with low voltage fast EEG activity. J. NeurophysioL, 1962, 25: 812-816. EVARTS,E. V. Temporal patterns of discharge of pyramidal tract neurons during sleep and waking in the monkey. J. NeurophysioL, 1964, 27: 152-171. EVARTS,E. V., FLEMINO,T. C. and HUYrENLOCttER,P. R. Recovery cycle of visual cortex of the awake and sleeping cat. Amer. J. Physiol., 1960,199: 373-376. FAVALE, E., LOEn, C. and MANFREDI, M. Somatic responses evoked by central stimulation during natural sleep and during arousal. Arch. int. Physiol. Biochem., 1963, 7/: 229-235. FAVALE,E., LOEB,C. e MANFREDI,M. Modificazioni delle risposte evocate da stimolazione delle vie ottiche helle diverse fasi del sonno e del risveglio. Riv. Neurol., 1964, 34: 31-45. FAVALE,E. and MANFREDI,M. Pyramidal antidromic responses during natural sleep and arousal. Arch. int. Physiol. Biochem., 1963, 7/: 466-470. FROMMER,G. and GALAMBOS,R. Arousal effects on speci|ic thalamo-cortical evoked responses. Fed. Proc., 1964, 23: 209. HODES, R. Lower cortical threshold in rapid eye movefment periods than during sleep. Fed. Proc., 1964, 23: 208. JASPER, H. H. Recent advances in our understanding of ascending activities of the reticular system. In H. H. JASPER(Ed,), Reticular formation of the brain. Little, Brown and Co., Boston, 1958: 319-33 I. MARCHIAFAVA,P. L. and POMPEIANO,O. Pyramidal influence on spinal cord during desynchronized sleep. Arch. ital. Biol., 1964, 102: 500-529. MOURET, J., JEANNEROD,M. and JOUVET, M. L'activit6 61ectrique du ~yst~me visuel au cours de la phase paradoxal du sommeil chez le chat. J. Physiol. (Paris), 1963, 55: 305.-306. OKUMA, T. and FUJIMORt,M. Electrographic and evoked potential studies during sleep in the cat. Folia psychiat, neurol, jap., 1963,17: 25-50. PAt.ESTtNt,M., PISANO,M., ROSADnqI,G. and Ro~st, G. F. Responses evoked in the visual cortex by electrical stimulation of lateral geniculate body and optic radiations in the awake and sleeping cat. Exp. Neurol., 1964, 9: 17-30. PISANO,M., ROSADINI,G. • Rossl, G, F. Risposte corticali evocate da stimoli dromici ed antidromici durante il sonno e ia veglia. Riv. NeurobioL, 1962, 8: 414--426. Rossl, G. F. Sleep inducing mechanisms in the brain-stem. Eiectroenceph. clin. NeurophysioL, 1965, 19:276-283
CORTICAL EXCITABILITY DURING SLEEP
Electroenceph. din. NeurophysioL, 1963, Suppl. 24: 113-132. Rossl, G. F. A hypothesis on the neural basis of consciousness. Acta neurochir. ( Wien) , 1964,12:187-197. Rossl, G. F., PALF.Srml,M., I~SANO,M. and ROSADnql,G. An experimental study of the cortical reactivity during sleep and wakefulness. In M. JOUVET(lEd.), Aspects anatomo-fonctionnels de la physiologie du sommeil. Coll. int. Centre Nat. Recherche Sci., Lyon, 1965. Rossl, G. F. and ZANCUETrl,A. The brain stem reticular formation. Anatomy and physiology. Arch. ital. Biol., 1957, 95: 199-435.
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Reference: P ^ ~ N I , M., PISANO,M., ROSADINI,O. and Rossl, O. F. Excitability cycle of the visual cortex during sleep and wakefulness. Electroenceph. din. Neurophysiol., 1965,19: 276-283.
ELECTROENCEPHALOORAPHY AND CLINICAl. NEUROPHYSIOLDGY
E X C I T A B I L I T Y CYCLE O F T H E V I S U A L C O R T E X D U R I N G SLEEP A N D W A K E F U L N E S S 1 MARIe PALESTINI2, MARIe PISANO, GUIDO ROSADINI AND GIAN FRANCe ROSS1 Clinica Neurochirurgica dell'Universitd di Genova, Genoa (Italy)
(Accepted for publication: December 29, 1964) INTRODUCTION
The present research is part of a study of the excitability of the cerebral cortex of intact unanesthetized cats, during physiological changes in the degree of alertness: wakefulness and sleep. The excitability of the visual cortex was examined in the experiments reported below. As is well known, an electrical change of definite morphology and latency can be elicited by a volley of afferent impulses in almost all the structures of the brain (evoked potential). The interpretation of the neural mechanisms responsible for the genesis of such a potential is far from being satisfactory (Chang 1959); however, the changes in its amplitude are commonly considered to reflect changes in the functional condi. tions of the structure from which it is recorded. In previous researches we have shown that the amplitude of the late post-synaptic components (4th surface positive wave and 5th surface negative wave) of the electrical potential evoked in the visual cortex of the cat by a single electrical stimulus applied to the optic radiations is definitely influenced by the degree of alertness (Palestini et al. 1964; Rossi et al. 1965). Two stag~.~ of sleep of different depths can be recognized in the cat (see Rossi 1963, 1964 for references): a stage of light sleep, electroencephalographically characterized by slow, high voltage rhythms ("synchronized" sleep) and a stage of deep sleep, accompanied by fast, low voltage electroencephalographic activity ("desynchronized" sleep, with x The research was supported by "Consiglio Nazionale delle Ricerche (lmpresa di Elettrofisiologia) '° and Office of Scientific Research OAR through the European Office, Aerospace Research, United States Air Force (Grant AF EOAR 64-11). A preliminary note was published in Boll Soc. ital. Biol. sper., 1964, 39: 1662-1664. Present address: Centre de Psiquiatria Experimental, Universidad de Chile, Santiago de Chile.
electrocortical rhythms quite similar to those recorded during wakefulness), by complete muscular relaxation, marked blood pressure fall and typical rapid movements of the eyes. The amplitude of the cortical potentials evoked by a volley of impulses coming from the optic radiations was found to be definitely larger during sleep than during wakefulness; no constant or significant difference between the two phases of sleep was observed (Palestini et ai. 1964; Rossi et al. 1965). Similar results were obtained almost simultaneously by Cordeau (1965). Walsh and Cordeau (1964) anc~ Favale et al. (1964), though in the experiments of the last authors the amplitude of the potentials evoked during desynchronized sleep seemed very inconstant. These findings seemed to indicate that the cortical excitability is higher during sleep than during wakefulness. By recording the cortical electrical activity of cats through nonpolarizable electrodes connected with direct coupled differential amplifiers, Arduini et al. 0957) reported the appearance of a marked, long-lasting, surface negative potential shift during arousal from sleep. Caspers (1961, 1962, 1965) confirmed the phenomenon in intact unanesthetized rats; in addition, he made the interesting observation that sleep is accompanied by a surface-positive shift of the cortical electrical activity and that the amplitude of this shift is related to the depth of sleep. According to very recent findings of Wurtz et al. (1964) in the normal cat, the DC cortical potential, though negative at the moment of arousal from sleep, becomes positive during the wakeful state; a similar positive polarization is present during desynchronized sleep, while synchronized sleep is characterized by negative cortical polarization. We do not want to comment uponthe difference between the results of Caspers and ~-rWurtz and Eiectroeneeph. clin. NeurophysioL, 1965, 19:276--283
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coworkers. What matters is that, independent of their sign, these variations in the polarization of the cerebral cortex might have an influence on the amplitude of the electro-cortical responses to corticipetal impulses. As our hypothesis on the behavior of cortical excitability during sleep and wakefulness was based on the study of amplitude variations of the cortical evoked potentials, new experiments had to be performed to check its validity. In the present research, instead of comparing the amplitudes of cortical potentials evoked during the two stages of sleep and during wakefulness, we compared the so-called cortical "recovery cycle" in the three different conditions. With this technique the degree of excitability of the cortical neurons is given by the behavior of their refractoriness or depression following their activation by corticipetal impulses (Chang 1959). The phenomenon is expressed by the ratio between the amplitudes of two potentials evoked in the cortex by volleys of afferent impulses elicited by two identical stimuli, one following on the other in rapid succession, but with a variable interval. A phenomenon, therefore, that cannot be affected by the enduring changes in the polarization of the cerebral cortex described above.
CA). Screw electrodes fixed in the skull and steel wires passed through the posterior cervical muscles were connected with an ink-writing electroencephalograph (Battaglia-Rangoni M.10) and used for continuous monitoring of the electroencephalographic and electromyographic activity. The experimental sessions started at least two days after surgery and were repeated for several days. The cat was kept in a dark, relatively sound-proof cage. The variations of wakefulness and of the two phases of sleep were revealed by the electroencephalographic patterns and by the electrical activity of the posterior cervical muscles. RESULTS
I. Criteria followed for the evaluation o f the excitability level of the visual cortex Paired stimuli (SI and $2) of equal intensity and duration were applied to the optic radiations every 3-4 sec. The interval between S I and $2 ranged from 50 to 750 msec; the following intervals were usually employed: 50, 100, 150, 200, 250, 300, 350, 400, 450, 500 and 750 msec. Each pair l!0
RI
MATERIAL AND METHODS
Ten adult cats were used. The electrode implantation was performed under barbiturate anesthesia and with an aseptic technique similar to that previously described (Pisano et al. 1962; Palestini et al. 1964; Rossi et al. 1965). The optic radiations were bipolarly stimulated through copper electrodes, having the extremities electrolytically platinized, and implanted with the stereotaxic ipstrument. The locations ofthese electrodes were checked ph~,siologically during the operation and anatomically after the death of the animal. Paired impulses from 0.03 to 0.1 msec duration were used (Tektronix 161 and 162). Their intensity was arbitrarily fixed at a level 50% higher thail the lowest capable of constantly evoking a cortical response during relaxed wakefulness. Silver electrodes for recording were placed on the dura overlying the visual cortical area. The cortical responses were amplified (Grass P5), recorded on a cathode ray oscilloscope (Tektronix 502) and photographed (Grass
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radiation stimulation in ,t typical experiment. I I is the control response (100~). Ordinates: amplitude of the tested response R2 relative to the amplitude of the control response RI in percentage units. Abscissae: intervals in msec between the stimuli SI and $2 evoking the responses RI and R2. Electroenceph. olin. Neurophysiol., 1965, 19:276-283
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M. PALESTINIet aL
of stimuli was applied 50 times during each one of the three conditions examined: wakefulness, sleep with electroencephalographic synchronization 0ight sleep) and sleep with electroencephalographic desynchronization (deep sleep). About 1650 pairs of stimuli were therefore employed in each experimental session. The reasons which necessitated such a large number of stimuli were reported and discussed els~,~where (Pisano et ai. 1962; Palestini et al. 1964; Rossi et al. 1965). The amplitudes of the two responses RI and R2 evoked in the visual cortex by each pair of radiation stimuli were measured between the peaks of the largest positive (C4) and negative (C5) deflections. The mean amplitudes of RI and of R2 were then calculated for each group of 50 pairs of responses to stimuli at a given interval. Finally, the ratio between the mean amplitudes of the two respon-
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ses to the two stimuli(mR2/mRl) was evaluated. As was expected, with the shortest intervals between SI and $2 the ratio mR2/mRl was less than 1 ; this was taken as an indication that the impulses arising from the second stimulus of ehe pair reached a subresponsive visual cortex. The progressiveincrease of the interval between S 1and $2 was followed by a parallel increase of the ratio mR2/mR 1, ascribed to the progressive recovery of cortical excitability. Finally, the ratio mR2/m R1 became equal to 1; the excitability of the cortical neurons at the moment they were activated by the second stimulus was considered to be completely recovered, being of the same magnitude as at the moment of the first stimulus. No attempt was made to study the cortical recovery cycle by employing S 1-$2 intervals of less than 50 msec.
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Fig. 2 Responses of the visual cortex to 5 pairs of identical stimuli applied to the optic radiations during synchronized sleep (LS), desynchronized sleep (DS) and wakefulness(W). The mean of the ratios between the 5, second (R2)'and the 5 first (RI) responses (m R2/RI) is similar during synchronized and desynchronizedsleep and higher during the two forms of sleep than during wakefuln--~s.Note the great fluctuationsin amplitude of the evoked potentials during synchronizedsleep and its relative stabilityduring desynchronizedsleepand wakefulness. Electroenceph. clin. Neurophysioi., 1965, 19:276-283
279
CORTICAL EXCITABILITY DURING SLEEP
2. Changes in the excitability o f the visual cortex during wakefulness and the two stages ~,j"'~-'-~,¢e_pThe results of a typical experiment are illustrated in Fig. 1. In this and in the following figures the ratio mR2]mRl is given in percentage terms, RI being equal to 100. As can be seen in the figure, the excitability cycle during wakefulness is different from that recorded during sleep; on the contrary, it has a similar behavior during the synchronized (light) and during the desynchronized (deep) phases of sleep. The excitability cycle during wakefulness differs in the two following respects from those during the two forms of sleep: (a) the duration of the interval S 1-$2 necessary for complete recovery (mR2/mRl = 1) or, in other words, the duration of the period of subexcitability following RI, is longer during wakefulness than during both synchronized and desynchronized sleep; during wakefulness the amplitude of mR2 has not yet reached that of mR l when the interval S 1-$2 is long enough for complete recovery during sleep 050 msec); (b) the degree of depression of cortical excitability (revealed by the low level of R2) is greater during wakefulness than during sleep; the curve expressing the cortical excitability cycle during wakefulness is always below that expressing sleep and does not meet it with the intervals SI-$2 used (Fig. 3).
In the case illustrated in Fig. 1 the cortical recovery time is slightly shorterduringdesynchronized sleep than during synchronized sleep. Such a difference, however, was not present in all cats; in most experiments the two phases of sleep were characterized by similar excitability cycles (Fig. 3) and in one case a quicker recovery was found during synchronized sleep. Another typical finding is illustrated in Fig. 2, namely the great fluctuation of individual R2/RI ratios during synchronized sleep; a difference of 300% could be found.The value of the R2/KI ratio is definitely more uniform though not absolutely stable during both deep sleep and wakefulness. Fig. 3 gives the averaged results of all our experiments. The longer duration and greater degree of cortical depression during wakefulness than during both forms of sleep, illustrated in the first figure, is evident also here and seems to be a constant phenonienon. No relevant differences can be found between the two phases ofsleep. DISCUSSION
Depression of the excitability of the visual cortical neurons occurs following their activation by a volley of afferent impulses. Such a depression is of greater degree and longer duration during wakefulness than during both light sleep (EEG synchronization) and deep sleep (EEG desynchronization). This agrees with the findings Meon of oll e x p e r i m e n t s of Evarts et al. (1960) obtained with a technique 120 similar to the one here described but limited to R1 the study of wakefulness and of sleep with synchnmized EEG activity. As said at the beginning, the present research ¢/~i./" '80 was undertaken with the aim of checking the interpretation given to our previous work on the ~J 0 changes in amplitude of visual cortical responses 6~ & to single shocks to the lateral geniculate radiaR2 .s tions. The results support such an interpretation: g 4o the excitability of the visual cortex is higher durIk~t tam u - ing sleep than during wakefulness. deep sleep . . . . . . 20 Our results cannot disprove the hypothesis wokefulrm~ . . . . . . that changes of polarization of the cerebral cor(Intervol S l - $2) tex during sleep and wakefulness (Arduini et al. i I i I I I 50 150 2 5 0 3 5 0 4 5 0 550 rnsec 1957: Caspers 1961, 1962, 1965; Wurtz et al. Fig. 3 1964) influence the amplitude of evoked cortical Recovery cycle of the visual cortical response to optic potentials. However, they show that the variaradiation stimulation. Averagedresultsin 10cats. See Fig. tions in amplitude of the cortical response are I for explanation. •
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not exclusively due to different cortical potential gradients. In fact, the latter might perhaps influence the amplitude of a single evoked potential, but could not affect the ratio R2/RI studied in the present experiments. It is likely, therefore, that the changes in amplitude of the electrical potentials evoked in the visual cortex by stimulation of the optic radiations during sleep and wakefulness are due, at least in part, to corresponding differences in neuronal recruitment. The possible neural processes in the cerebral cortex underlying the changes in amplitude of the single cortical evoked potentials during physiological sleep and wakefulness have already been discussed at length by us (Palestini et al. 1964; Rossi et al. 1965) and by others (Evarts etal. 1960; at~,,.,! u . vt~t.J.tw . . .~11.. E 4 $~. lit ~,T~~ t 3 J , Llo,:A. , . ~ c'q. P~ , Cordeau 1965; see Bremer 1961 and Zanchetti 1962 for the literature on acute preparations). One may assume that the same processes are responsible for the changes in amplitude of the two cortical responses RI and R2. Whatever the nature of these neural mechanisms, the following remarks can be made. 1. The excitability of the visual cortical neurons activated by radiation impulses seems to be related to the two basic physiological conditions of vigilance: sleep and wakefulness. However, the level of the cortical excitability is similar during the two phases of sleep. The best known and generally accepted mechanism of sleep, at least in the cat, is the functional depression of the brain-stem reticular activating structures (see Rossi 1963, 1964, for references). It is likely that the depression of the activating system is: (a) present during all forms of physiological sleep and (b) the main neural event distinguishing sleep from wakefulness. The depression of the activating system, therefore, seems to parallel the changes in visual cortical excitability found in the present research. A causal relationship between the two phenomena might be suggested and seems supported by experimental findings obtained in acute preparations (see Bremer 1961 for references). During wakefulness the reticular activating system would have a depressing influence on visual cortical excitability; the increased excitability observed during both synchronized and desynchronized sleep would be due to release from depression.
The existence of inhibitory phenomena in the cerebral cortex during arousal seems supported by some results of micro-electrode work (Whitlock et al. 1953; Jasper 1958). However, other researches have shown that the level of activity of cortical neurons during wakefulness is similar to that recorded during sleep with EEG desynchronization and higher than that recorded during sleep with EEG synchronization (Evarts 1962, 1964; Arduini et al. 1963). We pointed out previously (Rossi et al. 1965) that the latter findings seem in contrast with the occurrence of inhibition during wakefulness. An attempt at interpretation of this apparent contrast was made recently by Evarts (1964) on the basis of the results obtained by analysing rate and temporal patterns of discharge of pyramidal tract neurons in the monkey; he suggested that during sleep with EEG synchronization the reduction of the inhibitory phenomena may be associated with a reduction of "excitatory drive". We do not know whether such an interpretation might be applicable to the behavior of the neurons of the visual cortex of the cat as well. However, the hypothesis of disinhibition during sleep would well explain our results. 2. The mean excitability levels (i.e. the mean of several R2/R1 ratios)are similar during the two forms of sleep. However, the value of the single R2/R1 ratio is very fluctuating during synchronized sleep and relatively stable during desynchronized sleep (Fig. 2). This seems to be the only difference that our experiments could show between the two phases of sleep. Since the cortical excitability is stable also during wakefulness, the phenomenon seems related to the patterns of electro-cortical activity as recorded in the EEG. The hypothesis has been made above that an ascending influence from the b,'ain-stem activating structures during wakefulness depresses the visual cortical excitability. It is well know that such an influence is responsible for the desynchronization of the electro-cortical rhythms characterizing wakefulness (see Rossi and Zanchetti 1957 for references); it is possible that this influence is also responsible for the stability of the co~ ~cal excitability cycle. According to the same hypo~ ~ -sis, at the beginnh, g of sleep the visual cortical excitability increases as a consequence of the reduction or suppression of the ascending Electroenceph. clin. Neurophysiol., 1965, 19:276-283
281
CORTICAL EXCITABILITY DURING SLEEP
flow of reticular impulses. The reticular structures have a restraining influence on the thalamic synchronizing pacemaker; their depression, therefore, is followed by release of this pacemaker and synchronization of the electro-cortical rhythms (see Rossi and Zanchetti 1957 for references). It is possible that the large fluctuations of the visual conical excitability cycle observed during synchronized sleep are due to the varying activity of the synchronizing thalamo-cortical circuits. In the foregoing the persistence of the functional depression of the activating systems after the transition from synchronized to desynchronized sleep has been considered to be responsible tbr the persistence of the high cortical excitability. The occurrence of desynchronization in the second phase of sleep seems to be due to hypnogenic impulses ascending from the brainstem (see Rossi 1963, 1964 for references). It is possible that the same hypnogenic brain-stem influence has a stabilizing effect on cortical excitability and keeps it at a high level. As stated above, our results show that the excitability of the visual cortex is more stable during the desynchronized phase of sleep than during the synchronized one. That does not mean, however, that the cortical excitability during desynchronized sleep is absolutely stable. We know that phasic changes in cortical activity are present during desynchronized sleep (Evarts 1962, 1964; Mouret etal. 1963: Marchiafava and Pompeiano 1964), chiefly in coincidence with episodes of typical eye movements. We have no evidence of a possible relation between these changes and the behavior of cortical excitability. 3. The study ofthe recovery cycle asa means of investigating central nervous system excitability during physiological sleep and wakefulness has been applied so far only to the visual area of the cerebral cortex 1. However, several researches have been performed in intact unanesthetized cats on the changes in amplitude of single potenI When this paper was ready for publication, Dr. Allison informed us of his study of the recovery 6ycle of the somatic sensory cortex (Allison, T. Cortical and subcortical evoked responses to central stimuli during wakefulness and sleep. Eleetroenceph. clin. Neurophysiol., 1965, 18: 13 I - i 39). His results are in good agreement with those reported here.
tials evoked in other cortical areas and in thalamic nuclei (Pisano et al. 1962; Favale et al. 1963; Favale and Manfredi 1963; Okuma and Fujimori 1963; Frommer and Galambos 1964; Palestini et al. 1964; Cordeau 1965; Rossiet aL 1965) or on the variations of the threshold of electrical cortical stimulation (Hodes 1964). The results of these researches indicate that: (a) the excitability changes of the sensori-motor cortex during wakefulness and the two phases of sleep are to some extent different from those observed in the visual corticol area; (b) the excitability changes of the thalam~ relay nucki ventro-postero-lateralis and lateral geniculate, though similar for the two nuclei, are definitely different from those observed at the cortical level (highest excitability during desynchronized sleep and lowest excitability during synchronized sleep). These findings emphasize the limitations of our results and of their implication for the nature of sleep and arousal mechanisms. SUMMARY
The excitability cycle of the visual cortex of intact unanesthetized cats was studied during the states of wakefulness, sleep with EEG synchronization and sleep with EEG dcsynchronization. The study was made by analysing the relative amplitudes of the two potentials evoked in the visual cortical area by two identical stimuli to the optic radiations, separated by a variable time interval. The excitability of the visual cortical neurons is higher during sleep than during wakefulness; no significant differences are found between the two phases of sleep. The phenomenon is tentatively interpreted by assuming that during sleep the cerebral cortex is released from an inhibitory influence exerted by the reticular activating system. The fluctuations of cortical excitability during synchronized sleep might be due to the varying activity of the synchronizing thalamo-cortical circuits; its relative stability during desynchronized sleep might be ascribed to an ascending hypnogenic brainstem influence. Different cortical areas might show different excitability changes during sleep and wakefulness; the excitability changes ofthe thalamus seem to be partially different from those of the cerebral cortex. Electroenceph. clin. Neurophysiol., 1965, 19:276-283
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M. PALFSI'INI et aL P.~SU~
CYCLED'EXCITABILIT~DU CORTEXVISUELPENDANT LE SOMMEILET LA VEILLE
Les a u t e u r s 6 t u d i e n t le cycle d'excitabilit6 du cortex visuel chez le chat intact n o n anesth~si6, au ~cours des ~tats de veille, de sommeil avec synchronisation E E G et de sommeil avec d~synchronisation EEG. lls proc~dent ~ l'analyse des amplitudes relatives des deux potentiels 6voqu6s dans l'aire corticale visuelle par deux stimulations identiques appliqu6es aux radiations optiques et s6par~es par des intervalles de temps variables. L'excitabilit6 des neurones du cortex visuel est plus ~lev~e au c~urs du sommeil que pendant l'~tat de veille; il n'a pas 6t6 trouv6 de diff6rences significatives entre les deux phases de sommeil. Les auteurs tentent d'interpr~ter ce ph~nom~ne en ~mettant l'hypoth~se que durant le sommeil le cortex c~r6bral est lib6r~ d ' u n e influence inhibitrice exerc~e par le syst~me r6ticulaire activateur. Les fluctuations de l'excitabilit6 corticale pendant le sommeil synchronis6 pourraient ~tre dues ~t i'activit~ oscillante des circuits de synchronisation thalamo-corticaux; sa stabilit6 relative pendant le sommeil d6synchronis6 pourrait ~tre attribute ~ une influence ascendante hypnog~ne du tronc c6r~bral. Des aires corticales diff~rentes pourraient montrer des modifications diff~rentes d'excitabilit~ au cours du sommeil et de la veille; les ehangements d'excitabilit6 du thalamus paraissent diff~rer en partie de ceux du cortex c~r~bral. REFERENCES ARDUINI, A., BERLUCCHI,G. and STRATA,P. Pyramidal activity during sleep and wakefulness. Arch. ital. Biol,, 1963,101: 530-544. ARDUnq~,A., MANCtA,M. and MECHELSE,K. Slow potential changes elicited in the cerebral cortex by sensory reticular stimulations. Arch. itaL Biol., 1957, 95: 127138. BREMER, F. Neurogenic factors influencing the evoked potentials of the cerebral cortex. Sensory communication. M.I.T. and Wiley, New York, 1961: 675-698. CASPEr, H. Changes of cortical D.C. potentials in the sleep-wakefulness cycle. In G. E. W. WOLS~t,mOLMe and M. O'CoNNoR (Eds.), The nature of sleep. Churchill, London, l ~ i . 237-253. CASper, H. Die Vertinderungen der corticale Gleichspannung und ihre Beziehungen zur senso-motoriscnen Aktivittit (Verhalten) bei Weckreizungen am freibeweglichen Tier. Proc. int. Union. physiol. Sci., 22rid Congr. Leyden, 1962,1: 443-447.
CASPERS, H. Shifts of cortical steady potential during various stages of sleep. In M. $OUVL,r (Ed.), Aspects anatomo-fonctionneis de "la physiologie du sommeiL Coll. int. Centre Nat. Recherche Sci., Lyon, 1965. CHANG, H. T. The evoked potentials. In J. FIELD et al. (EAs.), Handbook of physiology, Sect. 1. Amer. Physiol. Sot., Washington, 1959,1: 229-313. CORDEAU,J. P. Vagiatious de la transmission des messages sensoriels en fonction des diff~rents ~tats d'~veil et de sommeil. In M. JOUVL~ (Ed.), Aspects a n a t o m o fonctimtnels de la physiologie du sommeiL Coll. int. Centre Nat. Recherche Sci., Lyon, 1965. EVARTS,E. V. Activity in neurons in visual cortex of the cat during sleep with low voltage fast EEG activity. J. NeurophysioL, 1962, 25: 812-816. EVARTS,E. V. Temporal patterns of discharge of pyramidal tract neurons during sleep and waking in the monkey. J. NeurophysioL, 1964, 27: 152-171. EVARTS,E. V., FLEMINO,T. C. and HUYrENLOCttER,P. R. Recovery cycle of visual cortex of the awake and sleeping cat. Amer. J. Physiol., 1960,199: 373-376. FAVALE, E., LOEn, C. and MANFREDI, M. Somatic responses evoked by central stimulation during natural sleep and during arousal. Arch. int. Physiol. Biochem., 1963, 7/: 229-235. FAVALE,E., LOEB,C. e MANFREDI,M. Modificazioni delle risposte evocate da stimolazione delle vie ottiche helle diverse fasi del sonno e del risveglio. Riv. Neurol., 1964, 34: 31-45. FAVALE,E. and MANFREDI,M. Pyramidal antidromic responses during natural sleep and arousal. Arch. int. Physiol. Biochem., 1963, 7/: 466-470. FROMMER,G. and GALAMBOS,R. Arousal effects on speci|ic thalamo-cortical evoked responses. Fed. Proc., 1964, 23: 209. HODES, R. Lower cortical threshold in rapid eye movefment periods than during sleep. Fed. Proc., 1964, 23: 208. JASPER, H. H. Recent advances in our understanding of ascending activities of the reticular system. In H. H. JASPER(Ed,), Reticular formation of the brain. Little, Brown and Co., Boston, 1958: 319-33 I. MARCHIAFAVA,P. L. and POMPEIANO,O. Pyramidal influence on spinal cord during desynchronized sleep. Arch. ital. Biol., 1964, 102: 500-529. MOURET, J., JEANNEROD,M. and JOUVET, M. L'activit6 61ectrique du ~yst~me visuel au cours de la phase paradoxal du sommeil chez le chat. J. Physiol. (Paris), 1963, 55: 305.-306. OKUMA, T. and FUJIMORt,M. Electrographic and evoked potential studies during sleep in the cat. Folia psychiat, neurol, jap., 1963,17: 25-50. PAt.ESTtNt,M., PISANO,M., ROSADnqI,G. and Ro~st, G. F. Responses evoked in the visual cortex by electrical stimulation of lateral geniculate body and optic radiations in the awake and sleeping cat. Exp. Neurol., 1964, 9: 17-30. PISANO,M., ROSADINI,G. • Rossl, G, F. Risposte corticali evocate da stimoli dromici ed antidromici durante il sonno e ia veglia. Riv. NeurobioL, 1962, 8: 414--426. Rossl, G. F. Sleep inducing mechanisms in the brain-stem. Eiectroenceph. clin. NeurophysioL, 1965, 19:276-283
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Reference: P ^ ~ N I , M., PISANO,M., ROSADINI,O. and Rossl, O. F. Excitability cycle of the visual cortex during sleep and wakefulness. Electroenceph. din. Neurophysiol., 1965,19: 276-283.