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Facilitation of the direct cortical response of the visual cortex in association with rapid eye movement during paradoxical sleep in the cat
SHORT COMMUNICATIONS
415
Facilitation of the direct cortical response of the visual cortex in association with rapid eye movement during paradoxical sleep in the cat The direct cortical response (DCR) recorded from the surface of the cortex in the -vicinity of the stimulating electrode comprises several components 13,21. A threshold stimulus is followed by a slow negative deflection (N-wave) which is generally considered to represent postsynaptic potentials on the apical dendrites in the superficial layer of the cortex is. With stronger stimulation, the N-wave is preceded by several positive deflections (P-wave) which are believed to result from discharges in the deeper parts of the cortex la. Thus, with stimulus intensities which elicit a P- and N-wave complex, it is possible to detect the response of both the superficial cortical layer and the deeper parts of the cortex, Changes in the amplitude of the N-wave in the course of the sleep-wakefulness cycle have been briefly reported by several authors6,11,17. Simultaneously with bursts of the rapid eye movements (REM) of paradoxical sleep (PS) occur marked changes in activity not only in the oculomotor system but also in other sensory and m o t o r systems 1,2,16. During PS single neurons 9,1° show the characteristic pattern of rapid discharges separated by long silent intervals. In the visual cortex the discharges are often accompanied by a burst of R E M 9. It seemed probable that there might be changes in both the P- and N-waves of the D C R in the visual cortex during bursts of R E M in PS. To test this hypothesis, DCRs were recorded throughout the sleep-wakefulness cycle from the posterior lateral and the posterior sigmoid gyri of 11 cats with chronically implanted electrodes, described in detail elsewhere 19. DCRs were evoked at intervals of 1 sec with rectangular pulses of 0.01-0.04 msec duration at intensities which elicited monophasic N-waves or biphasic P- and N-wave complexes without causing any visible m o t o r responses. The EEG, the nuchal E M G and the electro-oculogram (EOG) were continuously monitored on a polygraph to ascertain the different stages of sleep. DCRs were displayed on a cathode ray oscilloscope simultaneously with the E O G or E E G ; measurement of the amplitudes of the various components was obtained from photographs. A
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Brain Research, 26 (1971) 415-419
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418
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When the animal was in an alert state (A) showing orientating responses, both P- and N-waves from the posterior lateral gyrus were of lower amplitude than when in the quiet waking state (QW) (Fig. 1). In slow wave sleep (SS), the P- and N-waves were of significantly greater amplitude than in QW. However, individual responses showed a considerable fluctuation in size, as shown by the large standard deviations in Table I. There was no apparent correlation between fluctuations in the DCRs and the occurrence of spindle waves in the EEG. During PS when the eyes were quiet (NREM), DCRs were usually of lower amplitude than during SS, but tended to be of greater amplitude than during QW. When DCRs were evoked during bursts of REM, both P- and N-waves were consistently facilitated. The increased amplitude of N-waves was significantly greater than was that of P-waves in these cases (Table I, N/P ratio). DCRs recorded from the posterior sigmoid gyrus did not show the same changes as did those recorded from the visual cortex. The responses were least when the animal was alert, as in recordings from the visual cortex, but they were of greatest amplitude during SS and were of slightly lower amplitude during REM bursts than in NREM. Fluctuations in the amplitude of the DCRs were less marked than in recordings from the visual cortex. Changes in the amplitude of the responses during the sleep-wakefulness cycle produced by weaker stimuli evoking monophasic N-waves only were essentially the same in both cortices as when stronger stimuli were employed. The N-wave is of greater amplitude during SS than during A over the suprasylvian gyrus 17 and the motor cortex 11 of the cat and the frontocentral cortex of the rat 6. This finding, confirmed by the present results, seems to hold true for various cortical sites. However, there were some differences in the responses over the posterior lateral and the posterior sigmoid gyri. In the posterior lateral cortex both P- and Nwaves were of greatest amplitude during REM bursts. However, in the posterior sigmoid cortex the amplitude of DCRs was greatest during SS and slightly reduced during REM bursts compared with their amplitude during NREM. Furthermore, there was no evidence for selective modification of P- or N-wave in any phase of the sleep-wakefulness cycle. According to current concepts of the mechanism of the DCR, the greater facilitation of N-waves than of P-waves in the posterior lateral gyrus during REM suggests that more apical dendrites were facilitated than were neurons of deeper layers. The facilitation may be related to PGO spikes 8 which have their origin in the pontine reticular formation 3 and appear in clusters over the occipital cortex during REM 14. Responses evoked by stimulation of the visual pathways 7,2° are also facilitated and there is an increase in single cell firing a in the visual cortex occurring simultaneously with PGO spikes. The absence of PGO spikes in the frontal cortex 4,x2 may be related to the lack of facilitation during REM in the posterior sigmoid gyrus. Department of Physiology, School of Dentistry, Aichi-Gakuin University, Nagoya 464 (Japan)
TOYOHIKO SATOH
1 BAUST,W., BERLUCCHI, G., AND MORUZZI, G., Changes in the auditory input in wakefulness Brain Research, 26 (1971) 415419
SHORT COMMUNICATIONS
2 3 4 5 6
7
8 9 10 11
12 13 14 15 16
17 18 19 20 21
419
and during the synchronized and desynchronized stages of sleep, Arch. ital. Biol., 102 (1964) 657-674. BIzzI, E., Discharge patterns of single geniculate neurons during the rapid eye movements of sleep, J. NeurophysioL, 29 (1966) 1087-1095. BIzzI, E., AND BROOKS, D. C., Functional connections between pontine reticular formation and lateral geniculate nucleus during deep sleep, Arch. ital. BioL, 101 (1963) 666-680. BROOKS,D. C., Localization and characteristics of the cortical waves associated with eye movement in the cat, Exp. Neurol., 22 (1968) 603-613. CALVET,J., CALVET, M. C., AND LANGLOIS,J. M., Diffuse cortical activation waves during socalled desynchronized EEG patterns, J. Neurophysiol., 28 (1965) 893-907. CASVERS,H., UND SCHULZE,H., Die Verfinderungen der corticalen Gleichspannung w~ihrend der natiJrlichen Schlaf-Wach-Perioden beim freibeweglichen Tier, Pfliigers Arch. ges. Physiol., 270 (1959) 103-120. DAGNINO,N., FAVALE,E., LOEB, C., MANFREDLM., AND SEITtrN, A., Nervous mechanisms underlying phasic changes in thalamic transmission during deep sleep, Electroenceph. clin. Neurophysiol., Suppl. 26 (1967) 156-163. DELORME, F., JEANNEROD,M., ET JOUVET, M., Effets remarquables de la r6serpine sur l'activit6 EEG phasique ponto-g6niculo-occipitale, C. R. Soc. Biol. (Paris}, 159 (1965) 900-903. EVARTS,E. V., Activity of neurons in visual cortex of cat during sleep with low voltage fast EEG activity, J. NeurophysioL, 25 (1962) 812-816. EVARTS, E. V., Temporal patterns of discharge of pyramidal tract neurons during sleep and waking in the monkey, J. NeurophysioL, 27 (1964) 152-171. IWAMA,K., AND KAWAMOTO,T., Responsiveness of cat motor cortex to electrical stimulation in sleep and wakefulness. In T. TOKIZANEAND J. P. SCHADfi (Eds.), Correlative Neurosciences, Progress in Brain Research, Vol, 21B, Elsevier, Amsterdam, 1966, pp. 54-63. JEANNEROD,M., AND SAKAI, K., Occipital and geniculate potentials related to eye movements in the unanaesthetized cat, Brain Research, 19 (1970) 361-377. LI, C. L., AND CHOU, S. N., Cortical intracellular synaptic potentials and direct cortical stimulation, J. cell. comp. Physiol., 60 (1962) 1-16. MOURET,J., JEANNEROD,M., ET JOUVET, M., L'activit6 61ectrique du syst~me visuel au cours de la phase paradoxale du sommeil chez le chat, J. Physiol. (Paris), 55 (1963) 305-306. OCHS, S., AND CLARK, F. J., Tetrodotoxin analysis of direct cortical responses, Electroenceph. clin. Neurophysiol., 24 (1968) 101-107. POMVEIANO,O., The neurophysiological mechanisms of the postural and motor events during desynchronized sleep. In S. S. KETV, E. V. EVARTSAND n . L. WILLIAMS(Eds.), Sleep and Altered States of Consciousness, Res. Publ. Ass. nerv. ment. Dis., Vol. 45, Williams and Wilkins, Baltimore, 1967, pp. 351-423. PURVtJRA, D. P., Observations on the cortical mechanism of EEG activation accompanying behavioral arousal, Science, 123 (1956) 804. PURVURA,D. P., AND GRUNDFEST,H., Nature of dendritic potentials and synaptic mechanisms in cerebral cortex of cat, J. Neurophysiol., 19 (1956) 573-595. SATOH,T., An electrode system for chronic recording of direct cortical response, J. PhysioL Soc. Japan, 32 (1970) 824-825. SATOI4, T., Relationship between the visual evoked response and the ponto-geniculo-occipital spike during natural sleep in the cat, J. Physiol. Soc. Japan, 32 (1970) 690-691. STOHR,P. E., GOLDRING,S., AND O'LEARY, J. L., Patterns of unit discharge associated with direct cortical response in monkey and cat, Electroenceph. din. Neurophysiol., 15 (1963) 882-888.
(Accepted December 18th, 1970)
Brain Research, 26 (1971) 415-419
415
Facilitation of the direct cortical response of the visual cortex in association with rapid eye movement during paradoxical sleep in the cat The direct cortical response (DCR) recorded from the surface of the cortex in the -vicinity of the stimulating electrode comprises several components 13,21. A threshold stimulus is followed by a slow negative deflection (N-wave) which is generally considered to represent postsynaptic potentials on the apical dendrites in the superficial layer of the cortex is. With stronger stimulation, the N-wave is preceded by several positive deflections (P-wave) which are believed to result from discharges in the deeper parts of the cortex la. Thus, with stimulus intensities which elicit a P- and N-wave complex, it is possible to detect the response of both the superficial cortical layer and the deeper parts of the cortex, Changes in the amplitude of the N-wave in the course of the sleep-wakefulness cycle have been briefly reported by several authors6,11,17. Simultaneously with bursts of the rapid eye movements (REM) of paradoxical sleep (PS) occur marked changes in activity not only in the oculomotor system but also in other sensory and m o t o r systems 1,2,16. During PS single neurons 9,1° show the characteristic pattern of rapid discharges separated by long silent intervals. In the visual cortex the discharges are often accompanied by a burst of R E M 9. It seemed probable that there might be changes in both the P- and N-waves of the D C R in the visual cortex during bursts of R E M in PS. To test this hypothesis, DCRs were recorded throughout the sleep-wakefulness cycle from the posterior lateral and the posterior sigmoid gyri of 11 cats with chronically implanted electrodes, described in detail elsewhere 19. DCRs were evoked at intervals of 1 sec with rectangular pulses of 0.01-0.04 msec duration at intensities which elicited monophasic N-waves or biphasic P- and N-wave complexes without causing any visible m o t o r responses. The EEG, the nuchal E M G and the electro-oculogram (EOG) were continuously monitored on a polygraph to ascertain the different stages of sleep. DCRs were displayed on a cathode ray oscilloscope simultaneously with the E O G or E E G ; measurement of the amplitudes of the various components was obtained from photographs. A
QW
SS
Post.
Gy.
NOREM ~c---
REM
. --.~.,~
•
Post.-~-..'-.'~- --~'~ SicJm..,...~f-"
~
.-~"~---~-~ "-~'-'7"f , /.
Fig. 1. Typical DCRs from the posterior lateral (upper) and the posterior sigmoid (lower) gyri in different phases of consciousness. Upper trace of each record, DCR. Lower traces, EOG except for SS where spindling on EEG is shown instead of FOG. Stimulus was applied at small dots. In A, small amount of muscular activities is superimposed. In REM, burst of REM is present on EOG. Upward deflection of DCR produced by surface negativity. Horizontal bar: 15 msec for DCR, 150 msec for EOG and EEG. Vertical bar: 1 mV for DCR, 600 #V for EOG and 100/~V for EEG. For explanation of abbreviations see text. Brain Research, 26 (1971) 415-419
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Brain Research, 26 (1971) 415-419
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418
SHORT COMMUNICATIONS
When the animal was in an alert state (A) showing orientating responses, both P- and N-waves from the posterior lateral gyrus were of lower amplitude than when in the quiet waking state (QW) (Fig. 1). In slow wave sleep (SS), the P- and N-waves were of significantly greater amplitude than in QW. However, individual responses showed a considerable fluctuation in size, as shown by the large standard deviations in Table I. There was no apparent correlation between fluctuations in the DCRs and the occurrence of spindle waves in the EEG. During PS when the eyes were quiet (NREM), DCRs were usually of lower amplitude than during SS, but tended to be of greater amplitude than during QW. When DCRs were evoked during bursts of REM, both P- and N-waves were consistently facilitated. The increased amplitude of N-waves was significantly greater than was that of P-waves in these cases (Table I, N/P ratio). DCRs recorded from the posterior sigmoid gyrus did not show the same changes as did those recorded from the visual cortex. The responses were least when the animal was alert, as in recordings from the visual cortex, but they were of greatest amplitude during SS and were of slightly lower amplitude during REM bursts than in NREM. Fluctuations in the amplitude of the DCRs were less marked than in recordings from the visual cortex. Changes in the amplitude of the responses during the sleep-wakefulness cycle produced by weaker stimuli evoking monophasic N-waves only were essentially the same in both cortices as when stronger stimuli were employed. The N-wave is of greater amplitude during SS than during A over the suprasylvian gyrus 17 and the motor cortex 11 of the cat and the frontocentral cortex of the rat 6. This finding, confirmed by the present results, seems to hold true for various cortical sites. However, there were some differences in the responses over the posterior lateral and the posterior sigmoid gyri. In the posterior lateral cortex both P- and Nwaves were of greatest amplitude during REM bursts. However, in the posterior sigmoid cortex the amplitude of DCRs was greatest during SS and slightly reduced during REM bursts compared with their amplitude during NREM. Furthermore, there was no evidence for selective modification of P- or N-wave in any phase of the sleep-wakefulness cycle. According to current concepts of the mechanism of the DCR, the greater facilitation of N-waves than of P-waves in the posterior lateral gyrus during REM suggests that more apical dendrites were facilitated than were neurons of deeper layers. The facilitation may be related to PGO spikes 8 which have their origin in the pontine reticular formation 3 and appear in clusters over the occipital cortex during REM 14. Responses evoked by stimulation of the visual pathways 7,2° are also facilitated and there is an increase in single cell firing a in the visual cortex occurring simultaneously with PGO spikes. The absence of PGO spikes in the frontal cortex 4,x2 may be related to the lack of facilitation during REM in the posterior sigmoid gyrus. Department of Physiology, School of Dentistry, Aichi-Gakuin University, Nagoya 464 (Japan)
TOYOHIKO SATOH
1 BAUST,W., BERLUCCHI, G., AND MORUZZI, G., Changes in the auditory input in wakefulness Brain Research, 26 (1971) 415419
SHORT COMMUNICATIONS
2 3 4 5 6
7
8 9 10 11
12 13 14 15 16
17 18 19 20 21
419
and during the synchronized and desynchronized stages of sleep, Arch. ital. Biol., 102 (1964) 657-674. BIzzI, E., Discharge patterns of single geniculate neurons during the rapid eye movements of sleep, J. NeurophysioL, 29 (1966) 1087-1095. BIzzI, E., AND BROOKS, D. C., Functional connections between pontine reticular formation and lateral geniculate nucleus during deep sleep, Arch. ital. BioL, 101 (1963) 666-680. BROOKS,D. C., Localization and characteristics of the cortical waves associated with eye movement in the cat, Exp. Neurol., 22 (1968) 603-613. CALVET,J., CALVET, M. C., AND LANGLOIS,J. M., Diffuse cortical activation waves during socalled desynchronized EEG patterns, J. Neurophysiol., 28 (1965) 893-907. CASVERS,H., UND SCHULZE,H., Die Verfinderungen der corticalen Gleichspannung w~ihrend der natiJrlichen Schlaf-Wach-Perioden beim freibeweglichen Tier, Pfliigers Arch. ges. Physiol., 270 (1959) 103-120. DAGNINO,N., FAVALE,E., LOEB, C., MANFREDLM., AND SEITtrN, A., Nervous mechanisms underlying phasic changes in thalamic transmission during deep sleep, Electroenceph. clin. Neurophysiol., Suppl. 26 (1967) 156-163. DELORME, F., JEANNEROD,M., ET JOUVET, M., Effets remarquables de la r6serpine sur l'activit6 EEG phasique ponto-g6niculo-occipitale, C. R. Soc. Biol. (Paris}, 159 (1965) 900-903. EVARTS,E. V., Activity of neurons in visual cortex of cat during sleep with low voltage fast EEG activity, J. NeurophysioL, 25 (1962) 812-816. EVARTS, E. V., Temporal patterns of discharge of pyramidal tract neurons during sleep and waking in the monkey, J. NeurophysioL, 27 (1964) 152-171. IWAMA,K., AND KAWAMOTO,T., Responsiveness of cat motor cortex to electrical stimulation in sleep and wakefulness. In T. TOKIZANEAND J. P. SCHADfi (Eds.), Correlative Neurosciences, Progress in Brain Research, Vol, 21B, Elsevier, Amsterdam, 1966, pp. 54-63. JEANNEROD,M., AND SAKAI, K., Occipital and geniculate potentials related to eye movements in the unanaesthetized cat, Brain Research, 19 (1970) 361-377. LI, C. L., AND CHOU, S. N., Cortical intracellular synaptic potentials and direct cortical stimulation, J. cell. comp. Physiol., 60 (1962) 1-16. MOURET,J., JEANNEROD,M., ET JOUVET, M., L'activit6 61ectrique du syst~me visuel au cours de la phase paradoxale du sommeil chez le chat, J. Physiol. (Paris), 55 (1963) 305-306. OCHS, S., AND CLARK, F. J., Tetrodotoxin analysis of direct cortical responses, Electroenceph. clin. Neurophysiol., 24 (1968) 101-107. POMVEIANO,O., The neurophysiological mechanisms of the postural and motor events during desynchronized sleep. In S. S. KETV, E. V. EVARTSAND n . L. WILLIAMS(Eds.), Sleep and Altered States of Consciousness, Res. Publ. Ass. nerv. ment. Dis., Vol. 45, Williams and Wilkins, Baltimore, 1967, pp. 351-423. PURVtJRA, D. P., Observations on the cortical mechanism of EEG activation accompanying behavioral arousal, Science, 123 (1956) 804. PURVURA,D. P., AND GRUNDFEST,H., Nature of dendritic potentials and synaptic mechanisms in cerebral cortex of cat, J. Neurophysiol., 19 (1956) 573-595. SATOH,T., An electrode system for chronic recording of direct cortical response, J. PhysioL Soc. Japan, 32 (1970) 824-825. SATOI4, T., Relationship between the visual evoked response and the ponto-geniculo-occipital spike during natural sleep in the cat, J. Physiol. Soc. Japan, 32 (1970) 690-691. STOHR,P. E., GOLDRING,S., AND O'LEARY, J. L., Patterns of unit discharge associated with direct cortical response in monkey and cat, Electroenceph. din. Neurophysiol., 15 (1963) 882-888.
(Accepted December 18th, 1970)
Brain Research, 26 (1971) 415-419