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Cortical long-axoned cells and putative interneurons during the sleep-waking cycle

Published online by Cambridge University Press:  04 February 2010

Mircea Steriade
Mircea Steriade
Affiliation:
Laboratoire de Neurophysiologie, Département de Physiologie, Faculté de Médecine, Université Laval, Québec, Canada G1K 7P4
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Abstract

Knowledge of the input-output characteristics of various neuronal types is a necessary first step toward an understanding of cellular events related to waking and sleep. In spite of the oversimplification involved, the dichotomy in terms of type I (long-axoned, output) neurons and type II (short-axoned, local) interneurons is helpful in functionally delineating the neuronal circuits involved in the genesis and epiphenomena of waking and sleep states. The possibility is envisaged that cortical interneurons, which are particularly related to higher neuronal activity and have been found in previous experiments to be more active during sleep than during wakefulness, might be involved in complex integrative processes occurring during certain sleep stages. Electrophysiological criteria for the identification of output cells and interneurons are developed, with emphasis on various possibilities and difficulties involved in recognizing interneurons of the mammalian brain. The high-frequency repetitive activity of interneurons is discussed, together with various possibilities of error to be avoided when interpreting data from bursting cells. Data first show opposite changes in spontaneous and evoked discharges of identified output cells versus putative interneurons recorded from motor and parietal association cortical areas in behaving monkeys and cats during wakefulness (W) compared to sleep with synchronized EEG activity (S): significantly increased rates of spontaneous firing, enhanced antidromic or synaptic responsiveness, associated with shorter periods of inhibition in type I (pyramidal tract, cortico-thalamic and cortico-pontine) cells during W versus significantly decreased frequencies of spontaneous discharge and depression of synaptically elicited reponses of type II cells during W compared to S. These findings are partly explained on the basis of recent iontophoretic studies showing that acetylcholine, viewed as a synaptic transmitter of the arousal system, excites output-type neurons and inhibits high-frequency bursting cells. Comparing W and S to the deepest stage of sleep with desynchronized EEG activity (D) in type I and type II cells revealed that: (a) the increased firing rates of output cells in D, over those in W and S, is substantially due to a tonic excitation during this state, and rapid eye movements (REMs) only contribute to the further increase of discharge frequencies; (b) in contrast, the increased rates of discharge in interneurons during D is entirely ascribable to REM-related firing. On the basis of experiments reporting that increased duration of D has beneficial effects upon retention of information acquired during W, the suggestion is made that increased firing rates of association cortical interneurons during REM epochs of D sleep are an important factor in maintaining the soundness of a memory trace.

Keywords

association cortexmotor cortexinterneuronsoutput cellsREM sleepsleep-waking cycle
Type
Target Article
Information
Behavioral and Brain Sciences , Volume 1 , Issue 3 , September 1978 , pp. 465 - 485
Copyright
Copyright © Cambridge University Press 1978

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References

REFERENCES

Altman, J. Postnatal growth and differentiation of the mammalian brain, with implications for a morphological theory of memory. In: The Neurosciences – a study program (ed. by Quarton, G. C., Melnechuk, Th., and Schmitt, F. O.), pp. 723–43. New York: The Rockefeller University Press, 1967.Google Scholar
Andersen, P., Eccles, J. C., and Loyning, Y.Pathway of postsynaptic inhibition in the hippocampus. Journal of Neurophysiology 27:608–19. 1964.CrossRefGoogle ScholarPubMed
Andersen, P., Eccles, J. C., and Sears, T. A.The ventro-basal complex of the thalamus: types of cells, their responses and their functional organization. Journal of Physiology (London). 174:370–99. 1964.CrossRefGoogle ScholarPubMed
Andersen, P., Gross, G. N., Lømø, T., and Sveen, O. Participation of inhibitory and excitatory interneurones in the control of hippocampal cortical output. In: The Interneuron (ed. by Brazier, M.A.B.), pp. 415–32. Berkeley and Los Angeles: University of California Press, 1969.CrossRefGoogle Scholar
Araki, T., and Terzuolo, C. A.Membrane currents in spinal motoneurones associated with the action potential and synaptic activity. Journal of Neurophysiology 25:772–89. 1962.CrossRefGoogle ScholarPubMed
Ben-Ari, Y., Dingledine, R., Kanazawa, I., and Kelly, J. S.Inhibitory effects of acetylcholine of neurons in the feline nucleus reticularis thalami. Journal of Physiology (London) 261:647–71. 1976a.CrossRefGoogle ScholarPubMed
Ben-Ari, Y., Kanazawa, I., and Kelly, J. S.Exclusively inhibitory action of iontophoretic acetylcholine on single neurones of feline thalamus. Nature. 259:327–30. 1976b.CrossRefGoogle ScholarPubMed
Bloch, V., and Fischbein, W. Sleep and psychological functions: memory. In: Experimental study of human sleep: methodological problems (ed. by Lairy, G. C. and Salzarulo, P.), pp. 157–73. Amsterdam: Elsevier, 1975.Google Scholar
Bodian, D. A model of synaptic and behavioral ontogeny. In: The Neurosciences – a second study program (ed. by Schmitt, F. O.), pp. 129–40. New York: The Rockefeller University Press, 1970.Google Scholar
Brock, L. G., Coombs, J. S., and Eccles, J. C.Intracellular recording from antidromically activated motoneurons. Journal of Physiology (London). 122:429–61. 1953.CrossRefGoogle Scholar
Burke, W. and Sefton, A. J.Discharge patterns of principal cells and interneurons in lateral geniculate nucleus of rat. Journal of Physiology (London). 187:201–12. 1966.CrossRefGoogle ScholarPubMed
Buser, P., Richard, D., and Lescop, J.Contrôle, par le cortex sensorimoteur, de la réactivité de cellules réticulaires mésencéphaliques chez le chat. Experimental Brain Research. 9:83–95. 1969.CrossRefGoogle Scholar
Calvin, W. H.Three modes of repetitive firing and the role of threshold time course between spikes. Brain Research. 69:341–46. 1974.CrossRefGoogle ScholarPubMed
Calvin, W. H.Generation of spike trains in CNS neurons. Brain Research, 84:1–22. 1975.CrossRefGoogle ScholarPubMed
Calvin, W. H. and Loeser, J. D.Doublet and burst firing patterns within the dorsal column nuclei of cat and man. Experimental Neurology, 48:406–26. 1975.CrossRefGoogle ScholarPubMed
Calvin, W. H., and Sypert, G. W.Fast and slow pyramidal tract neurons: an intracellular analysis of their contrasting repetitive firing properties in the cat. Journal of Neurophysiology 39:420–34. 1976.CrossRefGoogle ScholarPubMed
Calvin, W. H., and Ward, A. A. Jr.Structured timing patterns within bursts from epileptic neurons in undrugged monkey cortex. Experimental Neurology 21:535–49. 1968.CrossRefGoogle ScholarPubMed
Celesia, G. G., and Jasper, H. H.Acetylcholine released from cerebral cortex in relation to state of excitation. Neurology. 16:1053–64. 1966.CrossRefGoogle Scholar
Chang, H. T.Activation of internuncial neurons through collaterals of pyramidal fibers at cortical level. Journal of Neurophysiology 18:452–71. 1955.CrossRefGoogle ScholarPubMed
Colonnier, M. L. The structural design of the neocortex. In: Brain and conscious experience (ed. by Eccles, J. C.), pp. 1–23. New York: Springer, 1966.Google Scholar
Coombs, J. S., Eccles, J. C., and Fatt, P.The electrical properties of the motoneurone membrane. Journal of Physiology (London). 130:291–325. 1955.CrossRefGoogle ScholarPubMed
Darian-Smith, I., Phillips, C., and Ryan, R. D.Functional organization in the trigeminal main sensory and rostral spinal nuclei of the cat. Journal of Physiology (London). 168:129–46. 1963.CrossRefGoogle ScholarPubMed
Desiraju, T.Discharge properties of neurons of the parietal association cortex during states of sleep and wakefulness in the monkey. Brain Research, 47:69–75. 1972.CrossRefGoogle ScholarPubMed
Eccles, J. C.The inhibitory pathways of the central nervous system, 135 pp. Springfield, Ill., Thomas, 1969.Google Scholar
Eccles, J. C., Eccles, R. M., and Fatt, P.Pharmacological investigations on a central synapse operated by acetylcholine. Journal of Physiology (London). 131:154–69. 1956.CrossRefGoogle ScholarPubMed
Eccles, J. C., Eccles, R. M., Iggo, A., and Lundberg, A.Electrophysiological investigations of Renshaw cells. Journal of Physiology (London). 159:461–78, 1961.CrossRefGoogle ScholarPubMed
Eccles, J. C., Eccles, R. M., and Lundberg, A.Types of neurone in and around the intermediate nucleus of the lumbo-sacral cord. Journal of Physiology (London). 154:89–114. 1960.CrossRefGoogle Scholar
Eccles, J. C., Fatt, P., and Koketsu, K.Cholinergic and inhibitory synapses in a pathway from motor-axon collaterals to motoneurones. Journal of Physiology (London). 126:524–62. 1954.CrossRefGoogle Scholar
Eccles, J. C., Llinas, R., and Sasaki, K.The inhibitory interneurones within the cerebellar cortex. Experimental Brain Research 1:1–16. 1966.CrossRefGoogle ScholarPubMed
Evarts, E. V.Temporal patterns of discharge of pyramidal tract neurons during sleep and waking. Journal of Neurophysiology. 27:152–71. 1964.CrossRefGoogle ScholarPubMed
Evarts, E. V.Relation of discharge frequency to conduction velocity in pyramidal tract neurons. Journal of Neurophysiology. 28:216–28. 1965.CrossRefGoogle ScholarPubMed
Evarts, E. V. Unit activity in sleep and wakefulness. In: The Neurosciences – a study program (ed. by Quarton, G. C., Melnechuk, Th., and Schmitt, F. O.), pp. 545–556. New York: The Rockefeller University Press, 1967.Google Scholar
Evarts, E. V., Bental, E., Bihari, B., and Huttenlocher, P. R.Spontaneous discharge of single neurons during sleep and waking. Science. 135:726–28. 1962.CrossRefGoogle ScholarPubMed
Famiglietti, E. V. Jr.Dendro-dendritic synapses in the lateral geniculate nucleus of the cat. Brain Research. 20:181–91. 1970.CrossRefGoogle ScholarPubMed
Fischer-Perroudon, C., Mouret, J., and Jouvet, M.Sur un cas d'agrypnie (4 mois sans sommeil) au cours d'une maladie de Morvan. Effet favorable du 5-hydroxytryptophane. Electroencephalography and Clinical Neurophysiology. 36:1–18. 1974.CrossRefGoogle Scholar
Frigyesi, T. L.Intracellular recordings from neurons in dorsolateral thalamic reticular nucleus during capsular, basal ganglia and midline thalamic stimulation. Brain Research. 48:157–72. 1972.CrossRefGoogle ScholarPubMed
Fukuda, Y., and Iwama, K.Inhibition des interneurones du corps genouillé latéral par l'activation de la formation reticulée. Brain Research, 18:548–51. 1970.CrossRefGoogle Scholar
Fuller, J. F., and Schlag, J. S.Determination of antidromic excitation by the collision test: problems of interpretation. Brain Research. 112:283–98. 1976.CrossRefGoogle ScholarPubMed
Galindo, A., Krnjevic, K., and Schwartz, S.Patterns of firing in cuneate neurons and some effects of flaxedil. Experimental Brain Research. 5:87–101. 1968.CrossRefGoogle ScholarPubMed
Getting, P. A., and Willows, A. O. D.Modification of neuron properties by electrotonic synapses. II Burst formation by electrotonic synapses. Journal of Neurophysiology. 37:858–68. 1974.CrossRefGoogle ScholarPubMed
Gogan, P., Gueritand, J. P., Horcholle-Bossavit, G., and Tyc-Dumont, S.Inhibitory nystagmic interneurons. Physiological and anatomical identification within the abducens nucleus. Brain Research. 59:410–416. 1973.CrossRefGoogle ScholarPubMed
Golgi, C.Recherches sur l'histologie des centres nerveux. Archives Italiennes de Biologie. 3:285–317. 1886.Google Scholar
Granit, R., and Phillips, C. G.Excitatory and inhibitory processes acting upon individual Purkinje cells of the cerebellum in cats. Journal of Physiology (London). 133:520–47. 1956.CrossRefGoogle ScholarPubMed
Hajdu, F., Somogyi, Gy., and Tömböl, T.Neuronal and synaptic arrangement in the lateralis posterior-pulvinar complex of the thalamus in the cat. Brain Research. 73:89–104. 1974.CrossRefGoogle ScholarPubMed
Hikosaka, O., and Kawakami, T.Inhibitory interneurons in the reticular formation and their relation to vestibular nystagmus. Brain Research. 117:513–18. 1976.CrossRefGoogle ScholarPubMed
Hobson, J. A., and McCarley, R. W.Cortical unit activity in sleep and waking. Electroenceph. clin. Neurophysiol. 30:97–112. 1971.CrossRefGoogle ScholarPubMed
Hobson, J. A.Spontaneous discharge rates of cat cerebellar Purkinje cells in sleep and waking. Electroencephalography and Clinical Neurophysiology. 33:457–69. 1972.CrossRefGoogle ScholarPubMed
Hobson, J. A., Freedman, R., and Pivik, R. T.Time course of discharge rate changes by cat pontine brain stem neurons during the sleep cycle. Journal of Neurophysiology. 37:1297–1309. 1974a.CrossRefGoogle ScholarPubMed
Hobson, J. A., McCarley, R. W., Pivik, R. T. and Freedman, R.Selective firing by cat pontine brain-stem neurons in desynchronized sleep. Journal of Neurophysiology. 37:497–511. 1974b.CrossRefGoogle ScholarPubMed
Horridge, G. A. The interpretation of behavior in terms of interneurons. In: The Interneuron (ed. by Brazier, M. A. B.), pp. 1–20. Berkeley and Los Angeles: University of California Press, 1969.Google Scholar
Innocenti, G. M., and Manzoni, T.Response patterns of somatosensory cortical neurones to peripheral stimuli. An intracellular study. Archives Italiennes de Biologie. 110:322–47. 1972.Google ScholarPubMed
Ito, M., and Yoshida, M.The origin of cerebeliar-induced inhibition of Deiters neurones. I Monosynaptic initiation of the inhibitory postsynaptic potentials. Experimental Brain Research. 2:330–49. 1966.CrossRefGoogle ScholarPubMed
Iversen, S. D. Brain lesions and memory in animals. In: Physiological basis of memory (ed. by Deutsch, J. A.), pp. 305–64. New York: Academic Press, 1973.Google Scholar
Jacobson, M.Development of specific neuronal connections. Science. 163: 543–47. 1969.CrossRefGoogle ScholarPubMed
Jankowska, E. Identification of interneurons interposed in different spinal reflex pathways. In: Golgi Centennial Symposium (ed. by Santini, M.), pp. 236–46. New York: Raven Press, 1975.Google Scholar
Jankowska, E. and Lindström, S.Morphology of interneurones mediating Ia reciprocal inhibition of motoneurones in the spinal cord of the cat. Journal of Physiology (London). 226:805–23. 1972.CrossRefGoogle ScholarPubMed
Jasper, H. H., Khan, R. T., and Elliot, K. A. C.Amino-acids released from the cerebral cortex in relation to its state of activation. Science. 147:1448–49. 1965.CrossRefGoogle ScholarPubMed
Jasper, H., Ricci, G. F., and Doane, B. Patterns of cortical neuron discharge during conditioned response in monkeys. In: Neurological basis of behavior (ed. by Wolstenholme, G. E. W. and Connor, C. M.), pp. 277–94. Boston: Ciba Found Symposium, 1957.Google Scholar
Jones, E. G.Varieties and distribution of non-pyramidal cells in the somatic sensory cortex of the squirrel monkey. Journal of Comparative Neurology. 160:205–67. 1975.CrossRefGoogle ScholarPubMed
Jordan, L. M., and Phillis, J. W.Acetylcholine inhibition in the intact and chronically isolated cerebral cortex. British Journal of Pharmacology. 45:584–95. 1972.CrossRefGoogle ScholarPubMed
Jouvet, M.Neurophysiology of the states of sleep. Physiological Review. 47:117–77. 1967.CrossRefGoogle ScholarPubMed
Jouvet, M.Essai sur le rêve. Archives Italiennes de Biologie. 111:564–76. 1973.Google Scholar
Kandel, E. R., Frazier, W. T., Waziri, R., and Coggeshall, R. E.Direct and common connections among the identified neurons in Aplysia. Journal of Neurophysiology. 33:1352–76. 1967.CrossRefGoogle Scholar
Kelly, J. P., and Van Essen, D. C.Cell structure and function in the visual cortex of the cat. Journal of Physiology (London). 238:515–47. 1974.CrossRefGoogle ScholarPubMed
Kitsikis, A., and Steriade, M.Thalamic, callosal and reticular converging inputs to parietal association cortex in cat. Brain Research. 93:516–24. 1975.CrossRefGoogle ScholarPubMed
Koike, H., Mano, N., Okada, Y., and Oshima, T.Repetitive impulses generated in fast and slow pyramidal tract cells by intracellularly applied current steps. Experimental Brain Research. 11:263–81. 1970.CrossRefGoogle ScholarPubMed
Koike, H., Okada, Y., and Oshima, T.Accommodative properties of fast and slow pyramidal tract cells and their modification by different levels of their membrane potentials. Exp. Brain Res. 5:189–201. 1968.CrossRefGoogle Scholar
Krnjević, K.Chemical nature of synaptic transmission in vertebrates. Physiological Review. 54:418–540. 1974.CrossRefGoogle Scholar
Krnjević, K., Pumain, R., and Renaud, L.The mechanism of excitation by acetylcholine in the cerebral cortex. Journal of Physiology (London). 215:247–68. 1971.CrossRefGoogle ScholarPubMed
Kuno, M. Transmitter action and multiple discharge. In: Basic mechanisms of the epilepsies (ed. by Jasper, H. H., Ward, A. A. Jr., and Pope, A.), pp. 130–35. Boston: Little, Brown and Co., 1969.Google Scholar
Kuno, M. and Miyahara, J. T.Factors responsible for multiple discharge of neurons in Clarke's column. Journal of Neurophysiology. 31:624–38. 1968.CrossRefGoogle ScholarPubMed
Kupfermann, I., Carew, Th. J., and Kandel, E. R.Local, reflex, and central commands controlling gill and siphon movements in Aplysia. Journal of Neurophysiology. 37:996–1019. 1974.CrossRefGoogle ScholarPubMed
Lamarre, Y., Filion, M., and Cordeau, J. P.Neuronal discharges of the ventrolateral nucleus of the thalamus during sleep and wakefulness in the cat. I Spontaneous activity: Experimental Brain Research. 12:480–98. 1971.CrossRefGoogle ScholarPubMed
Leconte, P., Hennevin, E., and Bloch, V.Analyse des effets d'un apprentissage et de son niveau d'acquisition sur le sommeil paradoxal consécutif. Brain Research. 49:367–79. 1973.CrossRefGoogle Scholar
Li, C. L. Activity of interneurons in the motor cortex. In: Reticular formation of the brain (ed. by Jasper, H. H., Proctor, L. D., Knighton, R. S., Noshay, W. S., and Costello, R. T.), pp. 459–72. Boston-Toronto: Little, Brown and Co., 1958.Google Scholar
Llinas, R., Baker, R., and Sotelo, C.Electrotonic coupling between neurons in cat inferior olive. Journal of Neurophysiology. 37:560–71. 1974.CrossRefGoogle ScholarPubMed
Longo, V. G., Martin, W. R., and Unna, K. R.A pharmacological study on the Renshaw cell. Journal of Pharmacology and Experimental Therapeutics. 129:61–68. 1960.Google Scholar
Lorente de Nó, R. The cerebral cortex: architecture, intracortical connections and motor projections. In: Physiology of the nervous system (ed. by Fulton, J. F.), pp. 291–321. London: Oxford University Press, 1938.Google Scholar
Lucero, M.Lengthening of REM sleep duration consecutive to learning in the rat. Brain Research. 20:319–22. 1970.CrossRefGoogle ScholarPubMed
Lundberg, A. Discussion. In: The Interneuron (ed. by Brazier, M. A. B.), p. 223. Berkeley and Los Angeles: University of California Press, 1969.Google Scholar
Lundberg, A. Convergence of excitatory and inhibitory action on interneurones in the spinal cord. In: The Interneuron (ed. by Brazier, M. A. B.), pp. 231–65. Berkeley and Los Angeles: University of California Press, 1969.CrossRefGoogle Scholar
Marco, L. A., Brown, T. S., and Rouse, M. E.Unitary responses in ventrolateral thalamus upon intranuclear stimulation. Journal of Neurophysiology. 30:482–93. 1967.CrossRefGoogle ScholarPubMed
Massion, J., Angaut, P., and Albe-Fessard, D.Activités évoquées chez le chat dans la région du nucleus ventralis lateralis par diverses stimulations sensorielles. II Etude microphysiologique. Electroencephalography and Clinical Neurophysiology. 19:452–69. 1965.CrossRefGoogle Scholar
Minderhoud, J. M.An anatomical study of the efferent connections of the thalamic reticular nucleus. Experimental Brain Research. 12:435–46. 1971.CrossRefGoogle Scholar
Mitra, N. L.Quantitative analysis of cell types in mammalian neocortex. Journal of Anatomy. 89:467–83. 1955.Google Scholar
Morest, D. K.Dendrodendritic synapses of cells that have axons: the fine structure of the Golgi type II cell in the medial geniculate body of the cat. Zeitschrift fuer Anatomie and Entwicklungsgeschichte. 133:216–46. 1971.CrossRefGoogle ScholarPubMed
Moruzzi, G. The functional significance of sleep in particular regard to the brain mechanisms underlying consciousness. In: Brain and conscious experience (ed. by Eccles, J. C.), pp. 345–79. New York: Springer, 1966.Google Scholar
Naito, H., Nakamura, K., Kurosaki, T., and Tamura, Y.Precise location of fast and slow pyramidal tract cells in cat sensorimotor cortex. Brain Research. 14:237–39. 1969.CrossRefGoogle ScholarPubMed
Nakamura, Y., Goldberg, L. J., Chandler, S. H., and Chase, M. H.Intracellular analysis of trigeminal motoneuron activity during sleep in the cat. Science. 199:204–207. 1978.CrossRefGoogle ScholarPubMed
Nakamura, Y., Nozaki, S., Takatori, M., and Kikuchi, M.Possible inhibitory neurons in the bulbar reticular formation involved in the cortically evoked inhibition of the masseteric motoneuron of the cat. Brain Research. 115:512–17. 1976.CrossRefGoogle ScholarPubMed
Noda, H., and Adey, W. R.Firing of neuron pairs in cat association cortex during sleep and wakefulness. Journal of Neurophysiology. 33:672–84. 1970a.CrossRefGoogle ScholarPubMed
Noda, H.Firing variability in cat association cortex during sleep and wakefulness. Brain Research. 18:513–26. 1970b.CrossRefGoogle ScholarPubMed
Noda, H.Changes in neuronal activity in association cortex of the cat in relation to sleep and wakefulness. Brain Research. 19:263–75. 1970c.CrossRefGoogle ScholarPubMed
Noda, H.Neuronal activity in the association cortex of the cat during sleep, wakefulness and anesthesia. Brain Research. 54:243–59. 1973.CrossRefGoogle ScholarPubMed
Paintal, A. S.Intramuscular propagation of sensory impulses. Journal of Physiology (London). 148:240–51. 1959.CrossRefGoogle ScholarPubMed
Pasik, P., Pasik, T., and Hamori, J.Synapses between interneurons in the lateral geniculate nucleus of monkeys. Experimental Brain Research. 25:1–13. 1976.CrossRefGoogle ScholarPubMed
Pasik, P. and Szentagothai, J.Golgi type II interneurons in the neuronal circuit the monkey lateral geniculate nucleus. Experimental Brain Research. 17:18–34. 1973.CrossRefGoogle ScholarPubMed
Pavlov, I. P.“Innere Hemmung” der bedingten Reflexe und der Schlafein und derselbe Prozess. Skand. Arch. Physiol. 44:42–58. 1923.Google Scholar
Phillis, J. W.Acetylcholine release from the cerebral cortex: its role in cortical arousal. Brain Research. 7:378–89. 1968.CrossRefGoogle ScholarPubMed
Phillis, J. W. and York, D. H.Pharmacological studies on a cholinergic inhibition in the cerebral cortex. Brain Research. 10:297–306. 1968.CrossRefGoogle ScholarPubMed
Pollen, D. A.Intracellular studies of cortical neurons during thalamic induced wave and spike. Electroencephalography and Clinical Neurophysiology. 17:398–404. 1964.CrossRefGoogle ScholarPubMed
Prince, D. A. Topical convulsant drugs and metabolic antagonists. In: Experimental models of epilepsy, (ed. by Purpura, D. P., Penry, J. K., Tower, D. B., Woodbury, D. M., and Walter, R. D.), pp. 51–83. New York: Raven Press, 1972.Google Scholar
Purpura, D. P. Intracellular studies of synaptic organizations in the mammalian brain. In: Structure and function of synapses (ed. by Pappas, G. D. and Purpura, D. P.), pp. 257–302. New York: Raven Press, 1972.Google Scholar
Purpura, D. P. and Cohen, B.Intracellular recording from thalamic neurons during recruiting responses. Journal of Neurophysiology. 25:621–35. 1962.CrossRefGoogle ScholarPubMed
Purpura, D. P., McMurtry, J. G., and Maekawa, K.Synaptic events in ventro-lateral thalamic neurons during suppression of recruiting responses by brain stem reticular stimulation. Brain Research. 1:63–76. 1966.CrossRefGoogle Scholar
Purpura, D. P., Shofer, R. J., and Musgrave, F. S.Cortical intracellular potentials during augmenting and recruiting responses. II patterns of synaptic activities in pyramidal and nonpyramidal tract neurons. Journal of Neurophysiology. 27:133–51. 1964.CrossRefGoogle ScholarPubMed
Puzillout, J. J., and Ternaux, J. P.Origine pyramidale des variations phasiques bulbaires observées lors de l'endormement. Brain Research. 66:85–102. 1974.CrossRefGoogle Scholar
Ralston, H. J. III, and Herman, M. M.The fine structure of neurons and synapses in the ventro-basal thalamus of the cat. Brain Research. 14:77–97. 1969.CrossRefGoogle Scholar
Ramón y Cajal, S.Histologie du système nerveux de l'homme et des vertébrés, vol. II, 993 pp. Madrid: Consejo Superior de Investigaciones Cientificas, Instituto Ramon y Cajal (1955) (original edition Paris: Maloine, 1911).Google Scholar
Ramón y Cajal, S.Studies on vertebrate neurogenesis. Springfield, Ill.: Thomas, 1960 (revision and translation of a 1929 edition).Google Scholar
Renaud, L. P., and Kelly, J. S.Identification of possible inhibitory neurons in the pericruciate cortex of the cat. Brain Research. 79:9–28. 1974.CrossRefGoogle ScholarPubMed
Renaud, L. P.Simultaneous recordings from pericruciate pyramidal tract and nonpyramidal tract neurons; response to stimulation of inhibitory pathways Brain Research. 79:29–44. 1974.CrossRefGoogle ScholarPubMed
Renshaw, B.Central effects of centripetal impulses in axons of spinal ventral roots. Journal of Neurophysiology. 9:191–204. 1946.CrossRefGoogle ScholarPubMed
Sakakura, H.Spontaneous and evoked unitary activities of cat lateral geniculate neurons in sleep and wakefulness. Japanese Journal of Physiology. 18:23–42. 1968.Google ScholarPubMed
Scheibel, M. E., and Scheibel, A. B.The organization of the nucleus reticularis thalami: A Golgi study. Brain Research. 1:43–62. 1966.CrossRefGoogle Scholar
Scheibel, M. E. Anatomical basis of attention mechanisms in vertebrate brains. In: The Neurosciences – a study program (ed. by Quarton, G. C., Melnechuk, Th., and Schmitt, F. O.), pp. 577–602. New York: The Rockefeller University Press, 1967.Google Scholar
Scheibel, M. E. Elementary processes in selected thalamic and cortical subsystems – the structural substrates. In: The Neurosciences – second study program (ed. by Schmitt, F. O.), pp. 443–57. New York: The Rockefeller University Press, 1970.Google Scholar
Scheibel, M. E., Davies, Th. L., and Scheibel, A. B.On thalamic substrates of cortical synchrony. Neurology. 23:300–04. 1973.CrossRefGoogle ScholarPubMed
Schlag, J., and Waszak, M.Electrophysiological properties of units in the thalamic reticular complex. Experimental Neurology. 32:79–97. 1971.CrossRefGoogle ScholarPubMed
Shepherd, G. M.Responses of mitral cells to olfactory nerve volleys in the rabbit. Journal of Physiology (London). 168:89–100. 1963a.CrossRefGoogle ScholarPubMed
Shepherd, G. M.Neuronal systems controlling mitral cell excitability. Journal of Physiology (London). 168:101–17. 1963b.CrossRefGoogle ScholarPubMed
Shepherd, G. M. The olfactory bulb as a simple cortical system: experimental analysis and functional implications. In: The Neurosciences – a second study program (ed. by Schmitt, F. O.), pp. 539–52. New York: The Rockefeller University Press, 1970.Google Scholar
Sherrington, C. S.Man on his nature. New York: Doubleday, 1955.Google Scholar
Skrebitsky, V. B., and Sharonova, I. N.Reticular suppression of flashevoked IPSPs in visual cortex neurons. Brain Research. 111:67–78. 1976.CrossRefGoogle ScholarPubMed
Sloper, J. J.An electron microscopic study of the neurons of the primate motor and somatic sensory cortices. Journal of Neurocytology. 2:351–59. 1973.CrossRefGoogle ScholarPubMed
Spencer, W. A. Discussion. In: The Interneuron (ed. by Brazier, M. A. B.), pp. 432–41. Berkeley and Los Angeles: University of California Press, 1969.Google Scholar
Stefanis, C. Interneuronal mechanisms in the cortex. In: The Interneuron (ed. by Brazier, M. A. B.), pp. 497–526. Berkeley and Los Angeles: University of California Press, 1969.CrossRefGoogle Scholar
Steriade, M.Ascending control of motor cortex responsiveness. Electroencephalography and Clinical Neurophysiology. 26:25–40. 1969.CrossRefGoogle ScholarPubMed
Steriade, M. Short-axoned cells in the motor thalamocortical system during sleep and waking. In: Neural systems and circuitry concerned with sleepwaking behavior (ed. by Morgane, P. J. and Stern, W. C.), pp. 47–61. Los Angeles: UCLA Brain Information Service, 1973.Google Scholar
Steriade, M.Interneuronal epileptic discharges related to spike-and-wave cortical seizures in behaving monkeys. Electroencephalography and Clinical Neurophysiology. 37:247–63. 1974.CrossRefGoogle ScholarPubMed
Steriade, M. Cortical inhibition during sleep and waking. In: Mechanisms in transmission of signals for conscious behaviour (ed. by Desiraju, T.), pp. 209–48. Amsterdam: Elsevier, 1976.Google Scholar
Steriade, M., Apostol, V., and Oakson, G.Control of unitary activities in cerebellothalamic pathway during wakefulness and synchronized sleep. Journal of Neurophysiology. 34:384–413. 1971.CrossRefGoogle ScholarPubMed
Steriade, M., and Deschênes, M.Cortical interneurons during sleep and waking in freely moving primates. Brain Research. 50:192–99. 1973.CrossRefGoogle ScholarPubMed
Steriade, M.Inhibitory processes and interneuronal apparatus in motor cortex during sleep and waking. II Recurrent and afferent inhibition of pyramidal tract neurons. Journal of Neurophysiology. 37:1093–1113. 1974.CrossRefGoogle ScholarPubMed
Steriade, M. and Oakson, G.Inhibitory processes and interneuronal apparatus in motor cortex during sleep and waking. I Background firing and responsiveness of pyramidal tract neurons and interneurons. Journal of Neurophysiology. 37:1065–92. 1974.CrossRefGoogle ScholarPubMed
Steriade, M., Deschênes, M., Wyzinski, P., and Hallé, J. Y. Input-output organization of the motor cortex and its alterations during sleep and waking. In: Basic sleep mechanisms (ed. by Petre-Quadens, O. and Schlag, J.), pp. 144–200. New York: Academic Press, 1974.Google Scholar
Steriade, M., Diallo, A., Oakson, G., and White-Guay, B.Some synaptic inputs and telencephalic projection of lateralis posterior thalamic nucleus. Brain Research. 131:39–53. 1977.CrossRefGoogle Scholar
Steriade, M., and Hobson, J. A. Neuronal activity during the sleep-waking cycle. In: Progress in Neurobiology (ed. by Kerkut, G. A. and Phillis, J. W.), vol. 6, pp. 155–376. Oxford and New York: Pergamon Press, 1976.Google Scholar
Steriade, M., Iosif, G., and Apostol, V.Responsiveness of thalamic and cortical motor relays during arousal and various stages of sleep. Journal of Neurophysiology. 32:251–65. 1969.CrossRefGoogle ScholarPubMed
Steriade, M., Kitsikis, A., and Oakson, G.Thalamic inputs and subcortical targets of cortical neurons in areas 5 and 7 of cat. Experimental Neurology. 60:420–42. 1978.CrossRefGoogle ScholarPubMed
Steriade, M., Oakson, G., and Diallo, A.Reticular influences on lateralis posterior thalamic neurons. Brain Research. 131:55–71. 1977.CrossRefGoogle ScholarPubMed
Steriade, M., Oakson, G., and Kitsikis, A.Firing rates and patterns of output and non-output cells in cortical areas 5 and 7 of cat during the sleep-waking cycle. Experimental Neurology. 60:443–68. 1978.CrossRefGoogle Scholar
Steriade, M., and Wyzinski, P.Cortically elicited activities in thalamic reticularis neurons. Brain Research. 42:514–20. 1972.CrossRefGoogle ScholarPubMed
Steriade, M., and Apostol, V. Corticofugal projections governing rhythmic thalamic activity. In: Corticothalamic projections and sensorimotor activities (ed. by Frigyesi, T., Rinvik, E., and Yahr, M.), pp. 221–72. New York: Raven Press, 1972.Google Scholar
Steriade, M.Differential synaptic reactivity of simple and complex pyramidal tract neurons at various levels of vigilance. Experimental Brain Research. 17:87–110. 1973.CrossRefGoogle ScholarPubMed
Steriade, M., Wyzinski, P., Deschênes, M., and Guérin, M.Disinhibition during waking in motor cortex neuronal chains in cat and monkey. Brain Research. 30:211–17. 1971.CrossRefGoogle Scholar
Steriade, M. and Yossif, G.Spike-and-wave afterdischarges in cortical somatosensory neurons of cat. Electroencephalography and Clinical Neurophysiology. 37:633–48. 1974.CrossRefGoogle ScholarPubMed
Steriade, M.Afferent and recurrent collateral influences on cortical somatosensory neurons. Experimental Neurology. 56:334–60. 1977.CrossRefGoogle ScholarPubMed
Sukhov, A. G.Cortical inhibitory neurons. Fiziologiceski Zhurnal SSSR. 54:270–75. 1968.Google ScholarPubMed
Szentágothai, J.The “module-concept” in cerebral cortex architecture. Brain Research. 95:475–96. 1975.CrossRefGoogle Scholar
Szerb, J. C.Cortical acetylcholine release and electroencephalographic arousal. Journal of Physiology (London). 192:329–43. 1967.CrossRefGoogle ScholarPubMed
Takahashi, K.Slow and fast groups of pyramidal tract cells and their respective membrane properties. Journal of Neurophysiology. 28:908–24. 1965.CrossRefGoogle ScholarPubMed
Terzuolo, C. A., and Araki, T.An analysis of intra- versus extracellular potential changes associated with activity of single spinal cord motoneurons. Annals ofthe New York Academy of Sciences. 94:547–58. 1961.CrossRefGoogle Scholar
Tömböl, T. Collateral axonal arborizations. In: Golgi Centennial Symposium (ed. by Santini, M.), pp. 133–41. New York: Raven Press, 1975.Google Scholar
Ward, A. A. Jr. The epileptic neuron: chronic foci in animals and man. In: Basic mechanisms in the epilepsies (ed. by Jasper, H. H., Ward, A. A. Jr., and Pope, A.), pp. 263–88. Boston: Little, Brown and Co., 1969.Google Scholar
Waszak, M.Effect of polarizing currents on potentials evoked in neurons of the ventral leaf of nucleus reticularis thalami by intralaminar stimulation. Exp. Neurol. 40:82–89. 1973.CrossRefGoogle ScholarPubMed
Willis, W. D.The case for the Renshaw cell. Brain Behavior and Evolution. 4:5–52. 1971.CrossRefGoogle ScholarPubMed
Willis, W. D. and Willis, J. C.Properties of interneurons in the ventral spinal cord. Archives Italiennes de Biologie. 104:354–86. 1966.Google Scholar
Woody, C. D., and Black-Cleworth, P.Differences in excitability of cortical neurons as a function of motor projection in conditioned cats. Journal of Neurophysiology. 36:1104–16. 1973.CrossRefGoogle ScholarPubMed
Wyler, A. R.Epileptic neurons during sleep and wakefulness. Experimental Neurology. 42:593–608. 1974.CrossRefGoogle ScholarPubMed
Wyler, A. R. and Fetz, E. E.Behavioral control of firing patterns of normal and abnormal neurons in chronic epileptic cortex. Experimental Neurology. 42:448–64. 1974.CrossRefGoogle ScholarPubMed
Wyler, A. R., and Ward, A. A. Jr.Firing patterns of epileptic and normal neurons in the chronic alumina focus in undrugged monkeys during different behavioral states. Brain Research. 98:1–20. 1975.CrossRefGoogle ScholarPubMed