Neurophysiology of the States of Sleep
Michel Jouvet
Physiological Reviews 47 (2) pp : 117-177 (1967)


Definitions and Abbreviations

State of Sleep Characterized by Slow Cortical Activity Slow Sleep

Behavioral aspect

Electrophysiological aspect

Structures and mechanisms responsible for slow sleep

State of Sleep Characterized by Fast Cortical Activity-Paradoxical Sleep

Behavioral aspects

Electrophysiological aspects

Structures and mechanisms responsible for paradoxical sleep

A synthesis of paradoxical sleep mechanisms

Relationship with oneiric activity in man

Phylogenesis of the States of Sleep

Ontogenesis of the States of Sleep

Relationship Between Slow Sleep and Paradoxical Sleep Unicity or Duality of Sleep Mechanisms

A Possible Monoaminergic Theory of Sleep

Figure 1

Figure 2


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2 Definitions and Abbreviations

The confused terminology of the states of sleep is indicative of today's increasing interest about the sleep mechanisms. Until we get a biochemical definition of the states of sleep, the terminology must be understood by physiologists, clinicians, zoologists, and even psychologists ! So we must compare the states of sleep at various ages (from newborn infants to old people), in different species (from bird to man), and in various expetimental preparations (normal or pontine animals). That is why we cannot use a terminology based only on the electroencephalogram (EEG). "Slow or synchronized sleep," a term in general use, does not apply to stage I (drowsiness) in man, nor to newborn animals whose EEG does not vary during the different states of vigilance, nor to decorticate animals. The same remark is true for "fast or desynchronized sleep." Calling it "paradoxical sleep" implies no mechanism but expresses the astonishment of the physiologist at the accumulation of EEG and behavioral phenomena diverging from the "orthodox" conception of sleep. If we assume the rhombencephalon is necessary and even sufficient for the occurrence of paradoxical sleep, the term "rhombencephalic sleep" is then justified. The use of "activated sleep" indicates the existence of activating mechanisms that are rather difficult to define. The terms of "light" and "deep sleep" do not apply to man.

The following list, certainly incomplete, gives the terminology used to classify the two states of sleep (in the animal).

1) Synonyms for sleep characterized by slow cortical activity in adult animals sleep (up to 1958); deep sleep (100); light sleep (90); slow wave sleep (SWS) (140); slow sleep, synchronized sleep (240); telencephalic sleep (239); neo-sleep (240); firsl sleep (311); first phase of sleep (380), ortho sleep (420); quiet sleep (in kittens) (86); sleep without jerks (in kittens) (423); non rapid eye movements (NREM) sleep (131).

2) Synonyms for sleep characterized by fast cortical activity and abolition of neck EMG activity in adult animals sonno profondo (161); Tiefen Schlaf (274); activated sleep (122); paradoxical sleep (or paradoxical phase) (254); rhombencephalic phase of sleep (RPS) or rhombencephalic sleep (239); desynchronized sleep (328); fast sleep; fast wave sleep (FWS) (140); deep sleep (90); archeo sleep (240); second sleep (311); second phase of sleep (380); para-sleep (420); oneiric sleep (188) postreaction EEG (in the rabbit) (394); hyperarousal (in the rabbit) (395); phenomene particulier du sommeil (in the rabbit) (150); restless sleep (in kittens) (86); sleep with jerks (in kittens) (423); sommeil sismique (425); rapid eye movemenbs (REM) deep (131).

Nevertheless, recent progress in histochemical methods has permitted us to map out serotonergic and catecholaminergic systems in the brain stem (114, 169). The possible role of these systems in sleep mechanisms is also discussed separately.

It is necessary to make a few remarks concerning methodology; the study of sleep mechanisms is one of the fields of neurophysiology in which methodological problems are of paramount importance. Indeed, there is no absolute behavioral or electroencephalographic criterion of sleep. The fact that the low-voltage fast cortical activity (arousal reaction) (332) and behavioral arousal often occur together has led to an interchangeable but deplorable use of these terms. The electroencephalogram (EEG) variations are often admitted in acute experimentation as a sufficient criterion of wakefulness. Yet in no case does the state of the corticogram allow us to presume whether an animal is asleep or awake. If acute experimentation is carried out on anesthetized animals, the irreversible character of narcosis at once causes us to disregard one of the fundamental criteria of physiological sleep, namely its immediate interruption under the influence of a strong stimulation. The use of animals under curare or of the encephale isole preparation is doubtless a step forward. Yet, the difficulty of obtaining suitable ventilation (1) or of maintaining correct blood pressure without adding drugs hardly allows us to achieve a stable humoral state of long duration. Many humoral factors then can hasten the appearance of slow cortical waves (fall of blood pressure, alkalosis, etc.), whose mechanisms are not necessarily the same as those of the slow waves of sleep. Besides, the behavioral reactions of an animal under curare or encephale isole are much decreased, apart from the intrinsic or extrinsic ocular effectors; and curare may have synchronizing influences, which Hodes (211) ascribed to the reduction in proprioceptive afferent impulses. This reduction in proprioceptive afferent streams would then account for the conspicuous propensity of the encephale isole preparation to a synchronized cortical record (208, 344). Further, the mere fact of the "contention" of an unanesthetized animal not under curare in a stereotaxic apparatus, even if we disregard any painful stimulation (447), involves EEG correlations of sleep (fast spindles, absence of slow waves and of paradoxical sleep) different from those obtained in conditions of complete freedom. The same fact has been noticed after injection of reserpine, which produces EEG synchronization if the injection has been made before surgical manipulations but an arousal record if the injection is made after surgery (411).

This is why only chronic experimentation combining all the present resources of polygraphy is the appropriate means of studying the states of sleep. But this also is beset by many difficulties. The first is technical; it is difficult to record various zones of the brain stem in the same animal at the same time, though new technioues (74, 216) now allow a wider exploration. In addition, the unit exploration and identification of recorded neurons meet important technical difficulties. Intracellular recording, which would be useful in chronic conditions, has not yet been achieved. A second difficulty is that natural sleep is a spontaneous phenomenon (for we are still unaware of most of its triggering mechanisms). Sleep does not always occur when the experimenter wishes it and often occurs when it is not wanted; since Pavlov's time (352) this appearance of sleep in many circumstances has been considered to be within the limits of "internal inhibition." This is particularly true in the cat, which sleeps spontaneously for some 60-70 % of the day. The use of continuous polygraphic recordings (24 hr/ day, 7 days/week) has permitted us to describe very stable circadian sleep patterns in laboratory cats (120, 414) (see Table 1). The high percentage of spontaneous sleep makes very difficult the interpretation of the eventual appearance of sleep during or after any electrical (or chemical) central or peripheral "hypnogenic" stimulation. Consequently results obtained with these methods are dealt with in a special section, since their value is more limited than are the results of experiments of localized section or destruction. Yet even these latter methods do not elude criticism. Is it possible to study the integral phenomenon of sleep with the methods of serial sections used by Sherrington in the course of his analysis of the postural tonus? In the case of total section of the brain stem, which part of the cat is to be studied-the upper or the lower part? (See the remarkable discussion in ref 374.) Can we assume that after a circumscribed nervous lesion of the brain stem early EEG phenomena are the most important, or, on the contrary, are the most important phenomena the responses observed after "recovery" -the suppression of a probable "diaschisis" or the appearance of a possible super sensitivity of denervation (93, 410)?

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