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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III. State of sleep characterized by fast cortical activity paradoxical sleep

Since early times, hunters have noticed that during sleep their dogs showed sudden motor episodes (tail and lip movements, barking), and Lucretius [Denatura rerum. IV, 984-I004, quoted by Moruzzi (328)] long ago attributed these episodes to oneiric activity. Fontana (161), as far back as 1765, called "sonno profondo" this sleep with "convulsions." But 20 years were necessary, from the first electrical description, to integrate this state of sleep into neurophysiology. When EEG began to be applied to chronic experiments, Derbyshire et al. (130) reported fast cortical activity periods "as in the alert waking state," when sleep was less quiet "as judging by twitching of vibrissae." This observation was confirmed by Rheinberger and Jasper (371). At the same time, Klaue (274) described, at length, the two states of sleep in chronic cats and published the first EEG recording of the state of "Tiefen Schlaff" with fast cortical activity and low voltage. This work was unfortunately forgotten. In spite of short descriptions of cortical desynchronization [Hess et al. (204)] or of hippocampal theta thythm [Rimbaud et al. (373)] during sleep, we must recognize that until 1958 only the state of "slow sleep" was known and studied in the cat. It is to the credit of Dement and Kleitman (122, 126, 127), studying man and the cat, to have characterized definitely the periodical recurrence of activated sleep with rapid eye movements. This state of sleep was then interpreted as an intermediate phase beween slow sleep and arousal. Soon after the demonstration that this sleep was, in fact, "deeper" than slow sleep and could indeed be identified by a specific subcortical electrical activity (pontine spikes) and specific postural criteria (total atony) (252) led to the demonstration of its rhombencephalic origin and to the hypothesis that it was a different state of sleep (252, 254). Since then numerous observations were made about EEG and be havioral correlations (42, 217, 246, 277) (see bibliography in 240) of the state of sleep with fast cortical activity, whose paradoxical aspects gave it the name, among many others, of paradoxical sleep (254) (see footnote 2).

A. Behavioral Aspects

Somatic phenomena

Contrary to slow sleep, in which the behavioral criteria are imprecise, the onset and the end of paradoxical sleep (PS) may be fixed and assessed within a few seconds from mere behavioral criteria not only in intact cats but also in decorticate or chronic pontine preparations. Behavioral phenomena may be classified into two types tonic and phasic.

Atonia. The complete abolition of muscular tone of antigravity muscles and, above all, of neck muscles, is the most remarkable manifestation of the inhibition of muscular tone, typical of PS (254). Preceding or following, by a few seconds, the cortical desynchronization of PS, an electromyogram (EMG) silence accompanies the sudden fall of an animal's head. The end of PS is shown usually by a sudden recovery of a considerable EMG activity, whether the animal wakes or "falls" again into slow sleep. This very typical neck muscle atonia may be found alike in gamma (decerebrate animal preparations) (240) or in alpha (decerebrate animal preparations with removal of the anterior lobe of the cerebellum) type of spasticity (206). It is also observed after section of posterior roots from C1 to C7 (233,242)

Spinal refllexes. Accompanying this atonia, or even preceding it by a few seconds, a decrease or even a disappearance of heteronymous monosynaptic and plurisynaptic reflexes may be observed (171, 181-183, 284, 358, 420), whereas usually these do not vary much during slow sleep. The homonymous monosynaptic reflexes are not tonically inhibited during PS but only during the bursts of eye movements (358). Last, the posttetanic facilitation of monosynaptic reflex (obtained by stimulating the posterior roots) is abolished during PS but persists during slow sleep (25, 183).

Clonic movements. Among phasic phenomena typical of PS, eye movements are predominant and consequently are considered separately. They occur with cortical activation and their pattern is different from that of the eye movements of the waking state. However, they are not isolated and other phasic movements accompany (in a strange unpredictable manner) PS development sudden move ments of the ears, the vibrissae, the fingers (flexion) (see 172), the tail, and some times genuine clonic jerks of the back muscles. These phasic phenomena are especially developed in the kitten after birth (86, 236, 422, 423) and increase in a striking way after long PS deprivations (237, 429). The animal then seems to be animated with convulsions ["comincio a tremare tutto quasi fosse in qualche convulsione" (161)] .

Vegetative phenomena

These are constant in the cat and also express tonic and phasic changes in the vegetative sphere. A fall in blood pressure appears at PS onset (90, 170,261); it may be interrupted by short hypertensive phases during bursts of ocular movements. It is accompanied by a great irregularity in heart rate (bradycardia or tachycardia depending on the animal) (240), and it may also be observed when PS is induced by brain-stem stimulation (90). The falls in blood pressure are much larger after bilateral sinoaortic deafferentation; they fall to such low pres sure during PS that episodes of transient cerebral ischemia (EEG flattening and seizures) sometimes occur (189). But an artificial fall in blood pressure (caused by vagal stimulation) does not induce PS (90). The mechanisms of action of this fall in blood pressure are still unknown. The fall is not dependent on the muscular hypotonia since a blood pressure rise is often the first sign of the end of a PS episode, before the return of EMG activity (90, 170). Cerebral blood flow has been studied by methods using the shifts of cerebral temperature or of cerebral impedance (50, 260, 261). The most striking phenomenon is the large increase in blood flow that occurs during the generalized fall in blood pressure (260, 261).

Several hypotheses have attempted to explain this blood flow increase action of a cerebral vasodilatation or an increase in cerebral metabolism expressing itself by an augmentation of CO2, which is a well-known cerebral vasodilatator (260). An increased cerebral temperature at the onset of the fast cortical EEG of PS has also been reported (266, 367). Respiratory variations are also noticeable; most of the time, they consist of an irregularity and increase in the rhythm, whereas it is usual to observe an apnea at the end of PS (240).

The galvanic skin reflex (GSR), either spontaneous or induced by stimulating the peroneal nerve, has also been studied during PS (420). Most of the time (70 % of the cases), there is a notable decrease of both spontaneous and induced GSR during PS in comparison with slow sleep. Sometimes spontaneous GSR may appear in bursts during PS; interestingly enough, these bursts are not concomitant with the rapid eye movements.

Arousal threshold

If we trust the following criteria, PS appears as a deeper state of sleep than slow sleep; behavioral arousal threshold by reticular stimulation is much increased (up to 300%) in comparison with slow sleep (42, 90, 217, 254). This arousal threshold increase may also be observed in decorticate animals (240), which eliminates the hypothesis of a possible inhibitory corticoreticular feedback (221). The arousal threshold by auditory stimulation increases too, either slightly or sometimes greatly (96, 150, 240), and above all some stimulations, unable to induce behavioral arousal, involve the reappearance of slow sleep (217,240).

Other behavioral (muscular atonia) and vegetative (blood pressure fall) criteria also support the idea of a deeper level of sleep during PS. That is why this state of sleep is sometimes called "deep sleep" (90), opposed to "light sleep" (slow sleep). As a matter of fact, the concept of depth or "heaviness" of sleep is ambiguous and essentially depends on the criteria used. The possibility that some learning could occur during sleep (with conditioning methods) has been extensively studied (79, 80). Thus it appears that some classical conditioning is still possible during slow sleep whereas it is almost absent during PS. On the other hand, judging by the phasic movements of the eyes or of the legs, PS rather appears as a "restless, less quiet" sleep (130). It is not certain either that the increase in "depth" of PS in comparison with slow sleep is constant in all animal species (55), or even that the arousal threshold remains constant during PS in the cat (in correlation with blood pressure shifts) (90). Moreover, PS and slow sleep increasingly appear to be two qualitatively different states, and hence it is perhaps rather illusive to compare them from the quantitative ambiguous point of view o f "depth" or "lightness."

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