Paradoxical Sleep - A Study of its Nature and Mechanisms
Michel Jouvet
Progress In Brain Research Vol. 18 Sleep Mechanisms 1965
Evidence of the duality of the states of sleep

(a) EEG and behavioural findings

(b) Phylogenetic findings

(c) Ontogenetic findings

(d) Functional findings

(e) Structural findings

Mechanisms of paradoxical sleep

(a) Producing P.S. as a reflex

(b) Results of deafferentations

(c) Role of the hypothalamus and pituitary

(d) Deprivation of P.S. in the pontile animal

(e) Effects of temperature on P.S. in the pontile animal

(f) Action of gamma-butyrolactone (G.B.L.)

(g) Osmolarity of the blood and paradoxical sleep


(a) Duality of the states of sleep

(b) Mechanisms underlying the appearance of P.S.

Summary and Conclusions



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TISSOT : One form of sleep or several? The discussion brings to mind the classic quarrel between the neoticians and the associationists. The problem must be put differently. Although there are different structures, mechanisms and functions, often even opposed to one another, normal sleep has the characteristic quality of integrating them into a harmonious activity.

JOUVET: I agree with you, but if I adopt this way of trying to show the duality of the states of sleep it is because there is often a tendency to consider sleep as a single state with only quantitative changes - light or deep sleep. I think these terms are very misleading because they might give the impression that paradoxical sleep is only due to an intensification of the hypnic process whereas the occurrence of something else is in fact involved.

SOULAIRAC : The phylogenetic study of sleep ought to provide information about the physiological significance of the two types of sleep. The fact that only the higher vertebrates (mammals and to a very slight extent birds) manifest paradoxical sleep prompts the question whether it is not connected with the presence of the neocortical system.

One might suggest that just as development of the neocortex involves the appearance of a second vigilance system, superimposed on the fundamental mesencephalic system, paradoxical sleep would in the same way represent the manifestation of a second system of sleep regulation. This would then represent not a true duality but the coordination on the phylogenic plane of two chronologically different mechanisms controlling the unitary biological function of sleep in the higher vertebrates.

JOUVET : It would nevertheless seem that the cortex is not necessary for the occurrence of paradoxical sleep since the latter persists in decorticated or pontile animals. We also found to our surprise that, contrary to the classic theory, ontogenetic development does not simply repeat on a smaller scale the pattern of phylogeny since paradoxical sleep is particularly developed at birth, in both the kitten and the newborn human infant, whereas it is practically absent in birds. In this sense paradoxical sleep does not appear to be archisleop as we first thought.

HERNANDEZ-PEON : I share Prof. Hess' opinion supporting a unitary concept of sleep. Sleop and wakefulness are physiological states subserved by the dominance of antagonistic neural systems which must have a complex but integrated organization. I also agree with Prof. Jouvet that the region of the nucleus reticularis pontis caudalis plays an important role in the muscular hypotonia of the desynchronized phase of sleep. However, there is no need to postulate two different independent neural systems in order to explain the two groups of epiphenomena of sleep. Their habitual chronological relationship can be easily explained by different degrees of activation within a single sleep system which produces different degrees and extents of inhibition within the vigilance system.

JOUVET : I am afraid I do not agree with you at all. The fact that first slow then paradoxical sleep can be produced by injecting acetylcholine in situ is no proof that the same mechanism is responsible for both. Paradoxical sleep occurs spontaneously during slow sleep and it would be very naïve to imagine that it had been specifically produced when it occurs more than a minute after an injection. (The same applies, by the way, to slow sleep.) On the contrary we have demonstrated that slow sleep was not necessary for the occurrence of the paradoxical phase (ontogenesis, deprivation, pontile animals).

TISSOT : Dementia in advanced age has been shown to produce a longer duration of paradoxical sleep (as in the child) than that of the adult. This is another argument in favour of Jouvet's concept of archisleep.

JOUVET : I do not think we should generalize yet on the data concerning insanity. We have made tracings of psychotic subjects with Korsakoff's syndrome and have been surprised to see a significant decrease of paradoxical sleep in them.

MORUZZI : Prof. Jouvet has just given us new and very important facts on the phylogenic and ontogenic aspects of desynchronized or paradoxical sleep. I should like to ask his opinion of the relationship of classic or synchronized sleep to these bursts of desynchronized sleep which are of fairly short duration and characterized by essentially phasic phenomena.

What is the reason for the sudden disappearance of a phase of desynchronized sleep? An answer to this question might help us understand the functional significance of the phenomenon. Are we dealing with something new, which only interrupts synchronized sleep but which is not related to it and which disappears immediately and spontaneously, as any convulsive or subconvulsive manifestation? Or does synchronized sleep inevitably lead to paradoxical sleep and suppress it again as soon as it can deal with the situation?

It would be interesting to try to prolong the phases of paradoxical sleep in cases where it is very short, such as in the pigeon. A study of the postural and ocular effects in the thalamic pigeon would provide an answer to this question.

JOUVET : I think we are not yet in a position to solve this important problem. There seems to be no connection between the duration of slow sleep and that of the paradoxical sleep that follows. On the other hand, in about 70% of cases paradoxical sleep terminates in waking, however brief, and not in a return to slow sleep. We must regard paradoxical sleep as a self-regulated process of metabolic or enzymatic nature. Even after very long deprivation (22 days), such as we have recently carried out, the mean duration of recuperative paradoxical sleep falls to 6 min after 24 h. On the other hand, the intervals between each phase are shortened for some 12 days.

We have the impression that if paradoxical sleep represents either the synthesis or the elimination (or both) of some substance, this synthesis can only take place according to a process comprising a mechanism for its own autoregulation. The only way to increase the duration of paradoxical sleep (in the pontile animal) is hypothermia followed by rewarming.

It would of course be interesting to study thalamic pigeons, but I am afraid the phases of paradoxical sleep in birds are very short indeed.

KUGLER : Jouvet has demonstrated that in the case of the cat, the EEG patterns of certain phases of sleep accompanied by muscular atony are difficult to distinguish from the waking EEG. Hence he has coined the term 'paradoxical sleep' for these phases. In man, sleep accompanied by muscular atony and eye movements produces lowvoltage, fast EEG patterns instead of the high-amplitude slow activity of classic sleep. But they are not identical with the waking rhythm in humans. The frequencies are generally slower than those of the normal a-rhythm and present superimposed flat theta-waves. The patterns can more easily be compared with those of stage B of classic sleep. When alpha-like activity occurs it has a different topographical distribution and a different reactivity from the occipItal. alpha-rhythm. A characteristic of these phases, moreover, is the moment of occurrence: they occur only after classic sleep phases and not immediately after waking periods.

MINKOWSKI : I am wondering whether paradoxical sleep, accompanied by eve movements beneath closed eye-lids, as described so admirably by Prof. Jouvet, does not represent a recurrence - mutatis mutandis, of course - of the fetal form of sleep in the adult. Eye movements are very probably produced in the fetus long before the palpebral slits are formed, either as movements accompanying the first fetal head movements or as movements of proprioceptive origin in the strict sense of the word, i.e. produced by proprioceptive stimulation in the eyebal]s. From the anatomical aspect there is good reason to stress that the posterior longitudinal bundle in the protuberantial and mesencephalic tegmentum, one part of which unites and coordinates the oculomotor nuclei, is one of the formations that undergo myelinization earliest in the fetus - in the 4th month of intrauterine development - and that part of the fibres of the reticular formation and the nuclei and intracerebral parts of the oculomotor nerves undergo the same process shortly after. These formations thus constitute an anatomical fetal substrate for early eye movements which occur well before their postnatal reactions to visual stimulation.

As a result of my research into the successive development of nervous function in the early stages of the fetus, the newborn, the infant, the child and the adult, I formed the idea that each different phase of development does not completely disappear when the next one begins but continues to exist, at least potentially, at deep functional levels, and to interact according to the circumstances with the superimposed more highly differentiated adult components. It would be extremely interesting if this sleep could be demonstrated as manifesting the coexistence of elements of different genetic levels, the paradoxical phase of sleep appearing as a relic of fetal sleep in the general and complex sleep of the animal and adult human.

JOUVET : I fully agree with this interpretation. I think that experiments on apes will soon have reached the stage where we can study fetal sleep. The only facts we have so far refer to birds. Klein in my laboratory studied the chick embryo (from the 17th to the 20th day of incubation) and noted periods of rapid eye movements accompanied by bradycardia, but the cerebral electrical activity did not vary and no muscular activity could be recorded. These embryonic states possibly represent something connected with paradoxical sleep.

MONNIER : What differences in autonomic function have you observed during the two phases of sleep? How do the pupils react during paradoxical sleep?

JOUVET : The pupil is generally in a state of extreme miosis during paradoxical sleep (more contracted than during slow sleep). But short periods of mydriasis often accompany the sudden eye movements and even persist after cervical sympathectomy.

KONZETT : What is the effect of minimum doses of hypnotic substances on paradoxical sleep?

JOUVET : This question is very interesting. We have particularly studied the action of 'Nembutal'. This drug, even in anesthetic doses (30-35 mg/kg body weight), does not appear to suppress the occurrence of the paradoxical phase during anesthesia. Paradoxical sleep is certainly much more difficult to recognize than in the normal animal, but if the monophasic peaks in the pons or the lateral geniculate are taken as a criterion they will be seen to persist for regular periods of about 6 min during anesthesia and that their incidence is increased after selective deprivation. The process responsible for paradoxical sleep seems to be particularly active since it is not uppressed by anesthetic doses of 'Nembutal'.

PLETSCHER : What is the physiological significance of paradoxical sleep ?

JOUVET : I wish I could answer your question! This is certainly one of the most fascinating problems of the physiology of sleep. It would seem that paradoxical sleep may represent the expression of a 'dreaming function' and that it might possibly also have some connection with the phenomena of memory formation. A very speculative hypothesis would be that paradoxical sleep might represent the molecular synthesis of the proteins responsible for memory storage. This would explain the particular importance of paradoxical sleep at an early age when the learning processes are very much to the fore. We have equally been struck, as I mentioned just now, by the decrease of paradoxical sleep in subjects suffering from Korsakoff's syndrome (unpublished observations). However, I must confess that such observations are much too limited to enable us to establish a connection between paradoxical sleep and memory.

ARNOLD : Phylogenetically, sleep is a very old behavioural pattern. For this reason we are justified in discussing briefly the phenomenon of human sleep from the phylogenetic point of view. An important fact is that the development of man has been characterized by two absolutely opposed sleeping patterns. The earlier stage of phylogenetic development is represented by vegetarian tree-dwellers who also slept in trees. For this purpose the extremities must be kept in a cramped position (clinging function), which is only possible through a more or less upright position of the body produced by the corresponding tonus systems of the brain stem and spinal cord. In this sleeping position the distance between each member of the group is larger and the mutual protection smaller; defence or flight in the event of attack is only possible when signals (e.g. noise or vibration), perceived in spite of sleep, lead to immediate defence reactions.

At a later period, during the transition to prairie dwellers, quite different sleeping positions emerged with the development of a hunting community. While some kept watch the others huddled close together and lay in positions where the exposed surface of the body was reduced to a minimum as protection against loss of warmth and getting wet (fetal position). This demanded complete relaxation of the whole muscular apparatus, a horizontal position and a corresponding functional modification in postural reflexes.

These two phylogenically pre-formed and contrasting sleeping positions are still the extremes of a range of behavioural possibilities. Between these two extremes is a middle zone, which we might call the intermediary position. This perhaps includes paradoxical sleep with its numerous levels of activity expressed as frequent change of positions, muscular twitching and even sudden starts, attentive listening, getting up and sleep-walking.

It appears necessary not only to consider the complex pattern of sleep in man from the aspect of organization and fonction of neurophysiological substrates and their elements but also to bear in mind that the overall and detailed function of these elements is subordinate to the very old pattern of sleep and has wndergone the same phylogenic modifications.

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