THEORETICAL REVIEWThe trivial function of sleep☆
Introduction
In 1971, Rechtschaffen1 stated that ‘if sleep does not serve an absolute vital function, then it is the biggest mistake the evolutionary process ever made’. Thirty-five years later, this statement remains unchallenged despite the lack of convincing evidence.
The most compelling arguments supporting the vital function of sleep are (1) the experiments of long-term total sleep deprivation (TSD), resulting in the death of experimental animals2; (2) the deleterious results of short-term sleep deprivation (SD) in cognitive functions; (3) the complexity of sleep, which most probably determined Rechtschaffen's assertion; (4) the supposed adaptiveness of many sleep signs; and (5) the existence of sleep regulation. In this review, we cast doubts on the demonstrative value of these five arguments.
In this review, the state of low activity observed in poikilothermic animals will be called ‘rest’. Rest is an essential part of the activity–rest cycle of cold-blooded animals, and it has a well-acknowledged adaptive value.3 The term ‘sleep’ will be reserved for mammals and birds. Sleep is also part of the activity–rest cycle, and shares a number of common features with the poikilotherms rest state. Therefore, rest and sleep should provide the organism with a similar primary function, and this is what we call the ‘trivial function’ of sleep. However, mammal and bird sleep shows a number of additional traits (e.g. two phases, changes in the activity of discrete central nervous system regions, in the regulation of physiological functions, in psychological efficiency). Therefore, the search for the function of sleep should be restricted to the differential traits of sleep. In other words, sleep should have two functional aspects: first, a (trivial) function common with rest; and second, a specific function related to the differential signs that are exclusive to sleep.
In addition to sleep, we will also review wakefulness. The adaptive value of rest might be understood only if the whole rest–activity cycle is taken into account. Similarly, the value of sleep is inseparably linked to that of waking. However, the use of the same word (waking) to describe the active part of the cycle of poikilotherms and homeotherms could be misleading because it implies homology between the waking of the two groups. However, the neuroanatomical control of wakefulness has suffered important changes in the evolution from poikilotherms to homeotherms. In functional terms, these changes have allowed the development of conscience, a function that is most probably impossible for a brain without a cortex. But no clear functional advance has yet been demonstrated in the transition from rest to sleep. In this situation, the principle of parsimony should favour hypotheses supporting the absence of any functional difference between rest and sleep, whereas the burden of the proof should be charged to the defender of additional functions.
Section snippets
Stress and sleep deprivation
Doubts about the specificity of the consequences of long-term TSD are not new, and some authors have suggested that TSD is simply a form of Selye's syndrome of adaptation.4 However, Selye's syndrome is not the only condition causing lesions and death after exposition to unspecific stress. Here, attention will be devoted to theoretical considerations negating the usefulness of SD to provide evidence for the function of sleep. In addition, learned helplessness (LH) and multi-organ failure
Sleep and food deprivation (FD): similarities and differences
The use of sleep-deprived animals to study the function of sleep comes from the widely accepted homeostatic regulation of sleep.5 Accordingly, SD should be similar to the deprivation of other regulated needs (i.e. adequate food supply).
However, eating is an active behaviour and, within certain limits, hunger stress also enhances the activity of the animal, which increases the probability of discovering a suitable food source by means of a larger exploratory drive.6 Therefore, food ingestion and
Learned helplessness and long-term sleep deprivation
LH was first defined by Seligman.8 A typical LH experiment involves two animal groups. The control group receives escapable punishment (e.g. they can escape from a foot-shock by jumping to a safe compartment of the cage). The second group, ‘helpless’, receives exactly the same amount of punishment, but they cannot escape. Control animals readily learn to escape, whereas the helpless animals learn that there is no way to escape from the punishment, so that later, when offered the possibility,
Multi-organ failure syndrome and total sleep deprivation
MOFS, first described in 1975 by Baue,16 is well known in intensive-care units. Occasionally, after the recovery of an initial insult (e.g. major surgery, traumatic lesions, extensive burning), a rapid perturbation develops with a sequential or simultaneous implication of different organs and systems. Respiratory failure is the most frequent result, followed by a cascading failure of kidney, liver, cardiovascular, coagulation, central nervous system, and so on. Sepsis is considered the first
Short-term sleep deprivation
Perhaps, the most important difference between TSD and short-term SD lies in the absence of deleterious physiological imbalances in short-term SD. However, important cognitive deficits have been observed after short-term SD even in humans in whom no LH should occur. However, this does not mean a complete absence of stress. Quite the opposite, the prolongation of waking is always stressful, as everybody would attest. In consequence, the cognitive effects of short-term SD are also suspicious of
Is sleep always necessary? The evidence of sleep deprivation without stress
Long-term REM sleep suppression may be easily achieved by pharmacological procedures,37 and thousands of people taking antidepressant medication are currently living with almost no REM sleep. Also, the absence of negative effects has been reported in the case of almost total REM sleep suppression resulting from brain lesions.38 However, most surprisingly, TRD without adverse effects has been obtained in rats39 by substituting REM sleep by waking periods of a similar average length.
Interim summary 1: the existence of specific effects after sleep deprivation is disputable
The experiments of FD and SD cannot be compared. Pure FD causes no behavioural conflict, whereas these are unavoidable in SD. Therefore, the theoretical foundation of TSD is probably wrong and the results suspicious.
The results of unspecific stress are extremely variable. There is no reason to expect the same lesion or cognitive deficit after the application of different chronic and acute stressors. Thus, the existence of minute differences do not prove the absence of a general common mechanism.
The absence of adaptation is the null hypothesis
Williams49 observed in 1965 that adaptation is an onerous concept that should not be called in absence of positive proof. The lack of adaptation is parsimonious, and should be always considered as the null hypothesis in absence of definite counterproof, without need of demonstration.
The non-coding, deoxyribonucleic acid (DNA) as a metaphor for the non-adaptive value of sleep
The belief in the adaptive value of sleep is probably sustained by the so-called argument of complexity,50 also used, for instance, in the belief of the adaptive value of the eye: such a complex organ would require
Homeostatic regulation in poikilotherms
The homeostatic and circadian regulation of rest and activity seems to be opposite in poikilotherms, as homeostasis could determine rest during the inconvenient part of the geophysical cycle.66 In spite of this, it has been found that rest and sensory thresholds are increased after forced activity in both poikilotherm vertebrates and invertebrates.67 Therefore (1) the rest of poikilotherms could be independent of circadian cycles; (2) the homeostatic regulation observed in these animals could
The difference between non-rapid eye movement sleep and rapid eye movement sleep
Although the complexity provided by the existence of two phases and their variable amounts has already been discussed, their mere existence constitutes a challenge for any hypothesis trying to explain the function of sleep. This is the purpose of the following lines.
Evolution proceeds along two paths. A given structure could diverge to allow different functions in different species. This is the case of the mammalian limb, which allowed terrestrial animals to walk while evolving to support
Interim summary 2: most traits currently attributed to sleep could have no real significance
The most important traits of sleep/rest are the ability to choose a suitable resting site, the switching off of motor activity and sensitivity to irrelevant sensory inputs.
Waking has higher precedence in adaptation than sleep, which could be no more than rest. Most supposed sleep traits are likely to be waking traits instead.
No firm demonstration of rest regulation in poikilotherms has been reported. Instead, careful regulation exists for the amount of activity. The homeostatic regulation of
Conclusion: sleep is a junkyard in the evolution towards cortical conscience
Mammalian sleep has no function apart from the rest of simple organisms; this most likely represents its ‘absolute vital function’, as Webb91 and Meddis92 proposed many years ago. So, the problem of why we sleep only lies in explaining the complexity of the polygraphic sleep of homeotherms in front of the mere rest of simpler animals. Undoubtedly, sleep began as behavioural arrest; however, its essential function did not change when it acquired a number of bizarre traits. And so it remains, far
Acknowledgements
This work has been performed thanks to a grant from the Ministerio de Ciencia y Tecnología of the Spanish Government Number BFI2002-04583-C02-02.
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Authors contribution: M.C. Nicolau, A. Gamundi, M. Akaârir, S. Aparicio, C.Garau, S. Tejada, C. Roca, L. Gené and D. Moranta equally contributed to this report. R.V. Rial and S. Esteban led the redaction of the report.
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The most important references are denoted by an asterisk.