Elsevier

Progress in Neurobiology

Volume 62, Issue 4, 1 November 2000, Pages 379-406
Progress in Neurobiology

Why we sleep: the evolutionary pathway to the mammalian sleep

https://doi.org/10.1016/S0301-0082(00)00013-7Get rights and content

Abstract

The cause of sleep is a complex question, which needs first, a clear distinction amongst the different meanings of a causal relationship in the study of a given behavior, second, the requisites to be met by a suggested cause, and third, a precise definition of sleep to distinguish behavioral from polygraphic sleep. This review aims at clarifying the meaning of the question and at showing the phylogenetic origin of the mammalian and avian sleep. The phylogenetic appearance of sleep can be approached through a study of the evolution of the vertebrate brain. This began as an undifferentiated dorsal nerve, which was followed by the development of an anterior simplified brain and ended with the formation of the multilayered mammalian neocortex or the avian neostriate. The successive stages in the differentiation of the vertebrate brain produced, at least, two different waking types. The oldest one is the diurnal activity, bound to the light phase of the circadian cycle. Poikilotherms control the waking from the whole brainstem, where their main sensorymotor areas lie. Mammals developed the thalamocortical lines, which displaced the waking up to the cortex after acquiring homeothermy and nocturnal lifestyle. In order to avoid competence between duplicate systems, the early waking type, controlled from the brainstem, was suppressed, and by necessity was turned into inactivity, probably slow wave sleep. On the other hand, the nocturnal rest of poikilotherms most probably resulted in rapid eye movement sleep. The complex structure of the mammalian sleep should thus be considered an evolutionary remnant; the true acquisition of mammals is the cortical waking and not the sleep.

Section snippets

Introduction: the mystery of the sleep

For lay people, sleep provides with simple rest and recovery, but the magical world of dreams maintains, in the break point of a new century, a halo of mystery. For sleep researchers, and even for general scientists, the mystery increases: the brain does not rest, even in the deepest sleep. Two types of sleep have been recognized in mammals (Fig. 1), each one with many improbable features: the slow wave sleep (SWS), consisting in a general slowing of most bodily functions, and in a diminished

The causes of the sleep

The bizarre characteristics of the mammalian sleep, the discovery of two extremely different phases, the imperative need of sleep overwhelming the mere need of rest, raise the question on the causes of the sleep, a central issue in sleep research (Horne, 1988). Causal questions in behavior can be interpreted in several ways (Amlaner and Ball, 1994, Timbergen, 1963). A given behavior can appear as the result of some stimulus appearing either in the environment or in the internal medium, and in

The sleep as adaptation

A fundamental idea pervades every report proposing a physiological function for the sleep: its fundamental aim is a quest for adaptiveness. Every researcher interested in recognizing the function of the sleep should thus be an adaptationist at heart. If the sleep has any purpose at all, sleeping organisms should have an advantage in being sleepers in front of other hypothetical beings devoid of sleep. As animals do sleep, the trait should have been selected as better adapted than other eventual

Behavioral and polygraphic sleep

The search of the sleep causes presents additional problems due to the difficulty in finding a general definition of sleep. Many authors have contributed to develop a definition of sleep as a behavior. Almost 100 years ago, Pieron (1913) proposed three characteristics: (1) motor rest, (2) increased sensory thresholds and (3) easy reversibility. Flanigan (1973) added (4) stereotyped posture. Bruce Durie (1981) also included (5) specific rest sites and (6) circadian organization. This author also

Searching the evolutionary origin of sleep and waking

Sadly, sleep leaves no fossil record and the only way to understand its evolution will be of comprehensive nature, analyzing its manifestations in surviving forms. This has been attempted several times (Allyson and Van Twiver, 1970, Tauber, 1974, Monnier, 1980, Karmanova, 1982, Meddis, 1983, Hartse, 1994), but curiously, the evolution of waking has only been recently considered (Rial et al., 1993, Rial et al., 1997); the unity of the waking state in all vertebrates has been taken for granted.

Does the behavioral sleep in reptiles exist?

A number of reports have addressed the question of the activity states in reptiles. Most of these studies were made around the 70’s and almost all described the existence of a well organized behavioral sleep (Hunsaker and Lansing, 1962, Hermann et al., 1964, Tauber et al., 1966, Tauber et al., 1968, Vasilescu, 1970, Peyreton and Dusan-Peyreton, 1969, Karmanova and Churnosov, 1972, Flanigan, 1973, Flanigan, 1974, Flanigan et al., 1974a, Flanigan et al., 1974b, Hartse and Rechtschaffen, 1974,

The reptilian neurophysiology

If reptiles have a behavioral sleep more or less similar to the mammalian one, what can be said about its neurophysiological correlates? Trying to solve this question several studies have attempted to find slow EEG waves (or some alternative), spindles, and K-complexes to define SWS in reptiles. In the same way, the traits of REM in the form of rapid eye movements or low voltage and mixed frequency EEG, were looked for. The following sections summarize the main results.

The meaning of the differences in the mammalian and reptilian state indicators

Having described the most salient facts on the reptilian neurophysiology, one could try to compare their characteristics with those of mammals. This is shown in Table 1, where the neurophysiological characteristics of waking reptiles described up to now are compared with those of waking and SW sleeping mammals. Taking cortical activity, as shown by the EEG power profile, arousal reaction and evoked potentials, waking reptiles are opposite to waking mammals and practically equivalent to SW

How the mammalian waking and sleep appeared

Between late Triassic and the end of Cretaceous, reptiles were the dominant land vertebrates (Crompton et al., 1978). As the extant reptiles, they would only show two different behavioral states: activity during daytime and rest during night, constrained by the need of external heat sources. Only big animals, with high thermal inertia, would be able to maintain a relatively constant body temperature and night activity (Desmond, 1975). These exceptions aside, the night would be devoid of active

Why do we sleep?

The evolutionary path drawn in this way correlates well with the evolution of the vertebrate brain, with its hierarchical structure (Parmeggiani, 1982) (Fig. 9), and with the ontogeny of wakefulness and the two sleep states (Roffwarg et al., 1966). Nobody would consider the recapitulation law of Von Bauer and Haeckel as an absolute fact, because there is the possibility of a brand new feature, unrelated to phylogeny, appearing in the embryo of any species. However, it is striking how the law

The mammalian sleep as secondary adaptation

Indeed, additional environmental pressures may have subsequently modified the sleep in many ways. Evolutionary remnants can be reused for new purposes and several utilities might exist for the sleep in different animal species (Horne, 1988). Sleep may even turn to extremely reduced amounts when the predation or other environmental pressure turns the sleeping behavior lethal or semi lethal (Allison and Chichetti, 1976) or it can turn asymmetric in bizarre mammals having returned to life in the

Discussion

Three theories have been developed to explain the evolution of the sleep. First, Tauber et al., 1966, Tauber et al., 1968, Tauber et al., 1969, proposed that REM should be considered the primitive sleep. Their hypothesis will be called henceforth the “REM first” one. Almost simultaneously, the opposite hypothesis (“SWS first”) was proposed by Allison and Collaborators (Allyson and Goof, 1968, Allyson and Van Twiver, 1970, Allyson et al., 1972). This point of view received strength after the

Acknowledgements

This work has been in part supported by grants of the DGICYT, PS-93-0421 and FIS, 97/1032 from the Spanish Government.

References (174)

  • J.T. Corwin et al.

    Auditory brainstem response in five vertebrate classes

    Electroencephalogr. Clin. Neurophysiol

    (1982)
  • L. De Vera et al.

    Reptilian waking EEG: slow waves, spindles and evoked potentials

    Electroenceph. Clin. Neurophysiol

    (1994)
  • J.M. Del Corral et al.

    Stereotaxic atlas for the lizard Gallotia galloti

    Prog. Neurobiol

    (1990)
  • R. Drucker-Colin

    The function of sleep is to regulate the brain excitability in order to satisfy the requirements imposed by waking

    Behav. Brain Res

    (1995)
  • F. Garcı́a-Garcı́a et al.

    Endogenous and exogenous factors on sleep-wake cycle regulation

    Prog. Neurobiol

    (1999)
  • T. Gómez et al.

    A case report of spontaneous electrographic epilepsy in reptiles (Gallotia galloti)

    Comp. Biochem. Physiol

    (1990)
  • J.W. Hudson

    Torpidity in mammals

  • G.A. Marks et al.

    A functional role for REM sleep in brain maturation

    Behav. Brain Res

    (1995)
  • D. McGinty et al.

    Keeping cool: a hypothesis about the mechanisms and functions of slow wave sleep

    TINS

    (1990)
  • T. Allyson et al.

    Sleep in a primitive mammal, the spiny anteater

    Psichophysiol

    (1968)
  • T. Allyson et al.

    The evolution of sleep

    Nat. Hist

    (1970)
  • T. Allyson et al.

    Electrophysiological studies of the echidna Tachiglossus acculeatus

    Arch. Ital. Biol

    (1972)
  • T. Allison et al.

    Sleep in mammals: Ecological and constitutional correlates

    Science

    (1976)
  • F. Amizca et al.

    The K-complex: its slow (<1 Hz) rhythmicity and its relation to delta waves

    Neurology

    (1997)
  • F. Amizca et al.

    Spontaneous and artificial activation of neocortical seizures

    J. Neurophysiol

    (1999)
  • C.J. Amlaner et al.

    Avian sleep

  • J. Aschoff

    Survival value of diurnal rhythms

    Symp. Zool. Soc. London

    (1964)
  • J.J.M. Askenasy et al.

    Visual skill consolidation in the dreaming brain

  • F. Ayala Guerrero

    Sleep in a chelonian reptile (Kinosteron sp)

    Sleep Research

    (1985)
  • F. Ayala Guerrero et al.

    Sleep and wakefulness in the lizard Ctenosaura similis

    Estud. Med. Biol. Mex

    (1987)
  • L. Barthelémy et al.

    Etude lectroencphalographique de l’anguille (Anguilla anguilla L.)

    J. Physiol. (Paris)

    (1975)
  • Belekhova, M.G., Zagorulko, T.M., 1964. Correlations between background electrical activity, after-dicharge and EEG...
  • M.G. Belekhova

    Neurophysiology of the forebrain

  • R. Berger et al.

    Paradoxical sleep in the echidna

    Sleep Res

    (1995)
  • Bert, J., Godet, R., 1963. Raction d’eveil tlencphalique d’un Dipneuste. C.R. Societ de Biologie de l’ouest Africain,...
  • S.S. Bowersox et al.

    EEG spindle activity as a function of age: relationships to sleep continuity

    Brain Res

    (1985)
  • D.J. Bruce Durie

    Sleep in animals

  • T.H. Bullock et al.

    Accoustic evoked activity in the brain of sharks

    J. Comp. Physiol

    (1979)
  • W. Burr et al.

    Spontaneous brain activity in some species of amphybiams and a reptile

    Electroenceph. Clin. Neurophysiol

    (1973)
  • A.B. Butler et al.

    Comparative Vertebrate Neuroanatomy

    (1996)
  • G. Buzáski

    Hippocampal sharp waves: their origin and significance

    Brain Res

    (1986)
  • T.J. Cade

    Observations on torpidity in cautive chipmunks of the genus Eutamias

    Ecology

    (1973)
  • C.B.G. Campbell et al.

    The concept of homology and the evolution of the nervous system

    Brain. Behav. Evol

    (1970)
  • L.M. Carrascal et al.

    Thermal ecology and spatiotemporal distribution of the mediterranean lizard (Psammodromus algirus)

    Holartic Ecol

    (1989)
  • A.M. Castilla et al.

    Thermal biology, microhabitat selection and conservation of the insular lizard Podarcis hispanica atrata

    Oecologia

    (1991)
  • R. Conduit et al.

    Induction of visual imaginery during NREM sleep

    Sleep

    (1997)
  • A.W. Crompton et al.

    Evolution of homeothermy in mammals

    Nature

    (1978)
  • Darwin, C., 1859. On the origin of species by means of natural slection, or the preservation of favored races in the...
  • A.O.R. De Juan et al.

    Proyección telencefálica de estimulos sensoriales en batracios

    Acta Physiol. Latinoamer

    (1966)
  • L. De Vera et al.

    Effect of body temperature on the ventilatory responses in the lizard Gallota galloti

    Respir. Physiol

    (1986)
  • Cited by (75)

    • Mammalian NREM and REM sleep: Why, when and how

      2023, Neuroscience and Biobehavioral Reviews
    • Relationships between REM and NREM in the NREM-REM sleep cycle: a review on competing concepts

      2020, Sleep Medicine
      Citation Excerpt :

      However, the theory does not explain the alternation by itself, since even at thermoneutral ambient temperature, REM sleep is eventually ended. Perhaps thermosensitive REM sleep is an evolutionary remnant from ectotherm life (see Ref. [116]). Moreover, perhaps NREM and the cycling are ways to adapt this remnant to an endotherm world?

    • Sleep in the dog: comparative, behavioral and translational relevance

      2020, Current Opinion in Behavioral Sciences
      Citation Excerpt :

      Behavioral sleep is common in the animal kingdom, whereas polygraphically defined sleep is best characterized in mammals [1], including the dog (Table 1).

    • Sleep as spatiotemporal integration of biological processes that evolved to periodically reinforce neurodynamic and metabolic homeostasis: The 2m3d paradigm of sleep

      2016, Journal of the Neurological Sciences
      Citation Excerpt :

      In mammals, sleep is distinguished from wakefulness and different sleep stages are identified based on behavioral and electrophysiological criteria (Table 1). However, most non-mammalian species do not express the noninvasive electrophysiological correlates of mammalian sleep [4]. Intracranial EEG or multi-unit recording is informative but technically difficult to perform in laboratory animals without disturbing their normal sleep function.

    View all citing articles on Scopus
    View full text