Recent studies of sleep that bring closer the development of a cognitive neuroscience of conscious states are reviewed to reveal a unique integration of mechanistic and functional concepts.
The electrophysiology of non-rapid eye movement (NREM) sleep has been detailed to reveal the effects of brainstem reticular and neuromodulatory deactivation of the thalamocortical system. But instead of viewing these changes simply as inactivation, it has been suggested that the slow waves and spindles of NREM might reflect a differential mode of information processing by the brain in sleep. In particular, these findings are compatible with a two-stage hypothesis of sleep enhancement of plasticity — a model that is also supported by studies of human cognitive enhancement in sleep.
The transformational role of two methodological innovations is emphasized. Home-based studies of sleep allow investigators to obtain vast amounts of data about the kind of consciousness that is associated with active waking, quiet waking, sleep onset, NREM and REM sleep. At the same time, positron emission tomography (PET) imaging is used to reveal the relative blood flow in different regions of the human brain in waking, NREM and REM sleep.
The data from these two sources are complementary and informative. For example, in REM sleep (compared with waking) there is more blood flow directed towards the brain stem, the limbic forebrain and the parietal operculum; these findings map onto the marked increase in hallucinatory experience during REM. By contrast, the low levels of thinking during REM map onto the decrease in dorsolateral prefrontal cortical blood flow in that state.
The relevance of these findings to the brain-based activation–synthesis theory of dreaming is stressed by a systematic review of the differential increases in activation of forebrain structures revealed by PET imaging in: ascending arousal systems; thalamocortical and thalamic subcortical structures; limbic and paralimbic structures; motor initiation and control areas; visual association cortex; and the inferior parietal lobe.
Plasticity is now thought to be a major functional process that is generated by sleep. This idea is supported by recent developmental and human memory studies. The human cognitive studies reveal enhancement of learning by both NREM and REM sleep, indicating a two-stage process.
Such a model shares assumptions and structures with Buzsáki's electrophysiological model of a hippocampal-neocortical dialogue. Buzsáki posits a transfer of data from neocortex to hippocampus in active waking, and consolidation of information within the hippocampus along with its transfer back to the neocortex for longer-term storage during quiet waking and NREM. Recent experimental and theoretical work further indicates that intracortical processing occurs during REM, at which time new associative connections might be formed within the neocortex.
Sleep can be addressed across the entire hierarchy of biological organization. We discuss neuronal-network and regional forebrain activity during sleep, and its consequences for consciousness and cognition. Complex interactions in thalamocortical circuits maintain the electroencephalographic oscillations of non-rapid eye movement (NREM) sleep. Functional neuroimaging affords views of the human brain in both NREM and REM sleep, and has informed new concepts of the neural basis of dreaming during REM sleep — a state that is characterized by illogic, hallucinosis and emotionality compared with waking. Replay of waking neuronal activity during sleep in the rodent hippocampus and in functional images of human brains indicates possible roles for sleep in neuroplasticity. Different forms and stages of learning and memory might benefit from different stages of sleep and be subserved by different forebrain regions.
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Pace-Schott, E. F. & Hobson, J. A. The neurobiology of sleep: genetics, cellular physiology and subcortical networks. Nature Rev. Neurosci. 3, 591–605 (2002).
Hobson, J. A. & McCarley, R. W. The brain as a dream-state generator: an activation–synthesis hypothesis of the dream process. Am. J. Psychiatry 134, 1335–1348 (1977).
Hobson, J. A., Pace-Schott, E. F. & Stickgold, R. Dreaming and the brain: toward a cognitive neuroscience of conscious states. Behav. Brain Sci. 23, 793–842 (2000).
Steriade, M. Active neocortical processes during quiescent sleep. Arch. Ital. Biol. 139, 37–51 (2001).
Borbély, A. A. From slow waves to sleep homeostasis: new perspectives. Arch. Ital. Biol. 139, 53–61 (2001).
Nielsen, T. A. A review of mentation in REM and NREM sleep: 'covert' REM sleep as a possibile reconciliation of two opposing models. Behav. Brain Sci. 23, 851–866 (2000).
Buzsáki, G. The hippocampo–neocortical dialogue. Cereb. Cortex 6, 81–92 (1996).An important and influential theory on state-dependent memory consolidation at the level of the input and output circuits of the hippocampus.
Peigneux, P., Laureys, S., Delbeuck, X. & Maquet, P. Sleeping brain, learning brain. The role of sleep for memory systems. Neuroreport 12, A111–A124 (2001).An important review supporting the theory of sleep-dependent consolidation of neuroplastic changes initiated in waking (see also reference 10).
Stickgold, R. Sleep: off-line memory reprocessing. Trends Cogn. Sci. 2, 484–492 (1998).
Stickgold, R., Hobson, J. A., Fosse, R. & Fosse, M. Sleep, learning and dreams: off-line memory reprocessing. Science 294, 1052–1057 (2001).
Maquet, P. Functional neuroimaging of normal human sleep by positron emission tomography. J. Sleep Res. 9, 207–231 (2000).
Laureys, S. et al. Experience-dependent changes in cerebral functional connectivity during human rapid eye movement sleep. Neuroscience 105, 521–525 (2001).
Maquet, P. The role of sleep in learning and memory. Science 294, 1048–1052 (2001).
Steriade, M. Coherent oscillations and short-term plasticity in corticothalamic networks. Trends Neurosci. 22, 337–345 (1999).
Steriade, M. Corticothalamic resonance, states of vigilance and mentation. Neuroscience 101, 243–276 (2000).
Moruzzi, G. & Magoun, H. W. Brainstem reticular formation and activation of the EEG. Electroencephalogr. Clin. Neurophysiol. 1, 455–473 (1949).
Saper, C. B., Chou, T. C. & Scammell, T. E. The sleep switch: hypothalamic control of sleep and wakefulness. Trends Neurosci. 24, 726–731 (2001).
Rowley, J., Stickgold, R. A. & Hobson. J. A. Eye movement and mental activity at sleep onset. Conscious. Cogn. 7, 67–84 (1998).
Achermann, P. & Borbély, A. A. Low frequency (<1 Hz) oscillations in the human sleep electroencephalogram. Neuroscience 81, 213–222 (1997).A demonstration in the human sleep scalp EEG of the slow oscillation of NREM, an important EEG sign of NREM that was recently identified in depth recordings of the cat by Steriade's group
Simon, N. R., Lopes da Silva, F. H. & Manshanden, I. in Recent Advances in Biomagnetism (ed. Yoshimoto, T.) 373–376 (Tohoku Univ. Press, Tohoku, 1999).
Steriade, M., Nunez, A. & Amzica, F. Intracellular analysis of relations between the slow (<1 Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram. J. Neurosci. 13, 3266–3283 (1993).
Borbély, A. A. & Achermann, P. in Principles and Practice of Sleep Medicine (eds Kryger, M. H., Roth, T. & Dement, W. C.) 337–390 (W. B. Saunders, Philadelphia, Pennsylvania, 2000).
Lisman, J. E. Relating hippocampal circuitry to function: recall of memory sequences by reciptocal dentate–CA3 interactions. Neuron 22, 233–242 (1999).
Rioult-Pedotti, M.-S., Friedman, D. & Donoghue, J. P. Learning-induced LTP in neocortex. Science 290, 533–536 (2000).
Shaffery, J. P., Sinton, C. M., Bissette, G., Roffwarg, H. P. & Marks, G. A. Rapid eye movement sleep deprivation modifies expression of long-term potentiation in visual cortex of immature rats. Neuroscience 110, 431–443 (2002).An important new study showing that the endogenous stimulation of REM sleep might interact with early developmental plasticity of the visual cortex in a manner analogous to external visual input during waking.
Steriade, M. The Intact and Sliced Brain (MIT Press, Cambridge, Massachusetts, 2001).
Borbély, A. A. A two-process model of sleep regulation. Hum. Neurobiol. 1, 195–204 (1982).The initial presentation of a seminal idea in sleep science that is now supported by electrographic, anatomical and molecular findings (see also references 5 and 22).
Czeisler, C. A. & Khalsa, S. S. in Principles and Practice of Sleep Medicine (eds Kryger, M. H., Roth, T. & Dement, W. C.) 353–375 (W. B. Saunders, Philadelphia, Pennsylvania, 2000).
Strecker, R. E. et al. Adenosinergic modulation of basal forebrain and preoptic/anterior hypothalamic neuronal activity in the control of behavioral state. Behav. Brain Res. 115, 183–204 (2000).
Aeschbach, D. et al. Evidence from the waking electroencephalogram that short sleepers live under higher homeostatic sleep pressure than long sleepers. Neuroscience 102, 493–502 (2001).
Werth, E., Achermann P. & Borbély A. A. Fronto-occipital EEG power gradients in human sleep. J. Sleep Res. 6, 102–112 (1997).
Finelli, L. A., Borbély, A. A. & Achermann, P. Functional topography of the human nonREM sleep electroencephalogram. Eur. J. Neurosci. 13, 2282–2290 (2001).An important study showing a frontal predominance of low-frequency EEG rhythms in response to sleep deprivation, which indicates a greater homeostatic need for recovery sleep in the frontal cortex.
Harrison, Y. & Horne, J. The impact of sleep deprivation on decision making: a review. J. Exp. Psychol. Appl. 6, 236–249 (2000).A review on the effects of sleep deprivation on prefrontal functioning.
Beebe, D. W. & Gozal, D. Obstructive sleep apnea and the prefrontal cortex: towards a comprehensive model linking nocturnal upper airway obstruction to daytime cognitive and behavioral deficits. J. Sleep Res. 11, 1–16 (2002).
Balkin, T. J. et al. Bidirectional changes in regional cerebral blood flow across the first 20 minutes of wakefulness. Sleep Res. Online [online] (cited 11 Jul 02) 〈http://www.sro.org/cftemplate/wfsrscongress/indiv.cfm?ID=19998006〉 (1999).
Achermann, P., Werth, E., Dijk, D. J. & Borbély, A. A. Time course of sleep inertia after nighttime and daytime sleep episodes. Arch. Ital. Biol. 134, 109–119 (1995).
Dinges, D. F. in Sleep and Cognition (eds Bootzin, R., Kihlstrom, J. & Schacter, D.) 159–178 (American Psychological Association, Washington DC, 1990).
Llinas, R. & Ribary, U. Coherent 40-Hz oscillation characterizes dream state in humans. Proc. Natl Acad. Sci. USA 90, 2078–2081 (1993).
Anderer, P. et al. Low resolution brain electromagnetic tomography revealed simultaneously active frontal and parietal sleep spindle sources in the human cortex. Neuroscience 103, 581–592 (2001).
Inoue, S., Saha, U. K. & Musha, T. in Rapid Eye Movement Sleep (eds Mallick, B. N. & Inoue, S.) 214–220 (Marcel Dekker, New York, 1999).
Gross, D. W. & Gotman, J. Correlation of high-frequency oscillations with the sleep–wake cycle and cognitive activity in humans. Neuroscience 94, 1005–1018 (1999).
Perez-Garci, E., del Rio-Portilla, Y., Guevara, M. A., Arce, C. & Corsi-Cabrera, M. Paradoxical sleep is characterized by uncoupled gamma activity between frontal and perceptual cortical regions. Sleep 24, 118–126 (2001).
Buchsbaum, M. S., Hazlett, E. A., Wu, J. & Bunney, W. E. Positron emission tomography with deoxyglucose-F18 imaging of sleep. Neuropsychopharmacology 25, S50–S56 (2001).
Maquet, P. Sleep function(s) and cerebral metabolism. Behav. Brain Res. 69, 75–83 (1995).
Maquet, P. et al. Functional neuroanatomy of human slow wave sleep. J. Neurosci. 17, 2807–2812 (1997).
Braun, A. R. et al. Regional cerebral blood flow throughout the sleep–wake cycle. Brain 120, 1173–1197 (1997).The first H 215O PET neuroimaging study to include complete pairwise comparisons of waking, NREM sleep and REM sleep (see also references 47, 52 and 53).
Braun, A. R. et al. Dissociated pattern of activity in visual cortices and their projections during human rapid eye-movement sleep. Science 279, 91–95 (1998).An important extension of reference 46 in which evidence is presented that, during REM sleep, internal information is being processed between extrastriate and limbic cortices while they are functionally isolated from the external world in terms of both input (from the striate cortex) and output (through the frontal cortex).
Hofle, N. et al. Regional cerebral blood flow changes as a function of delta and spindle activity during slow wave sleep in humans. J. Neurosci. 17, 4800–4808 (1997).
Andersson, J. et al. Brain networks affected by synchronized sleep visualized by positron emission tomography. J. Cereb. Blood Flow Metab. 18, 701–715 (1998).
Kajimura, N. et al. Activity of midbrain reticular formation and neocortex during the progression of human non-rapid eye movement sleep. J. Neurosci. 19, 10065–10073 (1999).
Nofzinger, E. A. et al. Towards a neurobiology of dysfunctional arousal in depression: the relationship between beta EEG power and regional cerebral glucose metabolism during NREM sleep. Psychiatry Res. 98, 71–91 (2000).
Maquet, P. et al. Functional neuroanatomy of human rapid-eye-movement sleep and dreaming. Nature 383, 163–166 (1996).The first published H 215O PET study to compare human REM sleep with other behavioural states, and to show relative activation of limbic and midline subcortical areas and relative deactivation of dorsolateral prefrontal cortex in REM sleep (see also references 46, 47 and 53).
Nofzinger, E. A., Mintun, M. A., Wiseman, M. B., Kupfer, D. J. & Moore, R. Y. Forebrain activation in REM sleep: an FDG PET study. Brain Res. 770, 192–201 (1997).Functional neuroimaging of glucose metabolism in REM sleep compared with waking, in which the anterior paralimbic REM activation area is first specifically identified in sleep (see also references 46, 47 and 52).
Nofzinger, E. A. et al. Changes in forebrain function from waking to REM sleep in depression: preliminary analysis of [18F] FDG PET studies. Psychiatry Res. 91, 59–78 (1999).
Lovblad, K. O. et al. Silent functional magnetic resonance imaging demonstrates focal activation in rapid eye movement sleep. Neurology 53, 2193–2195 (1999).
Nofzinger, E. A. et al. Effects of bupropion SR on anterior paralimbic function during waking and REM sleep in depression: preliminary findings using [18F] FDG PET. Psychiatry Res. 106, 95–111 (2001).
Wu, J. et al. Prediction of antidepressant effects of sleep deprivation by metabolic rates in the ventral anterior cingulate and the medial prefrontal cortex. Am. J. Psychiatry 156, 1149–1158 (1999).
Maquet, P. & Franck, G. REM sleep and the amygdala. Mol. Psychiatry 2, 195–196 (1997).
Peigneux, P. et al. Generation of rapid eye movements during pardoxical sleep in humans. Neuroimage 14, 701–708 (2001).
Fosse, R., Stickgold, R. & Hobson, J. A. Brain–mind states: reciprocal variation in thoughts and hallucinations. Psychol. Sci. 12, 30–36 (2001).The demonstration of a reciprocal relationship between thoughts and hallucinatory activity across five distinct behavioural states in a large longitudinal database of the same subjects.
Hobson, J. A., McCarley, R. W. & Wyzinki, P. W. Sleep cycle oscillation: reciprocal discharge by two brainstem neuronal groups. Science 189, 55–58 (1975).
Ajilore, O. A., Stickgold, R., Rittenhouse. C. & Hobson, J. A. Nightcap: laboratory and home-based evaluation of a portable sleep monitor. Psychophysiology 32, 92–98 (1995).
Stickgold, R., Malia, A., Fosse, R. & Hobson, J. A. Brain–mind states. I. Longitudinal field study of sleep/wake factors influencing mentation report length. Sleep 24, 171–179 (2001).
Fosse, M., Fosse, R., Hobson, J. A. & Stickgold, R. Dreaming and episodic memory: a functional dissociation? J. Cogn. Neurosci. (in the press).
Hasselmo, M. Neuromodulation: acetylcholine and memory consolidation. Trends Cogn. Sci. 3, 351–359 (1999).
Hobson, J. A. Dreaming as Delirium (MIT Press, Cambridge, Massachusetts, 1999).
Solms, M. The Neuropsychology of Dreams: a Clinico-Anatomical Study (Lawrence Erlbaum Associates, Mahwah, New Jersey,1997).
Mesulam, M. M. Principles of Behavioral and Cognitive Neurology (Oxford Univ. Press, Oxford, UK, 2000).
Szymusiak, R. Magnocellular nuclei of the basal forebrain: substrates of sleep and arousal regulation. Sleep 18, 478–500 (1995).
Hobson, J. A., Pace-Schott, E. F. & Stickgold, R. Dream science 2000: a response to commentaries on 'Dreaming and the Brain'. Behav. Brain Sci. 23, 1019–1035 (2000).
Kahn, D., Stickgold, R., Pace-Schott, E. F. & Hobson, J. A. Dreaming and waking consciousness: a character recognition study. J. Sleep Res. 9, 317–325 (2000).
Pace-Schott, E. F. 'Theory of mind,' social cognition and dreaming. Sleep Res. Soc. Bull. 7, 33–36 (2001).
LeDoux, J. E. The Emotional Brain (Simon and Schuster, New York, 1996).
Fosse, R., Stickgold, R. & Hobson, J. A. The mind in REM sleep: reports of emotional experience. Sleep 24, 947–955 (2001).
Merritt, J. M., Stickgold, R., Pace-Schott, E., Williams, J. & Hobson, J. A. Emotion profiles in the dreams of men and women. Conscious. Cogn. 3, 46–60 (1994).
Nielsen, T. A., Deslauriers, D. & Baylor, G. W. Emotions in dream and waking event reports. Dreaming 1, 287–300 (1991).
Paus, T. Primate anterior cingulate cortex: where motor control, drive and cognition interface. Nature Rev. Neurosci. 2, 417–424 (2001).
Damasio, A. R. et al. Subcortical and cortical brain activity during the feeling of self-generated emotions. Nature Neurosci. 3, 1049–1056 (2000).
Liotti, M. et al. Differential limbic-cortical correlates of sadness and anxiety in healthy subjects: implications for affective disorders. Biol. Psychiatry 48, 30–42 (2000).
Pace-Schott, E. F. in Sleep and Dreaming: Scientific Advances and Reconsiderations (eds Pace-Schott, E. F., Solms, M., Blagrove, M. & Harnad, S.) (Cambridge Univ. Press, Cambridge, UK, in the press).
Cahill, L. & McGough, J. L. Mechanisms of emotional arousal and lasting declarative memory. Trends Neurosci. 21, 294–299 (1998).
Porte, H. S. & Hobson, J. A. Physical motion in dreams: one measure of three theories. J. Abnormal. Psychol. 105, 329–335 (1996).
Rye, D. B. Contributions of the pedunculopontine region to normal and altered REM sleep. Sleep 20, 757–788 (1997).
Mori, K., Mitani, H., Fujita, M. & Winters, W. D. Multiple unit activity of dorsal cochlear nucleus and midbrain reticular formation during paradoxical phase of sleep. Electroencephalogr. Clin. Neurophysiol. 33, 104–106 (1972).
Schmahmann, J. D. The role of the cerebellum in affect and psychosis. J. Neurolinguist. 13, 189–214 (2000).
Jouvet, M. The Paradox of Sleep: the Story of Dreaming (MIT Press, Cambridge, Massachusetts, 1999).
Revonsuo, A. The reinterpretation of dreams: an evolutionary hypothesis of the function of dreaming. Behav. Brain Sci. 23, 877–901 (2000).
Haxby, J. V., Hoffman, E. A. & Gobbini, M. I. The distributed human neural system for face perception. Trends Cogn. Sci. 4, 223–233 (2000).
Doricchi, F. & Violani, C. in The Neuropsychology of Sleep and Dreaming (eds Antrobus, J. S. & Bertini, M.) (Lawrence Erlbaum Associates, Mahwah, New Jersey, 1992).
Hobson, J. A. The Dream Drug Store (MIT Press, Cambridge, Massachusetts, 2001).
Siegel, J. The REM sleep–memory consolidation hypothesis. Science 294, 1058–1063 (2001).
Vertes, R. P. & Eastman, K. E. The case against memory consolidation in REM sleep. Behav. Brain Sci. 23, 867–876 (2000).
Roffwarg, H. P., Muzio, J. N. & Dement, W. C. Ontogenetic development of the human sleep–dream cycle. Science 152, 604–619 (1966).
Hobson, J. A. Sleep (Scientific American Library, New York, 1989).
Parmelee, A. H., Wenner, W. H., Akiyama, Y., Schultz, M. & Stern, E. Sleep states in premature and full-term newborn infants. Dev. Med. Child Neurol. 9, 70–77 (1967).
Crick, F. & Mitchison, G. The function of dream sleep. Nature 304, 111–114 (1983).
Marks, G. A., Shaffery, J. P., Oksenberg, A., Speciale, S. G. & Roffwarg, H. P. A functional role for REM sleep in brain maturation. Behav. Brain Res. 69, 1–11 (1995).
Frank, M. G., Issa, N. P. & Stryker, M. P. Sleep enhances plasticity in the developing visual cortex. Neuron 30, 275–287 (2001).
Kirkwood, A. & Bear, M. F. Elementary forms of synaptic plasticity in the visual cortex. Biol. Res. 28, 73–80 (1995).
Cheour, M. et al. Sleep sounds learned by sleeping newborns. Nature 415, 599–600 (2002).
Plihal, W. & Born, J. Effects of early and late nocturnal sleep on declarative and procedural memory. J. Cogn. Neurosci. 9, 534–547 (1997).
Smith, C. Sleep states and memory processes. Behav. Brain Res. 69, 137–145 (1995).
Pavlides, C. & Winson, J. Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes. J. Neurosci. 9, 2907–2918 (1989).
Wilson, M. A. & McNaughton, B. L. Reactivation of hippocampal ensemble memories during sleep. Science 265, 676–679 (1994).
Skaggs, W. E. & McNaughton, B. L. Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science 271, 1870–1873 (1996).
Louie, K. & Wilson, M. A. Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron 29, 145–156 (2001).
Poe, G. R., Nitz, D. A., McNaughton, B. L. & Barnes, C. A. Experience dependent phase reversal of hippocampal neuron firing during REM sleep. Brain Res. 855, 176–180 (2000).Shows that rat hippocampal replay of place cells during REM sleep occurs at the peak of theta oscillation — a point that favours LTP — in place cells that correspond to novel environments, but at the trough of theta oscillation — a point that favours long-term depression — for patterns that correspond to familiar environments. The authors suggest that this represents hippocampal consolidation followed by hippocampal erasure as information is transferred, over time, to the neocortex (see also references 103–106 and 108–111).
Nadasdy, Z., Hirase, H., Czurko, A., Csicsvari, J. & Buzsaki, G. Replay and time compression of recurring spike sequences in the hippocampus. J. Neurosci. 19, 9497–9507 (1999).
Hirase, H., Leinekugel, X., Czurko, A., Csicsvari, J. & Buzsaki, G. Firing rates of hippocampal neurons are preserved during subsequent sleep episodes and modified by novel awake experience. Proc. Natl Acad. Sci. USA 98, 9386–9390 (2001).
Siapas, A. G. & Wilson, M. A. Coordinated interactions between hippocampal ripples and cortical spindles during slow wave sleep. Neuron 21, 1123–1128 (1998).
Kudrimoti, H. S., Barnes, G. A. & McNaughton, B. L. Reactivation of hippocampal cell ensembles: effects of behavioral state, experience and EEG dynamics. J. Neurosci. 19, 4090–4101 (1999).
Datta, S. Avoidance task training potentiates phasic pontine-wave density in the rat: a mechanism for sleep-dependent plasticity. J. Neurosci. 20, 8607–8613 (2000).
Sanford, L. D., Silvestri, A. J., Ross, R. J. & Morrison, A. R. Influence of fear conditioning on elicited ponto-geniculo-occipital waves and rapid eye movement sleep. Arch. Ital. Biol. 139, 169–183 (2001).
Dave, A. S. & Margoliash, D. Song replay during sleep and computational rules for sensorimotor vocal learning. Science 290, 812–816 (2000).
Plihal, W. & Born, J. Effects of early and late nocturnal sleep on priming and spatial memory. Psychophysiology 36, 571–582 (1999).
Giuditta, A. et al. The sequential hypothesis of the function of sleep. Behav. Brain Res. 69, 157–166 (1995).
Stickgold, R., Whidbee, D., Schirmer, B., Patel, V. & Hobson, J. A. Visual discrimination task improvement: a multi-step process occurring during sleep. J. Cogn. Neurosci. 12, 246–254 (2000).A study showing a correlation of degree of TDT learning with duration of SWS in the first quarter of the night and REM sleep in the last quarter of the night, indicating a two-step process in the sleep-mediated enhancement of TDT learning (see also references 118–122).
Karni, A. & Sagi, D. Where practice makes perfect in texture discrimination: evidence for primary visual cortex plasticity. Proc. Natl Acad. Sci. USA 88, 4966–4970 (1991).
Stickgold, R., James, L. & Hobson, J. A. Visual discrimination learning requires sleep after training. Nature Neurosci. 3, 1237–1238 (2000).
Karni, A., Tanne, D., Rubenstein, B. S., Askenasy, J. J. M. & Sagi, D. Dependence on REM sleep of overnight improvement of a perceptual skill. Science 265, 679–682 (1994).
Gais, S., Plihal, W., Wagner, U. & Born, J. Early sleep triggers memory for early visual discrimination skills. Nature Neurosci. 3, 1335–1339 (2000).
Mednick, S. et al. The restorative effect of naps on perceptual deterioration. Nature Neurosci. 5, 677–681 (2002).
Walker, M., Brakefield, T., Morgan, A., Hobson, J. A. & Stickgold, R. Practice with sleep makes perfect: sleep-dependent motor learning. Neuron 35, 1–20 (2002).The demonstration of sleep-dependent enhancement of learning on a motor task.
Stickgold, R., Malia, A., Maguire, D., Roddenberry, D. & O'Connor, M. Replaying the game: hypnagogic images in normals and amnesiacs. Science 290, 350–353 (2000).
Stickgold, R., Scott, L., Rittenhouse, C. & Hobson, J. A. Sleep induced changes in associative memory. J. Cogn. Neurosci. 11, 182–193 (1999).
Hartley, D. Observations on Man, His Frame, His Duty and His Expectations (Johnson, London, 1791).
Hobson, J. A., Hoffman, E., Helfand, R. & Kostner, D. Dream bizarreness and the activation–synthesis hypothesis. Hum. Neurobiol. 6, 157–164 (1987).
Maquet, P. et al. Experience-dependent changes in cerebral activation during human REM sleep. Nature Neurosci. 3, 831–836 (2000).The first neuroimaging study to show, in humans, reactivation during sleep of areas corresponding to those activated during a defined preceding waking experience.
Martin, J. H. Neuroanatomy: Text and Atlas 2nd edn (Appleton & Lange, Stamford, Connecticut, 1996).
Hobson, J. A., Stickgold, R. & Pace-Schott, E. F. The neuropsychology of REM sleep dreaming. Neuroreport 9, R1–R14 (1998).
Cantero, J. L., Atienza, M., Stickgold, R. & Hobson, J. A. Nightcap: a reliable system for determining sleep onset latency. Sleep 25, 238–245 (2002).
This work was supported by grants from the National Institute on Drug Abuse and the National Institutes of Health. We thank R. Stickgold, R. Fosse, M. Fosse, M. Delnero and A. Morgan.
Encyclopedia of Life Sciences
MIT Encyclopedia of Cognitive Sciences
- CIRCADIAN RHYTHMS
Biological rhythms of physiology and behaviour that have a 24-h periodicity, which have evolved in response to the 24-h astronomical cycle to which all organisms are exposed.
- ULTRADIAN RHYTHMS
Biological rhythms that have a periodicity of less than 24 h, such as the approximately 90-min REM–NREM cycle of the adult human.
The polysomnographic measurement of eye movement by electrodes mounted adjacent to each eye, which detect movements of the electrical dipole produced by the retina.
- THALAMOCORTICAL OSCILLATIONS
Characteristic rhythmic variations in brain electrical potential that are thought to reflect summated interactions between excitatory and inhibitory neurons of the cortex and thalamus; they emerge when sensory input and ascending arousal from the brainstem reticular activating system to thalamic relay cells diminish during NREM sleep.
- LOCUS COERULEUS
A nucleus of the brainstem that is the main supplier of noradrenaline to the brain.
- DORSAL RAPHE NUCLEUS
A nucleus of the brainstem that comprises a large cluster of serotonin-containing neurons. An important supplier of serotonin to the forebrain and to other brainstem nuclei.
- LONG-TERM POTENTIATION
(LTP). An enduring increase in postsynaptic responsiveness as a result of high-frequency (tetanic) stimulation of presynaptic neurons. It is measured both as the amplitude of excitatory postsynaptic potentials and as the magnitude of postsynaptic-cell population spike. LTP is most often studied in the hippocampus and is often considered to be the cellular basis of learning and memory.
- TWO-PROCESS MODEL
An influential theory of sleep–wake regulation proposed by Alexander Borbély, which states that sleep–wake propensity results from the combined influence of an intrinsic circadian pacemaker and a homeostatic process that depends on the duration of previous waking.
An agent that promotes sleep. Endogenous somnogens accumulate during prolonged waking, tending to favour sleep regardless of the phase of the circadian cycle. Putative somnogens include adenosine, cytokines, hormones, melatonin, oleomide and prostaglandins.
- SLOW-WAVE ACTIVITY
A spectral analytic measure of total power in slow-oscillation and delta frequencies of the electroencephalogram (0.5–4.5 Hz) in NREM sleep, which is thought to be sensitive to the degree of pre-sleep homeostatic sleep pressure.
- EXECUTIVE FUNCTION
A cluster of high-order capacities, which include selective attention, behavioural planning and response inhibition, and the manipulation of information in problem-solving tasks.
- WORKING MEMORY
The representation of items held in consciousness during experiences or after the retrieval of memories. This form of memory is short-lasting and associated with the active rehearsal or manipulation of information.
- SLEEP INERTIA
The persistence of subjective sleepiness and cognitive slowing after awakening from sleep, especially SWS.
- PREFRONTAL CORTEX
The non-motor sectors of the frontal lobe that receive input from the dorsomedial thalamic nucleus and subserve working memory, complex attentional processes and executive functions such as planning, behavioural inhibition, logical reasoning, action monitoring and social cognition.
- BASAL GANGLIA
A group of interconnected subcortical nuclei in the forebrain and midbrain that includes the striatum (putamen and caudate nucleus), globus pallidus, subthalamic nucleus, ventral tegmental area and substantia nigra.
- LIMBIC/PARALIMBIC SYSTEM
Definitions vary, but usually encompass brain regions that are involved in emotion, instinct, memory and the integration of autonomic functions with conscious awareness. Includes subcortical structures such as the amygdala, hippocampus, hypothalamus and basal forebrain, as well as cortical areas such as the parahippocampal, entorhinal, insular, caudal medial orbitofrontal and anterior cingulate cortices.
- PGO WAVES
REM-associated phasic potentials that are recorded sequentially in the pons, thalamic lateral geniculate body and occipital cortex of the cat and are thought to be one way in which pseudosensory information from the brainstem might be transmitted to the cortex during human dreaming.
- BRODMANN AREAS
(BA). Korbinian Brodmann (1868–1918) was an anatomist who divided the cerebral cortex into numbered subdivisions on the basis of cell arrangements, types and staining properties (for example, the dorsolateral prefrontal cortex contains subdivisions, including BA 46, BA 9 and others). Modern derivatives of his maps are commonly used as the reference system for discussion of brain-imaging findings.
A subset of the basal ganglia that is often differentiated into the dorsal striatum (caudate nucleus and putamen) and the ventral striatum (for example, nucleus accumbens).
- EVENT-RELATED POTENTIALS
Electrical potentials that are generated in the brain as a consequence of the synchronized activation of neuronal networks by external stimuli. These evoked potentials are recorded at the scalp and consist of precisely timed sequences of waves or 'components'.
- LONG-TERM DEPRESSION
(LTD). An enduring weakening of synaptic strength that is thought to interact with long term potentiation (LTP) in the cellular mechanisms of learning and memory in structures such as the hippocampus and cerebellum. Unlike LTP, which is produced by brief high-frequency stimulation, LTD can be produced by long-term, low-frequency stimulation.
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Hobson, J., Pace-Schott, E. The cognitive neuroscience of sleep: neuronal systems, consciousness and learning. Nat Rev Neurosci 3, 679–693 (2002). https://doi.org/10.1038/nrn915
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