The cognitive neuroscience of sleep: neuronal systems, consciousness and learning

Key Points

  • 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.

Abstract

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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Figure 1: Levels of organization of sleep.
Figure 2: The thalamocortical machinery for the generation of oscillatory rhythms of NREM sleep and associated plasticity processes.
Figure 3: Relationships between the NREM oscillatory waveforms proposed by Steriade15.
Figure 4: Brain activation during sleep and waking.
Figure 5: The updated AIM formulation of the activation synthesis model of dreaming.
Figure 6: State-related changes measured using the Nightcap system.
Figure 7: Forebrain processes in normal dreaming — an integration of neurophysiological, neuropsychological and neuroimaging data.
Figure 8: A model of sleep-dependent memory consolidation.

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Acknowledgements

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.

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Correspondence to Edward F. Pace-Schott.

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DATABASES

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FURTHER INFORMATION

Encyclopedia of Life Sciences

circadian rhythms

learning and memory

sleep

sleep disorders

Laboratory of Neurophysiology

MIT Encyclopedia of Cognitive Sciences

consciousness

dreaming

memory

memory, human neuropsychology

memory storage, modulation of

sleep

Glossary

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.

ELECTRO-OCULOGRAPHY

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.

SOMNOGEN

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.

STRIATUM

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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