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The Cognitive Neuroscience of Sleep: Neuronal Systems, Consciousness and Learning

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The Cognitive Neuroscience of Sleep: Neuronal Systems, Consciousness and Learning REVIEWS THE COGNITIVE NEUROSCIENCE OF SLEEP: NEURONAL SYSTEMS, CONSCIOUSNESS AND LEARNING J. Allan Hobson and Edward F. Pace-Schott 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. CIRCADIAN RHYTHMS Can the neurobiology of sleep help us to understand keen interest in the electrophysiology and functional Biological rhythms of the neural basis of conscious experience? Does sleep significance of the brain-activated REM sleep state, physiology and behaviour that have consequences for cognitive functions such as given that it supports the greatest frequency and inten- have a 24-h periodicity, which learning and memory? We have recently reviewed the sity of dreaming, and its EEG bears a marked similarity have evolved in response to the 2,3 24-h astronomical cycle to genetic, cellular and subcortical mechanisms that con- to that of waking . In recent years, NREM sleep has which all organisms are trol the CIRCADIAN RHYTHMS of sleeping and waking, as been increasingly investigated in terms of its underlying exposed. well as the ULTRADIAN regularity of alternating rapid eye electrophysiology4,5, its accompanying subjective experi- movement (REM) and non-REM (NREM) stages of ences6, and its role in information transfer and organi- ULTRADIAN RHYTHMS 1 Biological rhythms that have a sleep . Here, we extend this examination of sleep zation in support of waking performance, exemplified 7–10 periodicity of less than 24 h, upwards in the hierarchy of biological organization. We by learning and memory . FIGURE 1a shows how such as the approximately first consider regional changes in neuronal activity dur- observations at the level of cerebral electrophysiology in 90-min REM–NREM cycle of ing sleep, and relate them to the accompanying alter- sleep lead to the consideration of conscious experience the adult human. ations in conscious experience. Then we examine the and cognitive performance. Laboratory of functional significance of the neurobiological changes Technological innovations that have changed our Neurophysiology, associated with sleep, with respect to their impact on picture of the brain basis of experience in waking and Department of Psychiatry, the efficiency of waking cognition. sleep include advances in quantitative electrophysiol- Harvard Medical School, Massachusetts Mental Traditionally, changes in the functions of neuronal ogy, the advent of functional neuroimaging, and the Health Center, systems have been measured at the level of organismal ability to record the waking and sleep of subjects out- 74 Fenwood Road, Boston, physiology by electrophysiological techniques, includ- side the sleep laboratory. Here, we show how it is now Massachusetts 02115, USA. ing electroencephalography (EEG), ELECTRO-OCULOGRAPHY possible to map upwards from the level of neuromodu- Correspondence to E.F.P.-S. (EOG) and electromyography (EMG), which are collec- latory systems to the functional geography of the e-mail: edward_schott@ 3,8,11 hms.harvard.edu tively termed polysomnography (PSG) and used to human brain and, finally, to cognition . FIGURE 1b doi:10.1038/nrn915 characterize sleep. Historically, there has also been a shows key brain regions involved in the control of NATURE REVIEWS | NEUROSCIENCE VOLUME 3 | SEPTEMBER 2002 | 679 © 2002 Nature Publishing Group REVIEWS a sleep–wake and REM–NREM cycles, along with the Behavioural state Wake NREM REM associated cognitive phenomena and functions. The Cognitive Acquisition Iteration Integration upper tier of structures is considered in this review; consequences of information of informatiion of information the lower tier is described in REF.1. Conscious Sensation and Vivid, externally Dull or absent Vivid, internally experience perception generated generated Electrophysiology of the sleeping brain Thought Logical Logical Illogical Quantitative electrophysiology in animals and increas- progressive perseverative bizarre ingly sophisticated processing of human scalp EEG sig- Movement Continuous Episodic Commanded but voluntary involuntary inhibited nals have gradually revealed how widespread cortical and subcortical systems generate the characteristic elec- Surface EMG trical rhythms of the different stages of sleep. Meanwhile, recordings EEG neuroimaging has allowed researchers to infer state- EOG dependent increases and decreases in the net activity of Single-cell PGO waves in lateral neuronal populations in specific subcortical and cortical depth geniculate nucleus regions. Investigators who use these techniques are recordings REM off (cat) Aminergic systems focusing attention increasingly on the role of sleep in (5-HT and NA) neuroplasticity, learning and memory 8,11–15. In this sec- REM on tion, we attempt to integrate the findings from these Cholinergic systems diverse sources and to present a unified picture. b Forebrain areas key to the neuropsychology of dreaming Thalamocortical generation of NREM oscillations Prefrontal cortex: Anterior limbic structures: Posterior cortices: At all levels of the neuraxis (including ascending acti- • Ventromedial • Amygdala, anterior cingulate, • Inferior parietal • Dorsolateral ventral striatum • Visual association vating systems of the brainstem and diencephalon, thalamic relay nuclei and the neocortex), most neurons show decreased firing during the transition from Thalamocortical 4 control of NREM waking to NREM sleep . These changes probably result sleep rhythms, from the classical disfacilitation of rostral areas by EEG activation and deactivation diminished excitation from neural systems that ascend from the brainstem4, and they validate Moruzzi and Magoun’s original concept16 of a reticular activating system. FIGURE 2 illustrates the anatomical structures and key cell types that are involved in the production and control of thalamocortically generated sleep rhythms. For THALAMOCORTICAL OSCILLATIONS to begin, several Hippocampal–cortical control of memory neuromodulatory influences on thalamocortical net- consolidation works must attenuate. These activating inputs include noradrenergic neurons from the LOCUS COERULEUS,sero- tonergic (5-hydroxytryptamine (5-HT)-synthesizing) Origin and expression Diencephalic control Pontine control of the projections from the DORSAL RAPHE NUCLEUS, histaminergic of circadian rhythms of sleep onset REM–NREM cycle neurons from the tuberomammillary nucleus, orexin- Hypothalamic nuclei: Hypothalamic nuclei: Mesopontine nuclei: ergic neurons from the lateral hypothalamus, and cholin- • Suprachiasmatic • Ventrolateral preoptic • Laterodorsal tegmental ergic neurons from the mesopontine tegmentum and • Subparaventricular • Lateral • Pedunculopontine 1 • Dorsomedial • Tuberomammillary • Dorsal raphe basal forebrain . Such inputs diminish under the influ- Basal forebrain • Locus coeruleus ence of circadian and homeostatic signals from the hypo- thalamus that are thought to be linked to sleep–wake Figure 1 | Levels of organization of sleep. a | Manifestation of the three cardinal states of 17 consciousness at levels of neural organization from the cellular generators of the non-rapid eye switching mechanisms . Just as diminution of ascend- movement (NREM)–REM cycle in the pontine brainstem to the state-dependent processing of ing activation allows thalamocortical oscillatory rhythms cognitive information in the forebrain. At the bottom level, depth recordings from single neurons in to emerge, such oscillations are abolished by the renewal the pontine brainstem of the cat show the reciprocal waning of firing in REM-off aminergic cells and of ascending cholinergic activation in REM sleep, and of waxing of firing in cholinergic REM-on cells1,3. Also depicted are the ponto-geniculo-occipital (PGO) cholinergic, aminergic and, possibly, histaminergic and waves that are proposed to convey pseudosensory information from the REM-activated subcortex orexinergic activation in waking4. to the neocortex during dreaming2. The second level (surface recordings) illustrates the characteristic physiological signs of each state in human polysomnographic (PSG) recordings that Drawing on two decades of work in animal models, consist of electroencephalogram (EEG), electro-oculogram (EOG) and electromyogram (EMG) Steriade’s group has begun to advance mechanistic output1,94. The third level lists variations in conscious experience during waking, NREM and REM models and functional hypotheses for the thalamocorti- sleep dreaming. The top level shows a proposed role for each state in the processing of cal oscillations that appear as waveforms of characteris- information related to learning and memory. 5-HT, 5-hydroxytryptamine (serotonin); NA, tic morphology and frequency in the human scalp EEG
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