Abstract
Sleep spindles are burstlike signals in the electroencephalogram (EEG) of the sleeping mammalian brain and electrical surface correlates of neuronal oscillations in thalamus. As one of the most inheritable sleep EEG signatures, sleep spindles probably reflect the strength and malleability of thalamocortical circuits that underlie individual cognitive profiles. We review the characteristics, organization, regulation, and origins of sleep spindles and their implication in non-rapid-eye-movement sleep (NREMS) and its functions, focusing on human and rodent. Spatially, sleep spindle-related neuronal activity appears on scales ranging from small thalamic circuits to functional cortical areas, and generates a cortical state favoring intracortical plasticity while limiting cortical output. Temporally, sleep spindles are discrete events, part of a continuous power band, and elements grouped on an infraslow time scale over which NREMS alternates between continuity and fragility. We synthesize diverse and seemingly unlinked functions of sleep spindles for sleep architecture, sensory processing, synaptic plasticity, memory formation, and cognitive abilities into a unifying sleep spindle concept, according to which sleep spindles 1) generate neural conditions of large-scale functional connectivity and plasticity that outlast their appearance as discrete EEG events, 2) appear preferentially in thalamic circuits engaged in learning and attention-based experience during wakefulness, and 3) enable a selective reactivation and routing of wake-instated neuronal traces between brain areas such as hippocampus and cortex. Their fine spatiotemporal organization reflects NREMS as a physiological state coordinated over brain and body and may indicate, if not anticipate and ultimately differentiate, pathologies in sleep and neurodevelopmental, -degenerative, and -psychiatric conditions.
Highlights
HISTORICAL LANDMARKSDEFINITIONS AND MEASUREMENTSROLE IN SLEEP’S MACRO- AND...NEUROPHYSIOLOGICAL MECHANISMS 821CORTICAL STATES AND THEIR ORIGINS 830SLEEP SPINDLES ACROSS THE LIFESPAN 836MEMORY CONSOLIDATIONCOGNITIVE ABILITIES AND INTELLIGENCE 844SLEEP DISORDERS AND...PHARMACOLOGICAL AND TARGETED... 849 UNIFYING VIEWS
hyperpolarization-activated cation-nonselective (HCN) channel subunit expression is variable across thalamic nuclei in rodents [315], with the slow and highly cAMP-sensitive HCN4 subtype enriched in somatosensory thalamus, which contributes to strong sleep spindles in rodent somatosensory cortex
Hippocampal sharp-wave ripples contain brief, high-frequency network discharges called ripples (80 –100 Hz in humans, up to 250 Hz in rodents) that arise within the feedforward circuitry of the CA1 pyramidal layer during non-rapid-eye-movement sleep (NREMS) [89, 229] and that are involved in replay of wakerelated hippocampal activity [504]
Summary
Sleep spindles refer to a well recognizable, burstlike sequence of 10 –15 Hz sinusoidal cycles in the electroencephalogram (EEG) of sleeping mammals. Since these landmark discoveries, sleep spindles have led to insights into novel organizing principles of mammalian sleep and into how sleep relates to cognitive abilities and disease. Sleep spindles have led to insights into novel organizing principles of mammalian sleep and into how sleep relates to cognitive abilities and disease Their phasic appearance over a hierarchy of time scales divides non-rapid-eye-movement sleep (NREMS) into time windows with variable cortical states and sensory arousability. Sleep spindles are becoming a tool to monitor the inner workings of TC loops as they are unconstrained by wakefulness-related activity These advances increase their diagnostic and therapeutic usefulness Ca2ϩ and signaling pathways, gating of synaptic plasticity, and their role in the complex sequence of events leading to sleep-dependent memory consolidation are other aspects awaiting to be clarified Progress on the role of sleep spindles in healthy sleep, and their implication in pathology, requires more insight into these mechanistic questions
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