Sleep and developmental plasticity: not just for kids

doi:10.1016/B978-0-444-53839-0.00014-4

Progress in Brain Research

Volume 193, 2011, Pages 221-232

https://doi.org/10.1016/B978-0-444-53839-0.00014-4 Get rights and content

Abstract

In a variety of mammalian species, sleep amounts are highest during developmental periods of rapid brain development and synaptic plasticity than at any other time in life [Frank, M. G. & Heller, H. C. (1997a). Development of REM and slow wave sleep in the rat. American Journal of Physiology, 272, R1792–R1799; Jouvet-Mounier, D., Astic, L., & Lacote, D. (1970). Ontogenesis of the states of sleep in rat, cat and guinea pig during the first postnatal month. Developmental Psychobiology, 2, 216–239; Roffwarg, H. P., Muzio, J. N., & Dement, W. C. (1966). Ontogenetic development of the human sleep-dream cycle. Science, 604–619]. Many of the mechanisms governing developmental plasticity also mediate plasticity in the adult brain. Therefore, studying the role of sleep in developmental plasticity may provide insights more generally into sleep function across the lifespan. In this chapter, I review the evidence that supports a critical role for sleep in developmental brain plasticity. I begin with an overview of past studies that support a role for sleep in general brain maturation. This is followed by more recent findings in the developing visual cortex that more specifically address a possible role for sleep in cortical plasticity.

Section snippets

Historical approaches to neonatal sleep function

Scientific views about sleep in early life have been greatly influenced by the seminal work of Howard Roffwarg and colleagues. In their present classic study in human infants, Roffwarg et al. (1966) proposed that the large amounts of rapid-eye-movement (REM) sleep in early infancy provide an important source of endogenous neural activity necessary for brain maturation. In the more recent formulations of the “Ontogenetic Hypothesis,” it is suggested that REM sleep not only promotes normal brain

Sleep and subcortical development in central visual pathways

A series of studies in the 1980s demonstrated a potential role for REM sleep in the early development of the LGN. Davenne and Adrien examined changes in neuronal morphology in the LGN in kittens after lesioning PGO generating centers in the brainstem (Davenne and Adrien, 1984). Bilateral electrolytic lesions in the rostral pontine tegmentum abolished PGO waves in the neonatal cat, resulting in smaller LGN volumes and reduced LGN soma sizes. A second study showed that PGO wave elimination

Sleep and ocular dominance plasticity

Ocular dominance plasticity (ODP) refers to physiological and anatomical changes in visual cortical circuits triggered by alterations in binocular vision. Although originally described in developing animals (Hubel and Wiesel, 1970, Wiesel and Hubel, 1963), ODP also occurs in the adult brain (Sato and Stryker, 2008, Sawtell et al., 2003) and shares in common numerous mechanisms that mediate plasticity in the hippocampus and nonsensory cortex. For example, like hippocampal-based synaptic

Summary

The Ontogenetic Hypothesis, at least in broad strokes, appears to have stood the test of time. Although much less work has been done in this area compared to other areas in sleep biology, there is a core set of findings that supports a role for sleep in brain development and plasticity. There are also a number of intriguing, unanswered questions yet to be explored.

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Citation Excerpt :
In this context, studies from developing human and animal brains have shown that merging role of sleep in the maturation and development of the brain and children with poor sleep usually experience several psychiatric, attention, behavioral, and cognitive problems in later life [11,234]. Indeed, it has been reported that sleep is essential for cortical maturation, myelination, synapse formation, the proliferation of oligodendrocytes, and modulation of neural cell membrane homeostasis [11,235–239]. In this view, studies have shown that rapid eye movement (REM) sleep is essential for the early myelination of the sensory processing areas and plays a key role in eliminating and maintaining the newly formed synapses, thus controlling the process of learning and memory [11,239,240].
Autism spectrum disorders (ASD) are a group of neurodevelopmental disorders that develop in early life due to interaction between several genetic and environmental factors and lead to alterations in brain function and structure. During the last decades, several mechanisms have been placed to explain the pathogenesis of autism. Unfortunately, these are reported in several studies and reviews which make it difficult to follow by the reader. In addition, some recent molecular mechanisms related to ASD have been unrevealed. This paper revises and highlights the major common molecular mechanisms responsible for the clinical symptoms seen in people with ASD, including the roles of common genetic factors and disorders, neuroinflammation, GABAergic signaling, and alterations in Ca⁺² signaling. Besides, it covers the major molecular mechanisms and signaling pathways involved in initiating the epileptic seizure, including the alterations in the GABAergic and glutamate signaling, vitamin and mineral deficiency, disorders of metabolism, and autoimmunity. Finally, this review also discusses sleep disorder patterns and the molecular mechanisms underlying them.
Sleep Assessment for Sleep Problems in Children
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Sleep is an active process with varying functions that differ with age and development, and are inclusive of, but not limited to, brain development,1 synaptic plasticity,2,3 learning and attention,4 emotional regulation,5 and behavior.6
Developmental pathways towards mood disorders in adult life: Is there a role for sleep disturbances?
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Citation Excerpt :
Particularly, Ringli and Huber (201l) hypothesized that slow wave sleep may contribute to cortical maturation by playing a role in the balance of brain synaptic strengthening/formation weakening/elimination that is titled during development (Ringli and Huber 201l). Sleep, especially slow wave activity, has been hypothesized to normalize synaptic strength and shape plastic brain processes (Frank 2011; Kayser et al., 2014; Kurth et al., 2015). In particular animal studies have shown that during critical periods of life, sleep is required for plastic processes underlying the maturation of specific brain circuits (Ringli and Huber 201l; Kayser et al., 2014; Kurth et al., 2015).
Mood disorders are among the most prevalent and serious mental disorders and rank high among to the leading global burdens of disease. The developmental psychopathology framework can offer a life course perspective on them thus providing a basis for early prevention and intervention. Sleep disturbances, are considered risk factors for mood disorders across childhood, adolescence and adulthood. Assuming that sleep disturbances may play a pivotal role in the pathogenesis of mood disorders from a life course point of view, we reviewed the data on developmental pathways towards mood disorders in adult life in relation to sleep disturbances.
From February 2017, a systematic search was conducted in PubMed, PsycINFO and Embase electronic databases for literature on developmental pathways to mood disorders in adult life in relation to sleep disturbances and to 1) pre-natal stress, 2) early brain developmental processes, and 3) temperaments, character and attachment style.
Eleven, 54 and 15 articles were respectively selected.
Experimental and clinical studies revealed that exposure to prenatal/early life stress results in sleep disturbances such as poor sleep and altered circadian regulation phases and may predict or even precipitate mood disorders in adulthood. Chronic sleep disruption may interfere with neuronal plasticity, connectivity and the developing brain thus contributing to the development of mood disorders. In addition sleep and circadian dysregulations have been shown to be related to those temperaments, character and attachment styles which are considered precursors of mood disorders. Sleep and circadian behaviours may serve as early targets regarding mood disorders.
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Ever since its discovery by Aserinsky and Kleitman in 1953, the quest to understand the function of rapid eye movement (REM) sleep has inspired researchers. Experimental evidence implicates both nonrapid eye movement (NREM) and REM sleep in learning and memory consolidation, although the underlying mechanisms remain unclear. It was suggested that REM sleep might provide a neural environment supporting processes essential to learning and cognition, including synaptic remodeling mechanisms such as long-term potentiation (LTP) and depotentiation or synaptic pruning of spines formed during previous wakefulness. Furthermore, the hypothesis “Sleep to remember, sleep to forget” posits that NREM sleep is important for the consolidation of newly formed memories, whereas the REM sleep state eliminates dispensable spines, thereby improving the signal-to-noise ratio in neural networks, the latter process often being referred to as an “unlearning” process that helps stabilize newly formed synapses and memories. In humans, REM sleep has frequently been associated with dreaming, which led to the hypothesis that REM sleep is important for the reactivation of emotional events that occurred during the previous waking period. Accordingly, the reactivation of brain regions linked to emotion regulation has been suggested to facilitate the consolidation of newly formed memories. Finally, the abundance of REM sleep during perinatal periods has supported the idea that REM sleep provides a context during which the development of neural circuits is facilitated.

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Chapter 14 - Sleep and developmental plasticity: not just for kids

Abstract

Section snippets

Historical approaches to neonatal sleep function

Sleep and subcortical development in central visual pathways

Sleep and ocular dominance plasticity

Summary

Current Opinion in Neurobiology

Neuron

Neuron

Trends in Neurosciences

Neuropharmacology

Neuroscience Letters

Brain Research

Trends in Neurosciences

Brain Research

Neuron

Neuroscience

Brain Research Bulletin

Pharmacology, Biochemistry, and Behavior

Pharmacology, Biochemistry, and Behavior

Behavioural Brain Research

Neuropharmacology

Neuron

Neuron

Brain Research

Brain Research

Brain Research

Brain Research

Developmental Brain Research

Brain Research

Physiology & Behavior

Neuron

Neuropharmacology

Developmental Brain Research

Neuroscience

Trends in Neurosciences

Neuron

Progress in Brain Research

Sleep Medicine Reviews

Neuroscience and Biobehavioral Reviews

Neuron

Progress in Neurobiology

Pharmacology, Biochemistry, and Behavior

European Journal of Pharmacology

Some aspects of the behavior of young and adult rats treated with p-chlorophenylalanine in infancy

Developmental Psychobiology

The sedating antidepressant trazodone impairs sleep-dependent cortical plasticity

PloS ONE

Disruption of experience-dependent synaptic modifications in striate cortex by infusion of an NMDA receptor antagonist

The Journal of Neuroscience

Cellular and molecular connections between sleep and synaptic plasticity

Progress in Neurobiology

The epidimiology of psychotropic drug use in children and adolescents

International Review of Psychiatry

Sleep to remember

The Neuroscientist

Role of the calcium-binding protein parvalbumin in short-term synaptic plasticity

Proceedings of the National Academy of Sciences of the United States of America

The ratio of NR2A/B NMDA receptor subunits determines the qualities of ocular dominance plasticity in visual cortex

Proceedings of the National Academy of Sciences of the United States of America

Synaptic plasticity: Multiple forms, functions, and mechanisms

Neuropsychopharmacology