Twitches emerge postnatally during quiet sleep in human infants and are synchronized with sleep spindles

Sokoloff, Greta; Dooley, James C.; Glanz, Ryan M.; Wen, Rebecca Y.; Hickerson, Meredith M.; Evans, Laura G.; Laughlin, Haley M.; Apfelbaum, Keith S.; Blumberg, Mark S.

doi:10.1016/j.cub.2021.05.038

Cited by 29 publications

(19 citation statements)

References 29 publications

(51 reference statements)

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“…In addition, our companion paper (PLACEHOLDER REFERENCE), further demonstrates that behavioral sleep habits are intertwined with neurophysiological sleep EEG features in infants: slow wave activity is related to daytime napping, whereas spindle density is associated with nighttime movements and awakenings. This supports the proposed concept that spindles play a role in sensorimotor microcircuitry development (Fernandez and Lüthi, 2020;Sokoloff et al, 2021). Thus, likely slow waves and spindles not only may serve as early biomarkers for altered thalamocortical connectivity, they are possibly furthermore crucial players in the sleep-dependent plasticity processes underlying neurodevelopmental changes.…”

Section: Thalamocortical Connectivity Is Quantified With Diffusion Tensor Imaging and Functional Magneticsupporting

confidence: 82%

“…The copyright holder for this preprint this version posted November 11, 2021. ; https://doi.org/10.1101/2021.11.10.468053 doi: bioRxiv preprint Interestingly, this process might involve brief muscle contractions -so-called myoclonic twitching. A recent study demonstrated that myoclonic twitches, which are thought to promote thalamocortical development through sensorimotor feedback loops, are concomitant with spindles in infants (Sokoloff et al, 2021). This hypothesis is further supported by the findings outlined in our companion paper demonstrating that an infant's spindle density correlates with nighttime movement (PLACEHOLDER REFERENCE).…”

Section: Discussionsupporting

confidence: 72%

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An Infant Sleep Electroencephalographic Marker of Thalamocortical Connectivity Predicts Behavioral Outcome in Late Infancy

Jaramillo¹,

Schoch²,

Markovic

et al. 2021

Preprint

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Infancy represents a critical period during which thalamocortical brain connections develop and mature. Deviations in the maturation of thalamocortical connectivity are linked to neurodevelopmental disorders. There is a lack of early biomarkers to detect and localize neuromaturational deviations, which can be overcome with mapping through high-density electroencephalography (hdEEG) assessed in sleep. Specifically, slow waves and spindles in non-rapid eye movement (NREM) sleep are generated by the thalamocortical system, and their characteristics, slow wave slope and spindle density, are closely related to neuroplasticity and learning. Recent studies further suggest that information processing during sleep underlying sleep-dependent learning is promoted by the temporal coupling of slow waves and spindles, yet slow wave-spindle coupling remains unexplored in infancy. Thus, we evaluated three potential biomarkers: 1) slow wave slope, 2) spindle density, and 3) the temporal coupling of slow waves with spindles. We use hdEEG to first examine the occurrence and spatial distribution of these three EEG features in healthy infants and second to evaluate a predictive relationship with later behavioral outcomes. We report four key findings: First, infants’ EEG features appear locally: slow wave slope is maximal in occipital and frontal areas, whereas spindle density is most pronounced frontocentrally. Second, slow waves and spindles are temporally coupled in infancy, with maximal coupling strength in the occipital areas of the brain. Third, slow wave slope, spindle density, and slow wave-spindle coupling are not associated with concurrent behavioral status (6 months). Fourth, spindle density in central and frontocentral regions at age 6 months predicts later behavioral outcomes at 12 and 24 months. Neither slow wave slope nor slow wave-spindle coupling predict behavioral development. Our results propose spindle density as an early EEG biomarker for identifying thalamocortical maturation, which can potentially be used for early diagnosis of neurodevelopmental disorders in infants. These findings are complemented by our companion paper that demonstrates the linkage of spindle density to infant nighttime movement, framing the possible role of spindles in sensorimotor microcircuitry development. Together, our studies suggest that early sleep habits, thalamocortical maturation, and behavioral outcome are closely interwoven. A crucial next step will be to evaluate whether early therapeutic interventions may be effective to reverse deviations in identified individuals at risk.HighlightsSlow waves and spindles occur in a temporally coupled manner in infancySlow wave slope, spindle density, and slow wave-spindle coupling are not related to concurrent behavioral developmentSpindle density at 6 months predicts behavioral status at 12 and 24 monthsSlow wave slope and slow wave-spindle coupling are not predictive of behavioral development

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Section: Thalamocortical Connectivity Is Quantified With Diffusion Tensor Imaging and Functional Magneticsupporting

confidence: 82%

Section: Discussionsupporting

confidence: 72%

An Infant Sleep Electroencephalographic Marker of Thalamocortical Connectivity Predicts Behavioral Outcome in Late Infancy

Jaramillo¹,

Schoch²,

Markovic

et al. 2021

Preprint

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“…A unique feature of REM sleep is the occurrence of myoclonic twitches, or spontaneous, discrete, spastic movements of the limbs (Tiriac et al, 2012 ; Blumberg et al, 2013 ; Sokoloff et al, 2020 ). These twitches occur throughout the mammalian lifespan, but are particularly abundant in infancy (Tiriac et al, 2012 ; Blumberg et al, 2013 ; Sokoloff et al, 2020 , 2021 ). The development of myoclonic twitches depends on sensory feedback; the spatiotemporal organization of twitches is disrupted in newborn ErbB2 muscle-specific knockout mice which lack muscle spindles and exhibit impaired proprioception in adulthood (Blumberg et al, 2015 ).…”

Section: Developmentmentioning

confidence: 99%

Roles for Sleep in Neural and Behavioral Plasticity: Reviewing Variation in the Consequences of Sleep Loss

Weiss

Donlea

2022

Front. Behav. Neurosci.

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Sleep is a vital physiological state that has been broadly conserved across the evolution of animal species. While the precise functions of sleep remain poorly understood, a large body of research has examined the negative consequences of sleep loss on neural and behavioral plasticity. While sleep disruption generally results in degraded neural plasticity and cognitive function, the impact of sleep loss can vary widely with age, between individuals, and across physiological contexts. Additionally, several recent studies indicate that sleep loss differentially impacts distinct neuronal populations within memory-encoding circuitry. These findings indicate that the negative consequences of sleep loss are not universally shared, and that identifying conditions that influence the resilience of an organism (or neuron type) to sleep loss might open future opportunities to examine sleep's core functions in the brain. Here, we discuss the functional roles for sleep in adaptive plasticity and review factors that can contribute to individual variations in sleep behavior and responses to sleep loss.

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“…Although twitch‐triggered spindle bursts during AS disappear within the first postnatal month (Whitehead, Meek, & Fabrizi, 2018), this should not be interpreted as evidence that twitches fail to trigger neural activity in cortical and subcortical structures at later ages. Moreover, beginning around 3 months of age, twitches begin to emerge during quiet sleep and, as they do so, they occur in synchrony with sleep spindles (Sokoloff et al, 2021). Importantly, in humans across the lifespan, sleep spindles have been implicated in a variety of functions associated with learning and memory (Mason, Lokhandwala, Riggins, & Spencer, 2021; Rasch & Born, 2013).…”

Section: Implications For Future Researchmentioning

confidence: 99%

Sleep as a window on the sensorimotor foundations of the developing hippocampus

Rio-Bermudez

Blumberg

2021

Hippocampus

Self Cite

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The hippocampal formation plays established roles in learning, memory, and related cognitive functions. Recent findings also suggest that the hippocampus integrates sensory feedback from self‐generated movements to modulate ongoing motor responses in a changing environment. Such findings support the view of Bland and Oddie (Behavioural Brain Research, 2001, 127, 119–136) that the hippocampus is a site of sensorimotor integration. In further support of this view, we review neurophysiological evidence in developing rats that hippocampal function is built on a sensorimotor foundation and that this foundation is especially evident early in development. Moreover, at those ages when the hippocampus is first establishing functional connectivity with distant sensory and motor structures, that connectivity is preferentially expressed during periods of active (or REM) sleep. These findings reinforce the notion that sleep, as the predominant state of early infancy, provides a critical context for sensorimotor development, including development of the hippocampus and its associated network.

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Twitches emerge postnatally during quiet sleep in human infants and are synchronized with sleep spindles

Cited by 29 publications

References 29 publications

An Infant Sleep Electroencephalographic Marker of Thalamocortical Connectivity Predicts Behavioral Outcome in Late Infancy

An Infant Sleep Electroencephalographic Marker of Thalamocortical Connectivity Predicts Behavioral Outcome in Late Infancy

Roles for Sleep in Neural and Behavioral Plasticity: Reviewing Variation in the Consequences of Sleep Loss

Sleep as a window on the sensorimotor foundations of the developing hippocampus

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