Homeostatic interplay between electrical activity and neuronal apoptosis in the developing neocortex

Blanquie, Oriane; Kilb, Werner; Sinning, Anne; Luhmann, Heiko J.

doi:10.1016/j.neuroscience.2017.06.030

Cited by 50 publications

(59 citation statements)

References 140 publications

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“…Early oscillatory activity in vivo has been most extensively – but not exclusively – described in the cortex and hippocampus . In these forebrain structures, fragmented oscillatory activity is thought to assist in the development of local neuronal networks, with effects on synapse formation, neuronal differentiation and migration, programmed cell death (apoptosis), and formation and refinement of topographic maps …”

Section: Synchronized Oscillations Orchestrate the Development Of Neumentioning

confidence: 99%

“…Perhaps the most direct, causal evidence for a role of oscillations in brain development comes from studies assessing their involvement in apoptosis . Apoptosis is the physiological process through which neurons and other cells die.…”

Section: Synchronized Oscillations Orchestrate the Development Of Neumentioning

confidence: 99%

“…This death is a normal process that complements the over‐production of neurons that characterizes early development; accordingly, apoptosis is a key contributor to the anatomical and functional development of the nervous system . Notably, in rat pups, oscillatory activity appears to determine the rate of apoptosis in sensorimotor cortex . Specifically, area‐specific levels of neuronal activity inversely correlate with the number of apoptotic neurons detected in local networks.…”

Section: Synchronized Oscillations Orchestrate the Development Of Neumentioning

confidence: 99%

“…In the cerebral cortex of humans and rodents, the earliest neural activity is characterized by the presence of brief oscillatory bursts interposed with periods of silence; this pattern of fragmented activity is referred to as discontinuous . Although different from the continuous oscillatory patterns of adults, these early oscillations appear to have important functions for the development of the nervous system . In addition, temporal coupling or coactivation of brief oscillatory events is indicative of connectivity among functionally related neural structures …”

Section: Introductionmentioning

confidence: 96%

“…Although different from the continuous oscillatory patterns of adults, these early oscillations appear to have important functions for the development of the nervous system. [3,[18][19][20] In addition, temporal coupling or coactivation of brief oscillatory events is indicative of connectivity among functionally related neural structures. [3,6,7,9,21] Early oscillatory dynamics in rats have often been described using in vitro preparations or under anesthetic conditions in vivo that preclude the normal expression of sleep-wake cycles.…”

Section: Introductionmentioning

confidence: 99%

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Active Sleep Promotes Functional Connectivity in Developing Sensorimotor Networks

Rio-Bermudez

Blumberg

2018

BioEssays

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A ubiquitous feature of active (REM) sleep in mammals and birds is its relative abundance in early development. In rat pups across the first two postnatal weeks, active sleep promotes the expression of synchronized oscillatory activity within and between cortical and subcortical sensorimotor structures. Sensory feedback from self-generated myoclonic twitches - which are produced exclusively during active sleep - also triggers neural oscillations in those structures. We have proposed that one of the functions of active sleep in early infancy is to provide a context for synchronizing developing structures. Specifically, neural oscillations contribute to a variety of neurodevelopmental processes, including synapse formation, neuronal differentiation and migration, apoptosis, and the refinement of topographic maps. In addition, synchronized oscillations promote functional connectivity between distant brain areas. Consequently, any condition or manipulation that restricts active sleep can, in turn, deprive the infant animal of substantial sensory experience, resulting in atypical developmental trajectories.

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Section: Synchronized Oscillations Orchestrate the Development Of Neumentioning

confidence: 99%

Section: Synchronized Oscillations Orchestrate the Development Of Neumentioning

confidence: 99%

Section: Synchronized Oscillations Orchestrate the Development Of Neumentioning

confidence: 99%

Section: Introductionmentioning

confidence: 96%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Active Sleep Promotes Functional Connectivity in Developing Sensorimotor Networks

Rio-Bermudez

Blumberg

2018

BioEssays

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Large‐scale waves of activity in the neonatal mouse brain in vivo occur almost exclusively during sleep cycles

Tabuena

Huynh

Metcalf

et al. 2022

Developmental Neurobiology

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Spontaneous electrical activity plays major roles in the development of cortical circuitry. This activity can occur highly localized regions or can propagate over the entire cortex. Both types of activity coexist during early development. To investigate how different forms of spontaneous activity might be temporally segregated, we used wide‐field trans‐cranial calcium imaging over an entire hemisphere in P1–P8 mouse pups. We found that spontaneous waves of activity that propagate to cover the majority of the cortex (large‐scale waves; LSWs) are generated at the end of the first postnatal week, along with several other forms of more localized activity. We further found that LSWs are segregated into sleep cycles. In contrast, cortical activity during wake states is more spatially restricted and the few large‐scale forms of activity that occur during wake can be distinguished from LSWs in sleep based on their initiation in the motor cortex and their correlation with body movements. This change in functional cortical circuitry to a state that is permissive for large‐scale activity may temporally segregate different forms of activity during critical stages when activity‐dependent circuit development occurs over many spatial scales. Our data also suggest that LSWs in early development may be a functional precursor to slow sleep waves in the adult, which play critical roles in memory consolidation and synaptic rescaling.

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

Rio-Bermudez

Blumberg

2021

Hippocampus

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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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Homeostatic interplay between electrical activity and neuronal apoptosis in the developing neocortex

Cited by 50 publications

References 140 publications

Active Sleep Promotes Functional Connectivity in Developing Sensorimotor Networks

Active Sleep Promotes Functional Connectivity in Developing Sensorimotor Networks

Large‐scale waves of activity in the neonatal mouse brain in vivo occur almost exclusively during sleep cycles

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

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