Changing subplate circuits: Early activity dependent circuit plasticity

Abstract

Early neural activity in the developing sensory system comprises spontaneous bursts of patterned activity, which is fundamental for sculpting and refinement of immature cortical connections. The crude early connections that are initially refined by spontaneous activity, are further elaborated by sensory-driven activity from the periphery such that orderly and mature connections are established for the proper functioning of the cortices. Subplate neurons (SPNs) are one of the first-born mature neurons that are transiently present during early development, the period of heightened activity-dependent plasticity. SPNs are well integrated within the developing sensory cortices. Their structural and functional properties such as relative mature intrinsic membrane properties, heightened connectivity via chemical and electrical synapses, robust activation by neuromodulatory inputs—place them in an ideal position to serve as crucial elements in monitoring and regulating spontaneous endogenous network activity. Moreover, SPNs are the earliest substrates to receive early sensory-driven activity from the periphery and are involved in its modulation, amplification, and transmission before the maturation of the direct adult-like thalamocortical connectivity. Consequently, SPNs are vulnerable to sensory manipulations in the periphery. A broad range of early sensory deprivations alters SPN circuit organization and functions that might be associated with long term neurodevelopmental and psychiatric disorders. Here we provide a comprehensive overview of SPN function in activity-dependent development during early life and integrate recent findings on the impact of early sensory deprivation on SPNs that could eventually lead to neurodevelopmental disorders.

Distinct distribution of subplate neuron subtypes between the sensory cortices during the early postnatal period

“…The auditory cortex (ACtx) is responsible for central sound processing. The SpNs in the ACtx respond to sounds and SpN circuits can be shaped by early auditory and visual experience (Meng et al, 2021;Mukherjee & Kanold, 2023;Mukherjee et al, 2022;Wess et al, 2017); thus, SpNs might play a crucial role in cortical circuit development and cortical processing before and after the presence of peripheral stimuli.…”

“…The auditory cortex (ACtx) is responsible for central sound processing. The SpNs in the ACtx respond to sounds and SpN circuits can be shaped by early auditory and visual experience (Meng et al., 2021; Mukherjee & Kanold, 2023; Mukherjee et al., 2022; Wess et al., 2017); thus, SpNs might play a crucial role in cortical circuit development and cortical processing before and after the presence of peripheral stimuli. Previous studies in the ACtx showed that the distinct spatial intracortical connectivity of SpNs changes during the first two postnatal weeks (PNWs) in mice (Meng et al., 2014; Viswanathan et al., 2012).…”

Dexmedetomidine as a Short-Use Analgesia for the Immature Nervous System

“…Interference with the cellular mechanisms involved in immature neural activity generation, through the administration of volatile anesthetics for general anesthesia, results in neuronal apoptosis in the developing nervous system [ 23 , 24 , 25 , 26 ]. Modulation of immature neuronal activity by sensory deprivation during the late in utero or early postnatal period results in alterations to cortical map development in the sensory systems ([ 27 , 28 , 29 , 30 , 31 ]; see [ 32 ], for review). It is arguably the crucial supracellular mechanism of the development of the brain’s diverse functional organization, and modulation of it affects the development of brain structures.…”

Early retinal deprivation crossmodally alters nascent subplate circuits and activity in the auditory cortex during the precritical period

“…For example, peripheral insult during the precritical period intramodally alters circuit connectivity of the earlier born subplate neurons (SPNs) (Meng et al, 2021; Mukherjee et al, 2021). SPNs are the first targets of thalamocortical inputs before they innervate L4 neurons at the onset of the critical period (Barkat et al, 2011; Friauf et al, 1990; Friauf & Shatz, 1991; Herrmann et al, 1994; Higashi et al, 2002; Molnar et al, 2003; Mukherjee & Kanold, 2022; Zhao et al, 2009). They are essential for the development of thalamocortical and corticocortical connections as well as patterning of the ocular dominance columns and barrels (Ghosh et al, 1990; Ghosh & Shatz, 1992, 1993; Kanold et al, 2003; Kanold & Luhmann, 2010; Kanold & Shatz, 2006; Molnar et al, 2020; Tolner et al, 2012).…”