Spatial organization and transitions of spontaneous neuronal activities in the developing sensory cortex

Abstract

The sensory cortex underlies our ability to perceive and interact with the external world. Sensory perceptions are controlled by specialized neuronal circuits established through fine‐tuning, which relies largely on neuronal activity during the development. Spontaneous neuronal activity is an essential driving force of neuronal circuit refinement. At early developmental stages, sensory cortices display spontaneous activities originating from the periphery and characterized by correlated firing arranged spatially according to the modality. The firing patterns are reorganized over time and become sparse, which is typical for the mature brain. This review focuses mainly on rodent sensory cortices. First, the features of the spontaneous activities during early postnatal stages are described. Then, the developmental changes in the spatial organization of the spontaneous activities and the transition mechanisms involved are discussed. The identification of the principles controlling the spatial organization of spontaneous activities in the developing sensory cortex is essential to understand the self‐organization process of neuronal circuits.

Epigenetic and Transcriptional Regulation of Spontaneous and Sensory Activity Dependent Programs During Neuronal Circuit Development

“…While such transcriptional and epigenetic transitions around the onset of sensory activity are just starting to be elucidated, it is well appreciated that this time window sees important shifts in the physiological patterns of spontaneous activity in somatosensory and visual thalamocortical networks ( Figure 4 , bottom panel; Colonnese and Phillips, 2018 ; Nakazawa and Iwasato, 2021 ). Generally, neurons initially fire asynchronously ( Figure 4 , bottom panel, labeled “transients”), but later coupling by synapses and gap junctions leads to more synchronous firing events where local neurons show highly correlated activity (e.g., neurons within a cortical column are correlated; Figure 4 , bottom panel, labeled “synchronous”).…”

“…Generally, neurons initially fire asynchronously ( Figure 4 , bottom panel, labeled “transients”), but later coupling by synapses and gap junctions leads to more synchronous firing events where local neurons show highly correlated activity (e.g., neurons within a cortical column are correlated; Figure 4 , bottom panel, labeled “synchronous”). Right before sensory transduction, network activity shifts from correlated seldom events (neurons fire together periodically with long periods of silence in between) to decorrelated continuous events ( Figure 4 , bottom panel, labeled “sparsified”), which are similar to network activity during adult processing, which ensues at the start of sensory experience ( Molnár et al, 2020 ; Nakazawa and Iwasato, 2021 ). This sparsification of cortical spontaneous activity has been proposed to rely on a reduced drive from the periphery ( Gribizis et al, 2019 ; Nakazawa et al, 2020 ), formation of intra-cortical circuitry and the onset of functional inhibition in cortex ( Romagnoni et al, 2020 ; Chini et al, 2021 ).…”

“…Overall, intrinsic spontaneous activity is now widely appreciated to be a key mechanism that predates extrinsic sensory inputs to instruct early steps of sensory circuit assembly ( Hooks and Chen, 2006 ; Kirkby et al, 2013 ; Thompson et al, 2017 ). The patterns and function of spontaneous activity have been thoroughly reviewed ( Arroyo and Feller, 2016 ; Leighton and Lohmann, 2016 ; Martini et al, 2021 ; Nakazawa and Iwasato, 2021 ). Here, we provide an overview of spontaneous activity in sensory systems, which is propaedeutic for the understanding of the molecular mechanisms downstream of spontaneous activity, discussed in the next chapter.…”

“…The presence of such spontaneous sensation and self-generated movement complicates the interpretation of early postnatal activity patterns, but spontaneous activity likely independent of these processes has been recently reported ( Nakazawa and Iwasato, 2021 ). A “patchwork-type” pattern of spontaneous activity, where both the neurons belonging to the same barrel as well as the thalamocortical axons (TCAs) projecting from a barreloid fire synchronously, and different barrels fire in a successive manner, was described in vivo in S1 from P0 to P5 ( Mizuno et al, 2018 , 2021 ; Nakazawa et al, 2020 ).…”

“…These waves are also relayed to the cortex and control the area size of the different sensory modalities by regulating TCA branching ( Moreno-Juan et al, 2017 ). At perinatal stages, localized whisker pad or thalamic stimulations elicit localized cortical responses, suggesting the present of a barrel “protomap.” In mice where these waves are specifically suppressed, such local responses activate larger cortical areas ( Antón-bolaños et al, 2019 ), implicating spontaneous thalamic activity in the creation of functional cortical maps ( Figure 1A ) that are then further refined by patchwork-type and sensory activity patterns after birth ( Antón-bolaños et al, 2019 ; Nakazawa and Iwasato, 2021 ).…”