Neuronal activity controls the development of interneurons in the somatosensory cortex

Abstract

BACKGROUND Neuronal activity in cortical areas regulates neurodevelopment by interacting with defined genetic programs to shape the mature central nervous system. Electrical activity is conveyed to sensory cortical areas via intracortical and thalamocortical neurons, and includes oscillatory patterns that have been measured across cortical regions. OBJECTIVE In this work, we review the most recent findings about how electrical activity shapes the developmental assembly of functional circuitry in the somatosensory cortex, with an emphasis on interneuron maturation and integration. We include studies on the effect of various neurotransmitters and on the influence of thalamocortical afferent activity on circuit development. We additionally reviewed studies describing network activity patterns. METHODS We conducted an extensive literature search using both the PubMed and Google Scholar search engines. The following keywords were used in various iterations: “interneuron”, “somatosensory”, “development”, “activity”, “network patterns”, “thalamocortical”, “NMDA receptor”, “plasticity”. We additionally selected papers known to us from past reading, and those recommended to us by reviewers and members of our lab. RESULTS We reviewed a total of 132 articles that focused on the role of activity in interneuronal migration, maturation, and circuit development, as well as the source of electrical inputs and patterns of cortical activity in the somatosensory cortex. 79 of these papers included in this timely review were written between 2007 and 2016. CONCLUSIONS Neuronal activity shapes the developmental assembly of functional circuitry in the somatosensory cortical interneurons. This activity impacts nearly every aspect of development and acquisition of mature neuronal characteristics, and may contribute to changing phenotypes, altered transmitter expression, and plasticity in the adult. Progressively changing oscillatory network patterns contribute to this activity in the early postnatal period, although a direct requirement for specific patterns and origins of activity remains to be demonstrated.

Reduced Excitability and Increased Neurite Complexity of Cortical Interneurons in a Familial Mouse Model of Amyotrophic Lateral Sclerosis

“…However, a number of studies highlight increased excitability of cortical pyramidal neuron populations both in vivo and in vitro (Pieri et al, 2009 ; Fogarty et al, 2015 ), which could drive changes in the morphological development of cortical interneurons. The inhibitory neurite arbor can undergo activity-dependent structural remodeling (Bartolini et al, 2013 ; Babij and De Marco Garcia, 2016 ) and the level of network activity can produce subtle but significant changes to interneuron morphology (Schuemann et al, 2013 ). Importantly, in networks deprived of activity, cortical interneurons have been shown to extend collaterals beyond their normal projection range (Marik et al, 2010 ).…”

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

“…Similarly to excitatory neurons, cortical GABAergic interneurons also require neuronal activity, potentially including spontaneous activity, for early developmental processes, initially thought to be activity-independent ( Babij and De Marco Garcia, 2016 ; Wamsley and Fishell, 2017 ). Blocking neuronal activity by hyperpolarization was shown to influence migration, cortical layer allocation, dendritogenesis and axonogenesis of selected subtypes of GABAergic interneurons during specific time windows of postnatal development ( De Marco García et al, 2011 ).…”

The Role of Inhibitory Interneurons in Circuit Assembly and Refinement Across Sensory Cortices

“…At the neocortical level, two main types of neurons constitute the building blocks of cortical circuits: excitatory pyramidal neurons (Pyr) and inhibitory GABAergic interneurons (INs). Although they only constitute ~15%–20% of the neuronal cortical population (Anderson et al, 1997 ; Cauli et al, 1997 ; Gonchar and Burkhalter, 1997 ; Gupta et al, 2000 ; Kawaguchi, 2001 ; Butt et al, 2005 ; Miyoshi et al, 2007 ; Xu et al, 2010 ), inhibitory INs are essential for the proper development of cortical circuits (Babij and De Marco Garcia, 2016 ) and play multiple roles in sensory processing in the mature cortex (Tremblay et al, 2016 ). GABAergic INs can be classified based on their axonal morphological features and innervation profile in multiple subtypes (DeFelipe et al, 2013 ; Mihaljevic et al, 2019 ).…”