Spontaneous Neuronal Activity in Developing Neocortical Networks: From Single Cells to Large-Scale Interactions.

Heiko J Luhmann,Maik C Stüttgen,Jenq-Wei Yang,Anne Sinning,Werner Kilb,Sergei Kirischuk,Vicente Reyes-Puerta

doi:10.3389/fncir.2016.00040

Abstract

Neuronal activity has been shown to be essential for the proper formation of neuronal circuits, affecting developmental processes like neurogenesis, migration, programmed cell death, cellular differentiation, formation of local and long-range axonal connections, synaptic plasticity or myelination. Accordingly, neocortical areas reveal distinct spontaneous and sensory-driven neuronal activity patterns already at early phases of development. At embryonic stages, when immature neurons start to develop voltage-dependent channels, spontaneous activity is highly synchronized within small neuronal networks and governed by electrical synaptic transmission. Subsequently, spontaneous activity patterns become more complex, involve larger networks and propagate over several neocortical areas. The developmental shift from local to large-scale network activity is accompanied by a gradual shift from electrical to chemical synaptic transmission with an initial excitatory action of chloride-gated channels activated by GABA, glycine and taurine. Transient neuronal populations in the subplate (SP) support temporary circuits that play an important role in tuning early neocortical activity and the formation of mature neuronal networks. Thus, early spontaneous activity patterns control the formation of developing networks in sensory cortices, and disturbances of these activity patterns may lead to long-lasting neuronal deficits.

Highlights

Neuronal populations have the ability to self-organize into networks that promote the generation of spontaneous, correlated neuronal activity already at earliest developmental stages
Spontaneous activity is organized in repetitive spike patterns, with a subgroup of neocortical neurons exhibiting a high degree of synaptic
This review aims to provide an update on the properties of spontaneous activity patterns in sensory neocortical areas during early stages of development and how these patterns are generated

Summary

INTRODUCTION

Neuronal populations have the ability to self-organize into networks that promote the generation of spontaneous, correlated neuronal activity already at earliest developmental stages. With the developmental shift from electrical to chemical synaptic transmission and increasing axonal connectivity, developing neuronal cultures generate repetitive burst discharges, which are synchronized over large fractions of the culture At this developmental stage, spontaneous activity is organized in repetitive spike patterns, with a subgroup of neocortical neurons exhibiting a high degree of synaptic. These studies offer the opportunity to obtain evidence for the causal relationship between network activity and the structural and functional development of the cerebral cortex Both in vitro and in vivo results strongly suggest that spontaneous synchronized burst activity represents a functional hallmark of developing neocortical networks. Since the developing cerebral cortex shows prominent anatomical and physiological changes during late prenatal and early postnatal stages, we will first briefly summarize the structure of the developing cerebral cortex

THE STRUCTURE OF THE DEVELOPING CEREBRAL CORTEX

SPONTANEOUS NEOCORTICAL ACTIVITY AT PRENATAL AND EARLY POSTNATAL STAGES

Findings

CURRENT CHALLENGES AND FUTURE DIRECTIONS