How Do Electric Fields Coordinate Neuronal Migration and Maturation in the Developing Cortex?

Vera P Medvedeva,Alessandra Pierani

doi:10.3389/fcell.2020.580657

Abstract

During development the vast majority of cells that will later compose the mature cerebral cortex undergo extensive migration to reach their final position. In addition to intrinsically distinct migratory behaviors, cells encounter and respond to vastly different microenvironments. These range from axonal tracts to cell-dense matrices, electrically active regions and extracellular matrix components, which may all change overtime. Furthermore, migrating neurons themselves not only adapt to their microenvironment but also modify the local niche through cell-cell contacts, secreted factors and ions. In the radial dimension, the developing cortex is roughly divided into dense progenitor and cortical plate territories, and a less crowded intermediate zone. The cortical plate is bordered by the subplate and the marginal zone, which are populated by neurons with high electrical activity and characterized by sophisticated neuritic ramifications. Neuronal migration is influenced by these boundaries resulting in dramatic changes in migratory behaviors as well as morphology and electrical activity. Modifications in the levels of any of these parameters can lead to alterations and even arrest of migration. Recent work indicates that morphology and electrical activity of migrating neuron are interconnected and the aim of this review is to explore the extent of this connection. We will discuss on one hand how the response of migrating neurons is altered upon modification of their intrinsic electrical properties and whether, on the other hand, the electrical properties of the cellular environment can modify the morphology and electrical activity of migrating cortical neurons.

Highlights

Construction of the nervous system is achieved through a complex succession of developmental processes
The field of cortical development is starting to recognize the importance of ion flow for regulation of Electric Fields in the Developing Cortex early neuronal development: proliferation, migration and differentiation
We have discussed the distribution of ion channels canonically involved in the synaptic ion exchange machinery, in the attempt to decipher the principles of electric regulation of migration and maturation in early cortical development, before functional synaptogenesis occurs

Summary

Introduction

Construction of the nervous system is achieved through a complex succession of developmental processes. Two are known to predominantly occur at different developmental stages in the cerebral cortex, cell migration largely embryonically and synaptogenesis postnatally. Research on chemical cues and adhesion molecules guiding neuronal migration, shaping tissue architecture and synapse formation has shed light on the molecular mechanisms underlying migration as well as morphogenesis of dendrites and spines and have been extensively reviewed (Solecki, 2012; Arai and Pierani, 2014; Barber and Pierani, 2016; Ledda and Paratcha, 2017; Chighizola et al, 2019; Lanoue and Cooper, 2019). The field of cortical development is starting to recognize the importance of ion flow for regulation of Electric Fields in the Developing Cortex early neuronal development: proliferation, migration and differentiation. While nowadays EF is an emerging player in guiding orientation and speed of migrating neurons and in regulating neuronal morphology, it remains to be determined whether and how neuronal migration and morphology establishment are linked

Objectives

Conclusion