Early patterns of electrical activity in the developing cerebral cortex of humans and rodents

During prenatal and early postnatal development, the cerebral cortex exhibits synchronized oscillatory network activity that is believed to be essential for the generation of neuronal cortical circuits. The nature and functional role of these early activity patterns are of central interest in neuroscience. Much of the research is performed in rodents and in vitro, but how closely do these model systems relate to the human fetal brain? In this review, we compare observations in humans with in vivo and in vitro rodent data, focusing on particular oscillatory activity patterns that share many common features: delta brushes, spindle bursts and spindle-like oscillations. There is considerable evidence that the basic functional properties of immature cortical networks are conserved through mammalian evolution, making the neonatal rodent an excellent model for studying early cortical activity and associated plasticity during the developmental period corresponding to the human fetal stage. This review is part of the INMED/TINS special issue Nature and nurture in brain development and neurological disorders, based on presentations at the annual INMED/TINS symposium (http://inmednet.com/).

Introduction

During development, about a trillion cortical neurons establish specific synaptic connections to produce highly organized functional cortical networks. There are many genetic determinants of early cortical connections [1], but spontaneous and sensory-driven activity is equally important for cortical development. Early electrical activity controls several developmental processes, including neuronal differentiation, migration, synaptogenesis, neurotransmitter specification and synaptic plasticity (for reviews, see Refs 2, 3, 4, 5, 6, 7, 8, 9). As in adults, early cortical activity is organized in distinct spatiotemporal patterns. However, the patterns of cortical activity during early developmental stages are remarkably different from those in adults. A variety of activity patterns has been described in the developing cortex of humans and in numerous animal models using various in vivo and in vitro preparations, experimental conditions and recording techniques. Many of these patterns share common features and probably reflect the same phenomena. In this paper, we will briefly review the various early cortical patterns, focusing on: (i) the oscillatory activity known as ‘delta brush’, identified in electroencephalographic recordings from human premature babies; (ii) recently described oscillatory patters of spindle bursts in the neonatal rat neocortex in vivo [10]; and (iii) ACh-dependent alpha–beta and beta–gamma oscillations in the neonatal rat and mouse cerebral cortex in vitro [11]. Remarkable similarities between these three patterns of activity suggest that the basic functional properties of immature cortical networks are conserved through mammalian evolution, making the neonatal rodent an excellent model for studying early cortical activity and associated plasticity during the developmental period corresponding to the fetal stage in humans.