Short reviewNeurotransmitters and gap junctions in developing neural circuits
Introduction
The adult vertebrate central nervous system (CNS) is characterized by highly organized neuronal circuits (complexity emerges). The developmental mechanisms that are responsible for the formation of these complex networks are classified in two categories: activity-dependent and activity-independent [55]. Traditionally, the earliest stages of circuit development (including establishment of cell phenotype, target selection, and the distribution of initial synaptic connections) are thought to depend solely on the genetic program of the cell — that is, independent of neural activity. The subsequent stages of development, namely synaptic refinement, are guided by neuronal activity driven by sensory inputs, and therefore is termed activity-dependent.
There is growing evidence, however, that prior to the maturation of afferent inputs, central structures rely on the spontaneous generation of neural activity to drive the early steps of circuit formation. Infusion of agents that block action potentials at the retinogenicualte synapse prevents the normal patterning of retinal ganglion cell axon arbors, indicating that before vision, neural activity profoundly influences the development of early circuits 124, 149. Action-potential based activity is also required for thalamic axons to select their appropriate targets in cortex [24].
Spontaneous activity has been observed in a wide variety of circuits within the developing CNS [177]. This activity can be measured in cells as spontaneous firing of action potentials and/or spontaneous transient increases in intracellular calcium concentration. In many of these circuits, such as the developing spinal cord, hippocampus, retina, and neocortex, the spontaneous activity is correlated over tens to hundreds of neurons (reviewed in Ref. [46]). The coupling responsible for these correlations can be extracellular, e.g., through neurotransmitter release, or intracellular via gap junctions. Here, we review the roles of synaptic activity and gap junctional communication in generating structured activity patterns in two spontaneously active circuits, the developing retina and the developing neocortex.
Section snippets
Neurotransmitters and gap junctions in the developing retina: retinal waves
Prior to photoreceptor maturation and eye opening, retinal ganglion cells (RGC), the projecting neurons on the retina, periodically fire bursts of action potentials. This spontaneous rhythmic activity was first measured in fetal rat pups and found to be highly correlated among neighboring ganglion cells [53]. Both extracellular recording using a multielectrode array [103]and imaging of calcium transients associated with bursts of action potentials 47, 170have revealed that these spontaneous
Gap junctions in the developing neocortex
As discussed in Section 2the early activity patterns in the developing retina are transmitted to the visual thalamus [109]and from there correlated activity is very likely to be relayed to the visual cortex. Although it is not known yet whether there is a causal relationship between retinal waves and biochemically mediated neuronal domains in the visual cortex 77, 78, both forms of coordinated activity may play a role in defining the boundaries of a crude pattern of functional domains in the
Development of chemical synaptic transmission in the neocortex
Having discussed the development and regulation as well as possible functions of gap junctions in the neocortex, we would like to dedicate the final chapters of this article to a brief review of chemical synaptogenesis and some of the roles of different neurotransmitters during neocortical development.
Synaptogenesis and circuit formation in the cerebral cortex can roughly be divided into two principal stages. The first stage involves the generation of neurons and glia and the migration of these
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