Initiation and propagation of neuronal coactivation in the developing hippocampus

Correlated neuronal activity is ubiquitous in developing nervous systems, where it may introduce spatiotemporal coherence and contribute to the organization of functional circuits. In this report, we used voltage-sensitive dyes and optical imaging to examine the spatiotemporal pattern of a spontaneous network activity, giant depolarizing potentials (GDPs), in rat hippocampal slices during the first postnatal week. The propagation pattern of the GDP is closely correlated to the anatomical organization of the network. In the hilus, where mossy cells and interneurons are not organized in layers, GDPs propagate at the same velocity in all directions. In CA3 and CA1, the activation is synchronous along the axis of the pyramidal cells' dendritic tree. The velocity of wave propagation is significantly different in three hippocampal subfields: it is slowest in the hilus, faster in CA3, and fastest in CA1. The velocity of horizontal propagation (along the axis of the pyramidal layer) has a large variation from trial to trial, suggesting that the horizontal velocity is determined to some extent by dynamic network factors. Imaging revealed that each GDP event is initiated from a small focus. The location of the initiation focus differs from event to event. All together, our data suggest that GDP is a propagating excitation wave, initiated from a small site, and propagating to the whole hippocampus. The spatiotemporal patterns of the wave in CA3 and CA1 areas show better synchrony along the pyramidal cell dendritic trees and progressive activation along the axis of the pyramidal cell layer.