Spatiotemporal evolution of excitation and inhibition in the rat barrel cortex investigated with multielectrode arrays

Abstract

We investigated the spatiotemporal evolution of activity in the rat barrel cortex using multielectrode arrays (MEAs). In acute brain slices, field potentials were recorded simultaneously from 60 electrodes with high spatial and temporal resolution. This new technique allowed us to map functionally discrete barrels and to observe the interplay between the excitatory and inhibitory network. The local field potentials (LFPs) were elicited by focal electrical stimulation in layer 4 (L4). Excitation recorded in a single barrel was first confined to the stimulated barrel and subsequently spread in a columnar manner to layer 2/3 (L2/3). This excitation in L4 and lower L2/3 was followed by inhibition curtailing excitation to a short period lasting only approximately 2 ms. In the uppermost layer, a long-lasting (approximately 10 ms), laterally spreading band of excitation remained active. Blockade of GABAA-receptors resulted in a long-lasting and diffuse activation of L4 and lower L2/3 and abolition of activation of the upper L2/3. Thus inhibition not only shaped the spatial-temporal map of excitation in L4 and lower L2/3 but also resulted indirectly in an excitatory action in the superficial layers. Stimulation in L6 revealed a feedforward inhibition to L4 and subsequently an excitatory L6-L4-L6 loop. The complex interplay between excitation and inhibition opens two spatial windows of excitation in the infra- and supragranular layers. They may prepare the L5 pyramidal neuron for associating top-down input from other cortical regions with bottom-up input from the whisker pad to generate behaviorally relevant output.