Differential modulation of CA1 and dentate gyrus interneurons during exploration of novel environments

Abstract

Parallel recordings of hippocampal principal cells and interneurons were obtained as rats foraged in familiar and adjacent, novel environments. Firing rates of each cell type were assessed as a function of spatial location. Many CA1 interneurons exhibited large decreases in activity in the novel compared with the familiar environment. Dentate gyrus interneurons, however, were much more likely to exhibit large increases in firing in the novel environment. Neither effect was correlated with basic interneuron discharge properties such as degree of theta modulation, baseline firing rate or degree of spatially modulated discharge. Both CA1 and dentate gyrus interneuron rate changes extended into regions of the familiar environment bordering the novel environment. Principal cells in CA1 and dentate gyrus exhibited similar patterns of place specific activity each being indicative of incorporation of novel spatial information into the spatial representation of the familiar environment. The data indicate that inhibitory networks in the CA1 and dentate gyrus areas are modulated in a divergent fashion during the acquisition of novel spatial information and that interneuron activities can be used to detect those regions of an environment subject to redistribution of principal cell spatial activity patterns.