Layer-Specific GABAergic Control of Distinct Gamma Oscillations in the CA1 Hippocampus

Abstract

The temporary interaction of distinct gamma oscillators effects binding, association, and information routing. How independent gamma oscillations are generated and maintained by pyramidal cells and interneurons within a cortical circuit remains unknown. We recorded the spike timing of identified parvalbumin-expressing basket cells in the CA1 hippocampus of anesthetized rats and simultaneously detected layer-specific gamma oscillations using current-source-density analysis. Spike timing of basket cells tuned the phase and amplitude of gamma oscillations generated around stratum pyramidale, where basket cells selectively innervate pyramidal cells with GABAergic synapses. Basket cells did not contribute to gamma oscillations generated at the apical tuft of pyramidal cells. This gamma oscillation was selectively modulated by a subset of local GABAergic interneurons and by medial entorhinal cortex layer 3 neurons. The generation of independent and layer-specific gamma oscillations, implemented onto hippocampal pyramidal cells along their somato-dendritic axis, can be explained by selective axonal targeting and precisely controlled temporal firing of GABAergic interneurons.