Deep and superficial single-cell dynamics during theta oscillations in CA1

Abstract

Theta oscillations (6-12Hz) are considered a major on-line mode of the hippocampus during spatial navigation. During encoding, it acts to channel information flow between regions across different oscillatory phases. The underlying synaptic currents in CA1 are generated by the CA3 and entorhinal inputs in interaction with local inhibition, but fine mechanisms of phase preference firing are still unknown. Recently, we and others have shown that CA1 is organized in sublayers, with deep and superficial principal cells displaying specific features during ongoing hippocampal rhythms. Here we investigate theta phase firing dynamics in CA1 using a combination of multisite and single-cell recordings with labelling in freely moving and anesthetized rats. For the first time, we confirmed histologically previous reports of different phase preference in deep and superficial CA1 pyramidal cells during ongoing theta oscillations. Calbindin-positive superficial cells fire earlier than calbindin-negative deep cells across theta cycles, closer to the CA3-generated stratum radiatum sink. Importantly, different responses between superficial and deep CA1 cells arise from dedicated intracellular dynamics governed by perisomatic inhibition. Our data identify mechanisms for phase-preference control of neuronal firing along the deep-superficial CA1 axis during theta oscillations.