Dentate spikes and external control of hippocampal function

Abstract

Mouse hippocampus CA1 place-cell discharge typically encodes current location but during slow gamma dominance (SGdom), when slow gamma oscillations (30-50 Hz) dominate mid-frequency gamma oscillations (70-90 Hz) in CA1 local field potentials, CA1 discharge switches to represent distant recollected locations. We report that dentate spike type 2 (DSM) events initiated by MECII[->]DG inputs promote SGdom and change excitation-inhibition coordinated discharge in DG, CA3, and CA1, whereas type 1 (DSL) events initiated by LECII[->]DG inputs do not. Just before SGdom, LECII-originating slow gamma oscillations in dentate gyrus and CA3-originating slow gamma oscillations in CA1 phase and frequency synchronize at the DSM peak when discharge within DG and CA3 increases to promote excitation-inhibition cofiring within and across the DG[->]CA3[->]CA1 pathway. This optimizes discharge for the 5-10 ms DG-to-CA1 neuro-transmission that coincides with SGdom. DSM properties identify extrahippocampal control of SGdom, and a cortico-hippocampal mechanism that switches between memory-related modes of information processing.