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 SG 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 medial entorhinal cortex II (MECII)-> dentate gyrus (DG) inputs promote SG(dom) and change excitation-inhibition coordinated discharge in DG, CA3, and CA1, whereas type 1 (DSL) events initiated by lateral entorhinal cortex II (LECII)-> DG inputs do not. Just before SG(dom), LECII-originating SG oscillations in DG and CA3-originating SG 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 SG(dom) initiates. DSM properties identify extrahippocampal control of SG(dom) and a cortico-hippocampal mechanism that switches between memory-related modes of information processing.