Dentate spikes and external control of hippocampal function

Mouse hippocampus CA1 place-cell discharge typically encodes current location, but during slow gamma dominance (SG(dom)), 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 (DS(M)) 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 (DS(L)) 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 DS(M) 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. DS(M) properties identify extrahippocampal control of SG(dom) and a cortico-hippocampal mechanism that switches between memory-related modes of information processing.