Dentate spikes and external control of hippocampal function

Dino Dvorak; Ain Chung; Eun Hye Park; André Antonio Fenton

doi:10.1016/j.celrep.2021.109497

Dentate spikes and external control of hippocampal function

Dino Dvorak, Ain Chung, Eun Hye Park, André Antonio Fenton

Neural Science

Research output: Contribution to journal › Article › peer-review

Abstract

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.

Original language	English (US)
Article number	109497
Journal	Cell Reports
Volume	36
Issue number	5
DOIs	https://doi.org/10.1016/j.celrep.2021.109497
State	Published - Aug 3 2021

Keywords

dentate gyrus
dentate spike
gamma
memory
neural coordination
oscillations
place cells
recollection
source localization
spike-field coupling

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology

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10.1016/j.celrep.2021.109497

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title = "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 SGdom 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 SGdom, 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 SGdom initiates. DSM properties identify extrahippocampal control of SGdom and a cortico-hippocampal mechanism that switches between memory-related modes of information processing.",

keywords = "dentate gyrus, dentate spike, gamma, memory, neural coordination, oscillations, place cells, recollection, source localization, spike-field coupling",

author = "Dino Dvorak and Ain Chung and Park, {Eun Hye} and Fenton, {Andr{\'e} Antonio}",

note = "Funding Information: This work was supported by NIH grants R01NS105472 and R01MH099128 . Publisher Copyright: {\textcopyright} 2021 The Authors",

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AU - Chung, Ain

AU - Park, Eun Hye

AU - Fenton, André Antonio

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N2 - 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 SGdom 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 SGdom, 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 SGdom initiates. DSM properties identify extrahippocampal control of SGdom and a cortico-hippocampal mechanism that switches between memory-related modes of information processing.

AB - 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 SGdom 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 SGdom, 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 SGdom initiates. DSM properties identify extrahippocampal control of SGdom and a cortico-hippocampal mechanism that switches between memory-related modes of information processing.

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Dentate spikes and external control of hippocampal function

Abstract

Keywords

ASJC Scopus subject areas

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