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Offline hippocampal reactivation during dentate spikes supports flexible memory.

Publication ,  Journal Article
McHugh, SB; Lopes-Dos-Santos, V; Castelli, M; Gava, GP; Thompson, SE; Tam, SKE; Hartwich, K; Perry, B; Toth, R; Denison, T; Sharott, A; Dupret, D
Published in: Neuron
November 2024

Stabilizing new memories requires coordinated neuronal spiking activity during sleep. Hippocampal sharp-wave ripples (SWRs) in the cornu ammonis (CA) region and dentate spikes (DSs) in the dentate gyrus (DG) are prime candidate network events for supporting this offline process. SWRs have been studied extensively, but the contribution of DSs remains unclear. By combining triple-ensemble (DG-CA3-CA1) recordings and closed-loop optogenetics in mice, we show that, like SWRs, DSs synchronize spiking across DG and CA principal cells to reactivate population-level patterns of neuronal coactivity expressed during prior waking experience. Notably, the population coactivity structure in DSs is more diverse and higher dimensional than that seen during SWRs. Importantly, suppressing DG granule cell spiking selectively during DSs impairs subsequent flexible memory performance during multi-object recognition tasks and associated hippocampal patterns of neuronal coactivity. We conclude that DSs constitute a second offline network event central to hippocampal population dynamics serving memory-guided behavior.

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Published In

Neuron

DOI

EISSN

1097-4199

ISSN

0896-6273

Publication Date

November 2024

Volume

112

Issue

22

Start / End Page

3768 / 3781.e8

Related Subject Headings

  • Optogenetics
  • Neurons
  • Neurology & Neurosurgery
  • Mice, Inbred C57BL
  • Mice
  • Memory
  • Male
  • Hippocampus
  • Dentate Gyrus
  • Animals
 

Citation

APA
Chicago
ICMJE
MLA
NLM
McHugh, S. B., Lopes-Dos-Santos, V., Castelli, M., Gava, G. P., Thompson, S. E., Tam, S. K. E., … Dupret, D. (2024). Offline hippocampal reactivation during dentate spikes supports flexible memory. Neuron, 112(22), 3768-3781.e8. https://doi.org/10.1016/j.neuron.2024.08.022
McHugh, Stephen B., Vítor Lopes-Dos-Santos, Manfredi Castelli, Giuseppe P. Gava, Sophie E. Thompson, Shu K. E. Tam, Katja Hartwich, et al. “Offline hippocampal reactivation during dentate spikes supports flexible memory.Neuron 112, no. 22 (November 2024): 3768-3781.e8. https://doi.org/10.1016/j.neuron.2024.08.022.
McHugh SB, Lopes-Dos-Santos V, Castelli M, Gava GP, Thompson SE, Tam SKE, et al. Offline hippocampal reactivation during dentate spikes supports flexible memory. Neuron. 2024 Nov;112(22):3768-3781.e8.
McHugh, Stephen B., et al. “Offline hippocampal reactivation during dentate spikes supports flexible memory.Neuron, vol. 112, no. 22, Nov. 2024, pp. 3768-3781.e8. Epmc, doi:10.1016/j.neuron.2024.08.022.
McHugh SB, Lopes-Dos-Santos V, Castelli M, Gava GP, Thompson SE, Tam SKE, Hartwich K, Perry B, Toth R, Denison T, Sharott A, Dupret D. Offline hippocampal reactivation during dentate spikes supports flexible memory. Neuron. 2024 Nov;112(22):3768-3781.e8.
Journal cover image

Published In

Neuron

DOI

EISSN

1097-4199

ISSN

0896-6273

Publication Date

November 2024

Volume

112

Issue

22

Start / End Page

3768 / 3781.e8

Related Subject Headings

  • Optogenetics
  • Neurons
  • Neurology & Neurosurgery
  • Mice, Inbred C57BL
  • Mice
  • Memory
  • Male
  • Hippocampus
  • Dentate Gyrus
  • Animals