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Optogenetic frequency scrambling of hippocampal theta oscillations dissociates working memory retrieval from hippocampal spatiotemporal codes

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  • Guillaume Etter

    (McGill University & Douglas Mental Health University Institute)

  • Suzanne Veldt

    (McGill University & Douglas Mental Health University Institute)

  • Jisoo Choi

    (McGill University & Douglas Mental Health University Institute)

  • Sylvain Williams

    (McGill University & Douglas Mental Health University Institute)

Abstract

The precise temporal coordination of activity in the brain is thought to be fundamental for memory function. Inhibitory neurons in the medial septum provide a prominent source of innervation to the hippocampus and play a major role in controlling hippocampal theta (~8 Hz) oscillations. While pharmacological inhibition of medial septal neurons is known to disrupt memory, the exact role of septal inhibitory neurons in regulating hippocampal representations and memory is not fully understood. Here, we dissociate the role of theta rhythms in spatiotemporal coding and memory using an all-optical interrogation and recording approach. We find that optogenetic frequency scrambling stimulations abolish theta oscillations and modulate a portion of neurons in the hippocampus. Such stimulation decreased episodic and working memory retrieval while leaving hippocampal spatiotemporal codes intact. Our study suggests that theta rhythms play an essential role in memory but may not be necessary for hippocampal spatiotemporal codes.

Suggested Citation

  • Guillaume Etter & Suzanne Veldt & Jisoo Choi & Sylvain Williams, 2023. "Optogenetic frequency scrambling of hippocampal theta oscillations dissociates working memory retrieval from hippocampal spatiotemporal codes," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-35825-5
    DOI: 10.1038/s41467-023-35825-5
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    References listed on IDEAS

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    1. Franziska Bender & Maria Gorbati & Marta Carus Cadavieco & Natalia Denisova & Xiaojie Gao & Constance Holman & Tatiana Korotkova & Alexey Ponomarenko, 2015. "Theta oscillations regulate the speed of locomotion via a hippocampus to lateral septum pathway," Nature Communications, Nature, vol. 6(1), pages 1-11, December.
    2. Ueli Rutishauser & Ian B. Ross & Adam N. Mamelak & Erin M. Schuman, 2010. "Human memory strength is predicted by theta-frequency phase-locking of single neurons," Nature, Nature, vol. 464(7290), pages 903-907, April.
    3. Jason J. Moore & Jesse D. Cushman & Lavanya Acharya & Briana Popeney & Mayank R. Mehta, 2021. "Linking hippocampal multiplexed tuning, Hebbian plasticity and navigation," Nature, Nature, vol. 599(7885), pages 442-448, November.
    4. Guillaume Etter & Suzanne van der Veldt & Frédéric Manseau & Iman Zarrinkoub & Emilie Trillaud-Doppia & Sylvain Williams, 2019. "Optogenetic gamma stimulation rescues memory impairments in an Alzheimer’s disease mouse model," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    5. Suzanne van der Veldt & Guillaume Etter & Coralie-Anne Mosser & Frédéric Manseau & Sylvain Williams, 2021. "Conjunctive spatial and self-motion codes are topographically organized in the GABAergic cells of the lateral septum," PLOS Biology, Public Library of Science, vol. 19(8), pages 1-36, August.
    6. Flavio Donato & Santiago Belluco Rompani & Pico Caroni, 2013. "Parvalbumin-expressing basket-cell network plasticity induced by experience regulates adult learning," Nature, Nature, vol. 504(7479), pages 272-276, December.
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    1. Masato Tsuji & Yuto Nishizuka & Kazuo Emoto, 2023. "Threat gates visual aversion via theta activity in Tachykinergic neurons," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    2. Lou T. Blanpain & Eric R. Cole & Emily Chen & James K. Park & Michael Y. Walelign & Robert E. Gross & Brian T. Cabaniss & Jon T. Willie & Annabelle C. Singer, 2024. "Multisensory flicker modulates widespread brain networks and reduces interictal epileptiform discharges," Nature Communications, Nature, vol. 15(1), pages 1-22, December.

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