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Brain region-specific gain modulation of place cells by VIP neurons

Author

Listed:
  • Nora Lenkey

    (University of Oslo)

  • Anna Christina Garvert

    (University of Oslo)

  • Máté Neubrandt

    (University of Oslo)

  • Birgit Kriener

    (University of Oslo)

  • Koen Vervaeke

    (University of Oslo)

Abstract

Gain modulation allows neurons to dynamically adjust their responsiveness to inputs without changing selectivity. While well-characterized in sensory areas, its role in higher-order brain regions governing spatial navigation and memory is unclear. Here, we used all-optical methods in mice performing a spatial task to demonstrate that vasoactive-intestinal peptide (VIP)-expressing neurons selectively control the gain of place cells and other cell types in the retrosplenial cortex (RSC) through disinhibition. Optogenetic manipulation revealed that this disinhibition, while broadly affecting network activity, selectively amplifies in-field place cell activity, improving spatial coding accuracy. In contrast, VIP neurons in the hippocampus have minimal impact on place field gain. Notably, simulations indicate that the benefit of gain modulation for RSC place cells is large compared to hippocampal place cells due to their much higher out-of-field activity and, therefore, lower signal-to-noise ratio. Here, we show an area-specific VIP-mediated gain control, enhancing spatial coding and, potentially, memory formation.

Suggested Citation

  • Nora Lenkey & Anna Christina Garvert & Máté Neubrandt & Birgit Kriener & Koen Vervaeke, 2025. "Brain region-specific gain modulation of place cells by VIP neurons," Nature Communications, Nature, vol. 16(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-60679-4
    DOI: 10.1038/s41467-025-60679-4
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    References listed on IDEAS

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    1. Dun Mao & Steffen Kandler & Bruce L. McNaughton & Vincent Bonin, 2017. "Sparse orthogonal population representation of spatial context in the retrosplenial cortex," Nature Communications, Nature, vol. 8(1), pages 1-9, December.
    2. Joshua Obermayer & Antonio Luchicchi & Tim S. Heistek & Sybren F. Kloet & Huub Terra & Bastiaan Bruinsma & Ouissame Mnie-Filali & Christian Kortleven & Anna A. Galakhova & Ayoub J. Khalil & Tim Kroon , 2019. "Prefrontal cortical ChAT-VIP interneurons provide local excitation by cholinergic synaptic transmission and control attention," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
    3. Ruggiero Francavilla & Vincent Villette & Xiao Luo & Simon Chamberland & Einer Muñoz-Pino & Olivier Camiré & Kristina Wagner & Viktor Kis & Peter Somogyi & Lisa Topolnik, 2018. "Connectivity and network state-dependent recruitment of long-range VIP-GABAergic neurons in the mouse hippocampus," Nature Communications, Nature, vol. 9(1), pages 1-17, December.
    4. Ed S. Lein & Michael J. Hawrylycz & Nancy Ao & Mikael Ayres & Amy Bensinger & Amy Bernard & Andrew F. Boe & Mark S. Boguski & Kevin S. Brockway & Emi J. Byrnes & Lin Chen & Li Chen & Tsuey-Ming Chen &, 2007. "Genome-wide atlas of gene expression in the adult mouse brain," Nature, Nature, vol. 445(7124), pages 168-176, January.
    5. F. Walker & M. Möck & M. Feyerabend & J. Guy & R. J. Wagener & D. Schubert & J. F. Staiger & M. Witte, 2016. "Parvalbumin- and vasoactive intestinal polypeptide-expressing neocortical interneurons impose differential inhibition on Martinotti cells," Nature Communications, Nature, vol. 7(1), pages 1-8, December.
    6. Hyun-Jae Pi & Balázs Hangya & Duda Kvitsiani & Joshua I. Sanders & Z. Josh Huang & Adam Kepecs, 2013. "Cortical interneurons that specialize in disinhibitory control," Nature, Nature, vol. 503(7477), pages 521-524, November.
    7. 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.
    8. Tsai-Wen Chen & Trevor J. Wardill & Yi Sun & Stefan R. Pulver & Sabine L. Renninger & Amy Baohan & Eric R. Schreiter & Rex A. Kerr & Michael B. Orger & Vivek Jayaraman & Loren L. Looger & Karel Svobod, 2013. "Ultrasensitive fluorescent proteins for imaging neuronal activity," Nature, Nature, vol. 499(7458), pages 295-300, July.
    9. Christopher D. Harvey & Philip Coen & David W. Tank, 2012. "Choice-specific sequences in parietal cortex during a virtual-navigation decision task," Nature, Nature, vol. 484(7392), pages 62-68, April.
    Full references (including those not matched with items on IDEAS)

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