IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-48374-2.html
   My bibliography  Save this article

Primacy of vision shapes behavioral strategies and neural substrates of spatial navigation in marmoset hippocampus

Author

Listed:
  • Diego B. Piza

    (Western University
    Western University)

  • Benjamin W. Corrigan

    (Western University
    Western University
    York University)

  • Roberto A. Gulli

    (Columbia University)

  • Sonia Carmo

    (McGill University)

  • A. Claudio Cuello

    (McGill University)

  • Lyle Muller

    (Western University
    Western University)

  • Julio Martinez-Trujillo

    (Western University
    Western University
    Western University
    Western University)

Abstract

The role of the hippocampus in spatial navigation has been primarily studied in nocturnal mammals, such as rats, that lack many adaptations for daylight vision. Here we demonstrate that during 3D navigation, the common marmoset, a new world primate adapted to daylight, predominantly uses rapid head-gaze shifts for visual exploration while remaining stationary. During active locomotion marmosets stabilize the head, in contrast to rats that use low-velocity head movements to scan the environment as they locomote. Pyramidal neurons in the marmoset hippocampus CA3/CA1 regions predominantly show mixed selectivity for 3D spatial view, head direction, and place. Exclusive place selectivity is scarce. Inhibitory interneurons are predominantly mixed selective for angular head velocity and translation speed. Finally, we found theta phase resetting of local field potential oscillations triggered by head-gaze shifts. Our findings indicate that marmosets adapted to their daylight ecological niche by modifying exploration/navigation strategies and their corresponding hippocampal specializations.

Suggested Citation

  • Diego B. Piza & Benjamin W. Corrigan & Roberto A. Gulli & Sonia Carmo & A. Claudio Cuello & Lyle Muller & Julio Martinez-Trujillo, 2024. "Primacy of vision shapes behavioral strategies and neural substrates of spatial navigation in marmoset hippocampus," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48374-2
    DOI: 10.1038/s41467-024-48374-2
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-48374-2
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-48374-2?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Berens, Philipp, 2009. "CircStat: A MATLAB Toolbox for Circular Statistics," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 31(i10).
    2. Emilio Kropff & James E. Carmichael & May-Britt Moser & Edvard I. Moser, 2015. "Speed cells in the medial entorhinal cortex," Nature, Nature, vol. 523(7561), pages 419-424, July.
    3. Arne D. Ekstrom & Michael J. Kahana & Jeremy B. Caplan & Tony A. Fields & Eve A. Isham & Ehren L. Newman & Itzhak Fried, 2003. "Cellular networks underlying human spatial navigation," Nature, Nature, vol. 425(6954), pages 184-188, September.
    4. Omer Hazon & Victor H. Minces & David P. Tomàs & Surya Ganguli & Mark J. Schnitzer & Pablo E. Jercog, 2022. "Noise correlations in neural ensemble activity limit the accuracy of hippocampal spatial representations," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    5. Nathaniel J. Killian & Michael J. Jutras & Elizabeth A. Buffalo, 2012. "A map of visual space in the primate entorhinal cortex," Nature, Nature, vol. 491(7426), pages 761-764, November.
    6. Mattia Rigotti & Omri Barak & Melissa R. Warden & Xiao-Jing Wang & Nathaniel D. Daw & Earl K. Miller & Stefano Fusi, 2013. "The importance of mixed selectivity in complex cognitive tasks," Nature, Nature, vol. 497(7451), pages 585-590, May.
    7. Roddy M. Grieves & Selim Jedidi-Ayoub & Karyna Mishchanchuk & Anyi Liu & Sophie Renaudineau & Kate J. Jeffery, 2020. "The place-cell representation of volumetric space in rats," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    8. Chinmay S. Purandare & Shonali Dhingra & Rodrigo Rios & Cliff Vuong & Thuc To & Ayaka Hachisuka & Krishna Choudhary & Mayank R. Mehta, 2022. "Moving bar of light evokes vectorial spatial selectivity in the immobile rat hippocampus," Nature, Nature, vol. 602(7897), pages 461-467, February.
    9. 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.
    10. Emma R. Wood & Paul A. Dudchenko & Howard Eichenbaum, 1999. "The global record of memory in hippocampal neuronal activity," Nature, Nature, vol. 397(6720), pages 613-616, February.
    11. Mathias Franzius & Henning Sprekeler & Laurenz Wiskott, 2007. "Slowness and Sparseness Lead to Place, Head-Direction, and Spatial-View Cells," PLOS Computational Biology, Public Library of Science, vol. 3(8), pages 1-18, August.
    12. Thomas Andrillon & Yuval Nir & Chiara Cirelli & Giulio Tononi & Itzhak Fried, 2015. "Single-neuron activity and eye movements during human REM sleep and awake vision," Nature Communications, Nature, vol. 6(1), pages 1-10, November.
    13. Abhinav Goyal & Jonathan Miller & Salman E. Qasim & Andrew J. Watrous & Honghui Zhang & Joel M. Stein & Cory S. Inman & Robert E. Gross & Jon T. Willie & Bradley Lega & Jui-Jui Lin & Ashwini Sharan & , 2020. "Functionally distinct high and low theta oscillations in the human hippocampus," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
    14. P. E. Jercog & Y. Ahmadian & C. Woodruff & R. Deb-Sen & L. F. Abbott & E. R. Kandel, 2019. "Heading direction with respect to a reference point modulates place-cell activity," Nature Communications, Nature, vol. 10(1), pages 1-8, December.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Oliver Barnstedt & Petra Mocellin & Stefan Remy, 2024. "A hippocampus-accumbens code guides goal-directed appetitive behavior," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    2. Vincent Douchamps & Matteo Volo & Alessandro Torcini & Demian Battaglia & Romain Goutagny, 2024. "Gamma oscillatory complexity conveys behavioral information in hippocampal networks," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    3. Johnson Ying & Alexandra T. Keinath & Raphael Lavoie & Erika Vigneault & Salah El Mestikawy & Mark P. Brandon, 2022. "Disruption of the grid cell network in a mouse model of early Alzheimer’s disease," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    4. Soraya L. S. Dunn & Stephen M. Town & Jennifer K. Bizley & Daniel Bendor, 2022. "Behaviourally modulated hippocampal theta oscillations in the ferret persist during both locomotion and immobility," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    5. Sina Mackay & Thomas P. Reber & Marcel Bausch & Jan Boström & Christian E. Elger & Florian Mormann, 2024. "Concept and location neurons in the human brain provide the ‘what’ and ‘where’ in memory formation," Nature Communications, Nature, vol. 15(1), pages 1-9, December.
    6. Marije ter Wal & Juan Linde-Domingo & Julia Lifanov & Frédéric Roux & Luca D. Kolibius & Stephanie Gollwitzer & Johannes Lang & Hajo Hamer & David Rollings & Vijay Sawlani & Ramesh Chelvarajah & Bernh, 2021. "Theta rhythmicity governs human behavior and hippocampal signals during memory-dependent tasks," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    7. Joshua M. Diamond & Julio I. Chapeton & Weizhen Xie & Samantha N. Jackson & Sara K. Inati & Kareem A. Zaghloul, 2024. "Focal seizures induce spatiotemporally organized spiking activity in the human cortex," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    8. Isabella C. Wagner & Luise P. Graichen & Boryana Todorova & Andre Lüttig & David B. Omer & Matthias Stangl & Claus Lamm, 2023. "Entorhinal grid-like codes and time-locked network dynamics track others navigating through space," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    9. Kyerl Park & Yoonsoo Yeo & Kisung Shin & Jeehyun Kwag, 2024. "Egocentric neural representation of geometric vertex in the retrosplenial cortex," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    10. Jennifer B Tennessen & Marla M Holt & Brianna M Wright & M Bradley Hanson & Candice K Emmons & Deborah A Giles & Jeffrey T Hogan & Sheila J Thornton & Volker B Deecke, 2023. "Divergent foraging strategies between populations of sympatric matrilineal killer whales," Behavioral Ecology, International Society for Behavioral Ecology, vol. 34(3), pages 373-386.
    11. Thomas Schreiner & Marit Petzka & Tobias Staudigl & Bernhard P. Staresina, 2023. "Respiration modulates sleep oscillations and memory reactivation in humans," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    12. Matteo Saponati & Martin Vinck, 2023. "Sequence anticipation and spike-timing-dependent plasticity emerge from a predictive learning rule," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    13. Thomas Schreiner & Elisabeth Kaufmann & Soheyl Noachtar & Jan-Hinnerk Mehrkens & Tobias Staudigl, 2022. "The human thalamus orchestrates neocortical oscillations during NREM sleep," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    14. Nicolas Cazin & Martin Llofriu Alonso & Pablo Scleidorovich Chiodi & Tatiana Pelc & Bruce Harland & Alfredo Weitzenfeld & Jean-Marc Fellous & Peter Ford Dominey, 2019. "Reservoir computing model of prefrontal cortex creates novel combinations of previous navigation sequences from hippocampal place-cell replay with spatial reward propagation," PLOS Computational Biology, Public Library of Science, vol. 15(7), pages 1-32, July.
    15. Jan Weber & Anne-Kristin Solbakk & Alejandro O. Blenkmann & Anais Llorens & Ingrid Funderud & Sabine Leske & Pål Gunnar Larsson & Jugoslav Ivanovic & Robert T. Knight & Tor Endestad & Randolph F. Helf, 2024. "Ramping dynamics and theta oscillations reflect dissociable signatures during rule-guided human behavior," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    16. Pierre O. Boucher & Tian Wang & Laura Carceroni & Gary Kane & Krishna V. Shenoy & Chandramouli Chandrasekaran, 2023. "Initial conditions combine with sensory evidence to induce decision-related dynamics in premotor cortex," Nature Communications, Nature, vol. 14(1), pages 1-28, December.
    17. Celia M. Gagliardi & Marc E. Normandin & Alexandra T. Keinath & Joshua B. Julian & Matthew R. Lopez & Manuel-Miguel Ramos-Alvarez & Russell A. Epstein & Isabel A. Muzzio, 2024. "Distinct neural mechanisms for heading retrieval and context recognition in the hippocampus during spatial reorientation," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    18. Dominik P. Koller & Michael Schirner & Petra Ritter, 2024. "Human connectome topology directs cortical traveling waves and shapes frequency gradients," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    19. Alireza Saeedi & Kun Wang & Ghazaleh Nikpourian & Andreas Bartels & Nikos K. Logothetis & Nelson K. Totah & Masataka Watanabe, 2024. "Brightness illusions drive a neuronal response in the primary visual cortex under top-down modulation," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    20. Masakazu Agetsuma & Issei Sato & Yasuhiro R. Tanaka & Luis Carrillo-Reid & Atsushi Kasai & Atsushi Noritake & Yoshiyuki Arai & Miki Yoshitomo & Takashi Inagaki & Hiroshi Yukawa & Hitoshi Hashimoto & J, 2023. "Activity-dependent organization of prefrontal hub-networks for associative learning and signal transformation," Nature Communications, Nature, vol. 14(1), pages 1-22, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48374-2. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.