IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-46012-5.html
   My bibliography  Save this article

Gamma oscillatory complexity conveys behavioral information in hippocampal networks

Author

Listed:
  • Vincent Douchamps

    (Université de Strasbourg, Laboratoire de Neurosciences Cognitives et Adaptatives (LNCA), CNRS, UMR 7364)

  • Matteo Volo

    (Université Claude Bernard Lyon 1, Institut National de la Santé et de la Recherche Médicale, Stem Cell and Brain Research Institute
    CY Cergy Paris Université, Laboratoire de Physique Théorique et Modélisation (LPTM), CNRS, UMR 8089)

  • Alessandro Torcini

    (CY Cergy Paris Université, Laboratoire de Physique Théorique et Modélisation (LPTM), CNRS, UMR 8089
    CNR - Consiglio Nazionale delle Ricerche, Istituto dei Sistemi Complessi)

  • Demian Battaglia

    (Université de Strasbourg, Laboratoire de Neurosciences Cognitives et Adaptatives (LNCA), CNRS, UMR 7364
    Aix-Marseille Université, Institut de Neurosciences des Systèmes (INS), INSERM
    University of Strasbourg Institute for Advanced Studies (USIAS))

  • Romain Goutagny

    (Université de Strasbourg, Laboratoire de Neurosciences Cognitives et Adaptatives (LNCA), CNRS, UMR 7364)

Abstract

The hippocampus and entorhinal cortex exhibit rich oscillatory patterns critical for cognitive functions. In the hippocampal region CA1, specific gamma-frequency oscillations, timed at different phases of the ongoing theta rhythm, are hypothesized to facilitate the integration of information from varied sources and contribute to distinct cognitive processes. Here, we show that gamma elements -a multidimensional characterization of transient gamma oscillatory episodes- occur at any frequency or phase relative to the ongoing theta rhythm across all CA1 layers in male mice. Despite their low power and stochastic-like nature, individual gamma elements still carry behavior-related information and computational modeling suggests that they reflect neuronal firing. Our findings challenge the idea of rigid gamma sub-bands, showing that behavior shapes ensembles of irregular gamma elements that evolve with learning and depend on hippocampal layers. Widespread gamma diversity, beyond randomness, may thus reflect complexity, likely functional but invisible to classic average-based analyses.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46012-5
    DOI: 10.1038/s41467-024-46012-5
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-46012-5
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-46012-5?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. 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.
    3. Joeri Bordes & Lucas Miranda & Maya Reinhardt & Sowmya Narayan & Jakob Hartmann & Emily L. Newman & Lea Maria Brix & Lotte Doeselaar & Clara Engelhardt & Larissa Dillmann & Shiladitya Mitra & Kerry J., 2023. "Automatically annotated motion tracking identifies a distinct social behavioral profile following chronic social defeat stress," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    4. Laura Lee Colgin & Tobias Denninger & Marianne Fyhn & Torkel Hafting & Tora Bonnevie & Ole Jensen & May-Britt Moser & Edvard I. Moser, 2009. "Frequency of gamma oscillations routes flow of information in the hippocampus," Nature, Nature, vol. 462(7271), pages 353-357, November.
    5. Wang, Yung-Hung & Yeh, Chien-Hung & Young, Hsu-Wen Vincent & Hu, Kun & Lo, Men-Tzung, 2014. "On the computational complexity of the empirical mode decomposition algorithm," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 400(C), pages 159-167.
    6. Thomas Hainmueller & Marlene Bartos, 2018. "Parallel emergence of stable and dynamic memory engrams in the hippocampus," Nature, Nature, vol. 558(7709), pages 292-296, June.
    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. Chinnakkaruppan Adaikkan & Justin Joseph & Georgios Foustoukos & Jun Wang & Denis Polygalov & Roman Boehringer & Steven J. Middleton & Arthur J. Y. Huang & Li-Huei Tsai & Thomas J. McHugh, 2024. "Silencing CA1 pyramidal cells output reveals the role of feedback inhibition in hippocampal oscillations," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    2. 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.
    3. M. Agustina Frechou & Sunaina S. Martin & Kelsey D. McDermott & Evan A. Huaman & Şölen Gökhan & Wolfgang A. Tomé & Ruben Coen-Cagli & J. Tiago Gonçalves, 2024. "Adult neurogenesis improves spatial information encoding in the mouse hippocampus," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    4. 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.
    5. Natalia Grion & Athena Akrami & Yangfang Zuo & Federico Stella & Mathew E Diamond, 2016. "Coherence between Rat Sensorimotor System and Hippocampus Is Enhanced during Tactile Discrimination," PLOS Biology, Public Library of Science, vol. 14(2), pages 1-26, February.
    6. Luis M. Franco & Michael J. Goard, 2024. "Differential stability of task variable representations in retrosplenial cortex," Nature Communications, Nature, vol. 15(1), pages 1-17, 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. Hannah Muysers & Hung-Ling Chen & Johannes Hahn & Shani Folschweiller & Torfi Sigurdsson & Jonas-Frederic Sauer & Marlene Bartos, 2024. "A persistent prefrontal reference frame across time and task rules," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    9. Dongxiao Niu & Yi Liang & Wei-Chiang Hong, 2017. "Wind Speed Forecasting Based on EMD and GRNN Optimized by FOA," Energies, MDPI, vol. 10(12), pages 1-18, December.
    10. Taylor J. Malone & Nai-Wen Tien & Yan Ma & Lian Cui & Shangru Lyu & Garret Wang & Duc Nguyen & Kai Zhang & Maxym V. Myroshnychenko & Jean Tyan & Joshua A. Gordon & David A. Kupferschmidt & Yi Gu, 2024. "A consistent map in the medial entorhinal cortex supports spatial memory," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    11. 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.
    12. 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.
    13. Wei Sun & Ming Duan, 2019. "Analysis and Forecasting of the Carbon Price in China’s Regional Carbon Markets Based on Fast Ensemble Empirical Mode Decomposition, Phase Space Reconstruction, and an Improved Extreme Learning Machin," Energies, MDPI, vol. 12(2), pages 1-27, January.
    14. 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.
    15. Seetha Krishnan & Chad Heer & Chery Cherian & Mark E. J. Sheffield, 2022. "Reward expectation extinction restructures and degrades CA1 spatial maps through loss of a dopaminergic reward proximity signal," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    16. Pengcheng Zhou & Shawn D Burton & Adam C Snyder & Matthew A Smith & Nathaniel N Urban & Robert E Kass, 2015. "Establishing a Statistical Link between Network Oscillations and Neural Synchrony," PLOS Computational Biology, Public Library of Science, vol. 11(10), pages 1-25, October.
    17. 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.
    18. 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.
    19. Sun, Wei & Zhang, Chongchong, 2018. "Analysis and forecasting of the carbon price using multi—resolution singular value decomposition and extreme learning machine optimized by adaptive whale optimization algorithm," Applied Energy, Elsevier, vol. 231(C), pages 1354-1371.
    20. 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.

    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_s41467-024-46012-5. 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.