IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v16y2025i1d10.1038_s41467-025-56733-w.html
   My bibliography  Save this article

Deciphering neuronal variability across states reveals dynamic sensory encoding

Author

Listed:
  • Shailaja Akella

    (Allen Institute)

  • Peter Ledochowitsch

    (Allen Institute
    Canaery)

  • Joshua H. Siegle

    (Allen Institute)

  • Hannah Belski

    (Allen Institute)

  • Daniel D. Denman

    (Allen Institute
    University of Colorado)

  • Michael A. Buice

    (Allen Institute)

  • Severine Durand

    (Allen Institute)

  • Christof Koch

    (Allen Institute)

  • Shawn R. Olsen

    (Allen Institute)

  • Xiaoxuan Jia

    (Tsinghua University
    Tsinghua University)

Abstract

Influenced by non-stationary factors such as brain states and behavior, neurons exhibit substantial response variability even to identical stimuli. However, it remains unclear how their relative impact on neuronal variability evolves over time. To address this question, we designed an encoding model conditioned on latent states to partition variability in the mouse visual cortex across internal brain dynamics, behavior, and external visual stimulus. Applying a hidden Markov model to local field potentials, we consistently identified three distinct oscillation states, each with a unique variability profile. Regression models within each state revealed a dynamic composition of factors influencing spiking variability, with the dominant factor switching within seconds. The state-conditioned regression model uncovered extensive diversity in source contributions across units, varying in accordance with anatomical hierarchy and internal state. This heterogeneity in encoding underscores the importance of partitioning variability over time, particularly when considering the influence of non-stationary factors on sensory processing.

Suggested Citation

  • Shailaja Akella & Peter Ledochowitsch & Joshua H. Siegle & Hannah Belski & Daniel D. Denman & Michael A. Buice & Severine Durand & Christof Koch & Shawn R. Olsen & Xiaoxuan Jia, 2025. "Deciphering neuronal variability across states reveals dynamic sensory encoding," Nature Communications, Nature, vol. 16(1), pages 1-22, December.
  • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-56733-w
    DOI: 10.1038/s41467-025-56733-w
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-025-56733-w
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-025-56733-w?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. Shawn R. Olsen & Dante S. Bortone & Hillel Adesnik & Massimo Scanziani, 2012. "Gain control by layer six in cortical circuits of vision," Nature, Nature, vol. 483(7387), pages 47-52, March.
    2. Valerio Mante & David Sussillo & Krishna V. Shenoy & William T. Newsome, 2013. "Context-dependent computation by recurrent dynamics in prefrontal cortex," Nature, Nature, vol. 503(7474), pages 78-84, November.
    3. Joshua H. Siegle & Xiaoxuan Jia & Séverine Durand & Sam Gale & Corbett Bennett & Nile Graddis & Greggory Heller & Tamina K. Ramirez & Hannah Choi & Jennifer A. Luviano & Peter A. Groblewski & Ruweida , 2021. "Survey of spiking in the mouse visual system reveals functional hierarchy," Nature, Nature, vol. 592(7852), pages 86-92, April.
    4. Anderson Speed & Joseph Del Rosario & Navid Mikail & Bilal Haider, 2020. "Spatial attention enhances network, cellular and subthreshold responses in mouse visual cortex," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    5. James Trousdale & Yu Hu & Eric Shea-Brown & Krešimir Josić, 2012. "Impact of Network Structure and Cellular Response on Spike Time Correlations," PLOS Computational Biology, Public Library of Science, vol. 8(3), pages 1-15, March.
    6. Jonathan W. Pillow & Jonathon Shlens & Liam Paninski & Alexander Sher & Alan M. Litke & E. J. Chichilnisky & Eero P. Simoncelli, 2008. "Spatio-temporal correlations and visual signalling in a complete neuronal population," Nature, Nature, vol. 454(7207), pages 995-999, August.
    7. Roxana Zeraati & Yan-Liang Shi & Nicholas A. Steinmetz & Marc A. Gieselmann & Alexander Thiele & Tirin Moore & Anna Levina & Tatiana A. Engel, 2023. "Intrinsic timescales in the visual cortex change with selective attention and reflect spatial connectivity," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    8. Jeanette A Mumford & Jean-Baptiste Poline & Russell A Poldrack, 2015. "Orthogonalization of Regressors in fMRI Models," PLOS ONE, Public Library of Science, vol. 10(4), pages 1-11, April.
    9. Julie A. Harris & Stefan Mihalas & Karla E. Hirokawa & Jennifer D. Whitesell & Hannah Choi & Amy Bernard & Phillip Bohn & Shiella Caldejon & Linzy Casal & Andrew Cho & Aaron Feiner & David Feng & Nath, 2019. "Hierarchical organization of cortical and thalamic connectivity," Nature, Nature, vol. 575(7781), pages 195-202, November.
    10. Nicholas A. Steinmetz & Peter Zatka-Haas & Matteo Carandini & Kenneth D. Harris, 2019. "Distributed coding of choice, action and engagement across the mouse brain," Nature, Nature, vol. 576(7786), pages 266-273, December.
    11. James J. Jun & Nicholas A. Steinmetz & Joshua H. Siegle & Daniel J. Denman & Marius Bauza & Brian Barbarits & Albert K. Lee & Costas A. Anastassiou & Alexandru Andrei & Çağatay Aydın & Mladen Barbic &, 2017. "Fully integrated silicon probes for high-density recording of neural activity," Nature, Nature, vol. 551(7679), pages 232-236, November.
    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. Edward A. B. Horrocks & Fabio R. Rodrigues & Aman B. Saleem, 2024. "Flexible neural population dynamics govern the speed and stability of sensory encoding in mouse visual cortex," Nature Communications, Nature, vol. 15(1), pages 1-23, December.
    2. Jérémie Sibille & Carolin Gehr & Jonathan I. Benichov & Hymavathy Balasubramanian & Kai Lun Teh & Tatiana Lupashina & Daniela Vallentin & Jens Kremkow, 2022. "High-density electrode recordings reveal strong and specific connections between retinal ganglion cells and midbrain neurons," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    3. Yina Wei & Anirban Nandi & Xiaoxuan Jia & Joshua H. Siegle & Daniel Denman & Soo Yeun Lee & Anatoly Buchin & Werner Geit & Clayton P. Mosher & Shawn Olsen & Costas A. Anastassiou, 2023. "Associations between in vitro, in vivo and in silico cell classes in mouse primary visual cortex," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    4. Yanjie Wang & Zhaonan Chen & Guofen Ma & Lizhao Wang & Yanmei Liu & Meiling Qin & Xiang Fei & Yifan Wu & Min Xu & Siyu Zhang, 2023. "A frontal transcallosal inhibition loop mediates interhemispheric balance in visuospatial processing," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    5. Wen-Hao Zhang & Si Wu & Krešimir Josić & Brent Doiron, 2023. "Sampling-based Bayesian inference in recurrent circuits of stochastic spiking neurons," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    6. Adam R. Pines & Bart Larsen & Zaixu Cui & Valerie J. Sydnor & Maxwell A. Bertolero & Azeez Adebimpe & Aaron F. Alexander-Bloch & Christos Davatzikos & Damien A. Fair & Ruben C. Gur & Raquel E. Gur & H, 2022. "Dissociable multi-scale patterns of development in personalized brain networks," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    7. Kenneth W. Latimer & David J. Freedman, 2023. "Low-dimensional encoding of decisions in parietal cortex reflects long-term training history," Nature Communications, Nature, vol. 14(1), pages 1-24, December.
    8. Jean-Paul Noel & Edoardo Balzani & Cristina Savin & Dora E. Angelaki, 2024. "Context-invariant beliefs are supported by dynamic reconfiguration of single unit functional connectivity in prefrontal cortex of male macaques," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    9. Ashok Litwin-Kumar & Maurice J Chacron & Brent Doiron, 2012. "The Spatial Structure of Stimuli Shapes the Timescale of Correlations in Population Spiking Activity," PLOS Computational Biology, Public Library of Science, vol. 8(9), pages 1-15, September.
    10. Noel Federman & Sebastián A. Romano & Macarena Amigo-Duran & Lucca Salomon & Antonia Marin-Burgin, 2024. "Acquisition of non-olfactory encoding improves odour discrimination in olfactory cortex," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    11. Daniel Durstewitz, 2017. "A state space approach for piecewise-linear recurrent neural networks for identifying computational dynamics from neural measurements," PLOS Computational Biology, Public Library of Science, vol. 13(6), pages 1-33, June.
    12. João D. Semedo & Anna I. Jasper & Amin Zandvakili & Aravind Krishna & Amir Aschner & Christian K. Machens & Adam Kohn & Byron M. Yu, 2022. "Feedforward and feedback interactions between visual cortical areas use different population activity patterns," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    13. Shinichiro Kira & Houman Safaai & Ari S. Morcos & Stefano Panzeri & Christopher D. Harvey, 2023. "A distributed and efficient population code of mixed selectivity neurons for flexible navigation decisions," Nature Communications, Nature, vol. 14(1), pages 1-28, December.
    14. Longyu Ma & Lupeng Yue & Shuting Liu & Shi Xu & Jifu Tong & Xiaoyan Sun & Li Su & Shuang Cui & Feng-Yu Liu & You Wan & Ming Yi, 2024. "A distinct neuronal ensemble of prelimbic cortex mediates spontaneous pain in rats with peripheral inflammation," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    15. Kotaro Ishizu & Shosuke Nishimoto & Yutaro Ueoka & Akihiro Funamizu, 2024. "Localized and global representation of prior value, sensory evidence, and choice in male mouse cerebral cortex," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    16. Guihua Xiao & Yeyi Cai & Yuanlong Zhang & Jingyu Xie & Lifan Wu & Hao Xie & Jiamin Wu & Qionghai Dai, 2024. "Mesoscale neuronal granular trial variability in vivo illustrated by nonlinear recurrent network in silico," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    17. David Hocker & Il Memming Park, 2019. "Myopic control of neural dynamics," PLOS Computational Biology, Public Library of Science, vol. 15(3), pages 1-24, March.
    18. Javier G. Orlandi & Mohammad Abdolrahmani & Ryo Aoki & Dmitry R. Lyamzin & Andrea Benucci, 2023. "Distributed context-dependent choice information in mouse posterior cortex," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    19. Nir Moneta & Mona M. Garvert & Hauke R. Heekeren & Nicolas W. Schuck, 2023. "Task state representations in vmPFC mediate relevant and irrelevant value signals and their behavioral influence," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    20. Diego E. Hernandez & Andrei Ciuparu & Pedro Garcia da Silva & Cristina M. Velasquez & Benjamin Rebouillat & Michael D. Gross & Martin B. Davis & Honggoo Chae & Raul C. Muresan & Dinu F. Albeanu, 2025. "Fast updating feedback from piriform cortex to the olfactory bulb relays multimodal identity and reward contingency signals during rule-reversal," Nature Communications, Nature, vol. 16(1), pages 1-20, 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:16:y:2025:i:1:d:10.1038_s41467-025-56733-w. 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.