IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-49129-9.html
   My bibliography  Save this article

Coexistence of state, choice, and sensory integration coding in barrel cortex LII/III

Author

Listed:
  • Pierre-Marie Gardères

    (Université Paris Cité, Unit of Neural Circuits Dynamics and Decision Making
    Medical School, RWTH Aachen University)

  • Sébastien Gal

    (Université Paris Cité, Unit of Neural Circuits Dynamics and Decision Making)

  • Charly Rousseau

    (Université Paris Cité, Unit of Neural Circuits Dynamics and Decision Making)

  • Alexandre Mamane

    (Université Paris Cité, Unit of Neural Circuits Dynamics and Decision Making)

  • Dan Alin Ganea

    (Medical School, RWTH Aachen University
    Department of Biomedicine)

  • Florent Haiss

    (Université Paris Cité, Unit of Neural Circuits Dynamics and Decision Making)

Abstract

During perceptually guided decisions, correlates of choice are found as upstream as in the primary sensory areas. However, how well these choice signals align with early sensory representations, a prerequisite for their interpretation as feedforward substrates of perception, remains an open question. We designed a two alternative forced choice task (2AFC) in which male mice compared stimulation frequencies applied to two adjacent vibrissae. The optogenetic silencing of individual columns in the primary somatosensory cortex (wS1) resulted in predicted shifts of psychometric functions, demonstrating that perception depends on focal, early sensory representations. Functional imaging of layer II/III single neurons revealed mixed coding of stimuli, choices and engagement in the task. Neurons with multi-whisker suppression display improved sensory discrimination and had their activity increased during engagement in the task, enhancing selectively representation of the signals relevant to solving the task. From trial to trial, representation of stimuli and choice varied substantially, but mostly orthogonally to each other, suggesting that perceptual variability does not originate from wS1 fluctuations but rather from downstream areas. Together, our results highlight the role of primary sensory areas in forming a reliable sensory substrate that could be used for flexible downstream decision processes.

Suggested Citation

  • Pierre-Marie Gardères & Sébastien Gal & Charly Rousseau & Alexandre Mamane & Dan Alin Ganea & Florent Haiss, 2024. "Coexistence of state, choice, and sensory integration coding in barrel cortex LII/III," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49129-9
    DOI: 10.1038/s41467-024-49129-9
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-49129-9
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-49129-9?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. Sami El-Boustani & B. Semihcan Sermet & Georgios Foustoukos & Tess B. Oram & Ofer Yizhar & Carl C. H. Petersen, 2020. "Anatomically and functionally distinct thalamocortical inputs to primary and secondary mouse whisker somatosensory cortices," Nature Communications, Nature, vol. 11(1), pages 1-12, December.
    2. Timothy M. Otchy & Steffen B. E. Wolff & Juliana Y. Rhee & Cengiz Pehlevan & Risa Kawai & Alexandre Kempf & Sharon M. H. Gobes & Bence P. Ölveczky, 2015. "Acute off-target effects of neural circuit manipulations," Nature, Nature, vol. 528(7582), pages 358-363, December.
    3. Daniel Huber & Leopoldo Petreanu & Nima Ghitani & Sachin Ranade & Tomáš Hromádka & Zach Mainen & Karel Svoboda, 2008. "Sparse optical microstimulation in barrel cortex drives learned behaviour in freely moving mice," Nature, Nature, vol. 451(7174), pages 61-64, January.
    4. 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.
    5. Philipp Berens & Jeremy Freeman & Thomas Deneux & Nikolay Chenkov & Thomas McColgan & Artur Speiser & Jakob H Macke & Srinivas C Turaga & Patrick Mineault & Peter Rupprecht & Stephan Gerhard & Rainer , 2018. "Community-based benchmarking improves spike rate inference from two-photon calcium imaging data," PLOS Computational Biology, Public Library of Science, vol. 14(5), pages 1-13, May.
    6. Y. Kate Hong & Clay O. Lacefield & Chris C. Rodgers & Randy M. Bruno, 2018. "Sensation, movement and learning in the absence of barrel cortex," Nature, Nature, vol. 561(7724), pages 542-546, September.
    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. Lloyd E. Russell & Mehmet Fişek & Zidan Yang & Lynn Pei Tan & Adam M. Packer & Henry W. P. Dalgleish & Selmaan N. Chettih & Christopher D. Harvey & Michael Häusser, 2024. "The influence of cortical activity on perception depends on behavioral state and sensory context," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    2. 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.
    3. Matthijs N. Oude Lohuis & Jean L. Pie & Pietro Marchesi & Jorrit S. Montijn & Christiaan P. J. Kock & Cyriel M. A. Pennartz & Umberto Olcese, 2022. "Multisensory task demands temporally extend the causal requirement for visual cortex in perception," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    4. 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.
    5. Evan S. Schaffer & Neeli Mishra & Matthew R. Whiteway & Wenze Li & Michelle B. Vancura & Jason Freedman & Kripa B. Patel & Venkatakaushik Voleti & Liam Paninski & Elizabeth M. C. Hillman & L. F. Abbot, 2023. "The spatial and temporal structure of neural activity across the fly brain," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    6. Aniruddha Das & Sarah Holden & Julie Borovicka & Jacob Icardi & Abigail O’Niel & Ariel Chaklai & Davina Patel & Rushik Patel & Stefanie Kaech Petrie & Jacob Raber & Hod Dana, 2023. "Large-scale recording of neuronal activity in freely-moving mice at cellular resolution," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    7. Ravi Pancholi & Lauren Ryan & Simon Peron, 2023. "Learning in a sensory cortical microstimulation task is associated with elevated representational stability," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    8. 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.
    9. 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.
    10. Tristan G. Heintz & Antonio J. Hinojosa & Sina E. Dominiak & Leon Lagnado, 2022. "Opposite forms of adaptation in mouse visual cortex are controlled by distinct inhibitory microcircuits," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    11. Thomas C Südhof, 2016. "Truth in Science Publishing: A Personal Perspective," PLOS Biology, Public Library of Science, vol. 14(8), pages 1-4, August.
    12. Mohamad Motaharinia & Kim Gerrow & Roobina Boghozian & Emily White & Sun-Eui Choi & Kerry R. Delaney & Craig E. Brown, 2021. "Longitudinal functional imaging of VIP interneurons reveals sup-population specific effects of stroke that are rescued with chemogenetic therapy," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    13. 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.
    14. Gal Atlan & Noa Matosevich & Noa Peretz-Rivlin & Idit Marsh-Yvgi & Noam Zelinger & Eden Chen & Timna Kleinman & Noa Bleistein & Efrat Sheinbach & Maya Groysman & Yuval Nir & Ami Citri, 2024. "Claustrum neurons projecting to the anterior cingulate restrict engagement during sleep and behavior," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    15. Guo, Lei & Guo, Minxin & Wu, Youxi & Xu, Guizhi, 2023. "Specific neural coding of fMRI spiking neural network based on time coding," Chaos, Solitons & Fractals, Elsevier, vol. 174(C).
    16. Frank Gelens & Juho Äijälä & Louis Roberts & Misako Komatsu & Cem Uran & Michael A. Jensen & Kai J. Miller & Robin A. A. Ince & Max Garagnani & Martin Vinck & Andres Canales-Johnson, 2024. "Distributed representations of prediction error signals across the cortical hierarchy are synergistic," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    17. Drew C. Schreiner & Christian Cazares & Rafael Renteria & Christina M. Gremel, 2022. "Information normally considered task-irrelevant drives decision-making and affects premotor circuit recruitment," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    18. 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.
    19. Sebastian Reinartz & Arash Fassihi & Maria Ravera & Luciano Paz & Francesca Pulecchi & Marco Gigante & Mathew E. Diamond, 2024. "Direct contribution of the sensory cortex to the judgment of stimulus duration," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    20. Roberto Asín Achá & Dorit S. Hochbaum & Quico Spaen, 2020. "HNCcorr: combinatorial optimization for neuron identification," Annals of Operations Research, Springer, vol. 289(1), pages 5-32, June.

    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_s41467-024-49129-9. 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.