IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-28635-8.html
   My bibliography  Save this article

Opposite forms of adaptation in mouse visual cortex are controlled by distinct inhibitory microcircuits

Author

Listed:
  • Tristan G. Heintz

    (University of Sussex)

  • Antonio J. Hinojosa

    (University of Sussex)

  • Sina E. Dominiak

    (University of Sussex)

  • Leon Lagnado

    (University of Sussex)

Abstract

Sensory processing in the cortex adapts to the history of stimulation but the mechanisms are not understood. Imaging the primary visual cortex of mice we find here that an increase in stimulus contrast is not followed by a simple decrease in gain of pyramidal cells; as many cells increase gain to improve detection of a subsequent decrease in contrast. Depressing and sensitizing forms of adaptation also occur in different types of interneurons (PV, SST and VIP) and the net effect within individual pyramidal cells reflects the balance of PV inputs, driving depression, and a subset of SST interneurons driving sensitization. Changes in internal state associated with locomotion increase gain across the population of pyramidal cells while maintaining the balance between these opposite forms of plasticity, consistent with activation of both VIP->SST and SST->PV disinhibitory pathways. These results reveal how different inhibitory microcircuits adjust the gain of pyramidal cells signalling changes in stimulus strength.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28635-8
    DOI: 10.1038/s41467-022-28635-8
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-28635-8
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-28635-8?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. Bilal Haider & Michael Häusser & Matteo Carandini, 2013. "Inhibition dominates sensory responses in the awake cortex," Nature, Nature, vol. 493(7430), pages 97-100, January.
    2. Stelios M. Smirnakis & Michael J. Berry & David K. Warland & William Bialek & Markus Meister, 1997. "Adaptation of retinal processing to image contrast and spatial scale," Nature, Nature, vol. 386(6620), pages 69-73, March.
    3. 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.
    4. Nathan R. Wilson & Caroline A. Runyan & Forea L. Wang & Mriganka Sur, 2012. "Division and subtraction by distinct cortical inhibitory networks in vivo," Nature, Nature, vol. 488(7411), pages 343-348, August.
    5. Toshihiko Hosoya & Stephen A. Baccus & Markus Meister, 2005. "Dynamic predictive coding by the retina," Nature, Nature, vol. 436(7047), pages 71-77, July.
    6. Aylin Cimenser & Kenneth D Miller, 2014. "The Effects of Short-Term Synaptic Depression at Thalamocortical Synapses on Orientation Tuning in Cat V1," PLOS ONE, Public Library of Science, vol. 9(8), pages 1-18, August.
    7. B. Haider & M. Häusser & M. Carandini, 2013. "Correction: Corrigendum: Inhibition dominates sensory responses in awake cortex," Nature, Nature, vol. 500(7464), pages 612-612, August.
    8. Thomas Deneux & Attila Kaszas & Gergely Szalay & Gergely Katona & Tamás Lakner & Amiram Grinvald & Balázs Rózsa & Ivo Vanzetta, 2016. "Accurate spike estimation from noisy calcium signals for ultrafast three-dimensional imaging of large neuronal populations in vivo," Nature Communications, Nature, vol. 7(1), pages 1-17, November.
    9. 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.
    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. Manoj Kumar & Gregory Handy & Stylianos Kouvaros & Yanjun Zhao & Lovisa Ljungqvist Brinson & Eric Wei & Brandon Bizup & Brent Doiron & Thanos Tzounopoulos, 2023. "Cell-type-specific plasticity of inhibitory interneurons in the rehabilitation of auditory cortex after peripheral damage," Nature Communications, Nature, vol. 14(1), pages 1-23, December.
    2. Panagiotis Fotiadis & Matthew Cieslak & Xiaosong He & Lorenzo Caciagli & Mathieu Ouellet & Theodore D. Satterthwaite & Russell T. Shinohara & Dani S. Bassett, 2023. "Myelination and excitation-inhibition balance synergistically shape structure-function coupling across the human cortex," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    3. Miguel Maravall & Rasmus S Petersen & Adrienne L Fairhall & Ehsan Arabzadeh & Mathew E Diamond, 2007. "Shifts in Coding Properties and Maintenance of Information Transmission during Adaptation in Barrel Cortex," PLOS Biology, Public Library of Science, vol. 5(2), pages 1-12, January.
    4. 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.
    5. Marcus H C Howlett & Robert G Smith & Maarten Kamermans, 2017. "A novel mechanism of cone photoreceptor adaptation," PLOS Biology, Public Library of Science, vol. 15(4), pages 1-28, April.
    6. Yue Liu & Xiao-Jing Wang, 2024. "Flexible gating between subspaces in a neural network model of internally guided task switching," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    7. Jian K Liu & Tim Gollisch, 2015. "Spike-Triggered Covariance Analysis Reveals Phenomenological Diversity of Contrast Adaptation in the Retina," PLOS Computational Biology, Public Library of Science, vol. 11(7), pages 1-30, July.
    8. Sorinel A Oprisan & Xandre Clementsmith & Tamas Tompa & Antonieta Lavin, 2019. "Dopamine receptor antagonists effects on low-dimensional attractors of local field potentials in optogenetic mice," PLOS ONE, Public Library of Science, vol. 14(10), pages 1-39, October.
    9. Matthias S Keil & Agata Lapedriza & David Masip & Jordi Vitria, 2008. "Preferred Spatial Frequencies for Human Face Processing Are Associated with Optimal Class Discrimination in the Machine," PLOS ONE, Public Library of Science, vol. 3(7), pages 1-5, July.
    10. Panna Hegedüs & Bálint Király & Dániel Schlingloff & Victoria Lyakhova & Anna Velencei & Írisz Szabó & Márton I. Mayer & Zsofia Zelenak & Gábor Nyiri & Balázs Hangya, 2024. "Parvalbumin-expressing basal forebrain neurons mediate learning from negative experience," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    11. Mark L Ioffe & Michael J Berry II, 2017. "The structured ‘low temperature’ phase of the retinal population code," PLOS Computational Biology, Public Library of Science, vol. 13(10), pages 1-31, October.
    12. Joshua H Goldwyn & Bradley R Slabe & Joseph B Travers & David Terman, 2018. "Gain control with A-type potassium current: IA as a switch between divisive and subtractive inhibition," PLOS Computational Biology, Public Library of Science, vol. 14(7), pages 1-23, July.
    13. Joanna Bryson, 2008. "Embodiment versus memetics," Mind & Society: Cognitive Studies in Economics and Social Sciences, Springer;Fondazione Rosselli, vol. 7(1), pages 77-94, June.
    14. Ruxandra Barzan & Beyza Bozkurt & Mohammadreza M. Nejad & Sandra T. Süß & Tatjana Surdin & Hanna Böke & Katharina Spoida & Zohre Azimi & Michelle Grömmke & Dennis Eickelbeck & Melanie D. Mark & Lennar, 2024. "Gain control of sensory input across polysynaptic circuitries in mouse visual cortex by a single G protein-coupled receptor type (5-HT2A)," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    15. Matthias S Keil, 2009. "“I Look in Your Eyes, Honey”: Internal Face Features Induce Spatial Frequency Preference for Human Face Processing," PLOS Computational Biology, Public Library of Science, vol. 5(3), pages 1-13, March.
    16. Krishnamurthy V. Vemuru, 2022. "Implementation of the Canny Edge Detector Using a Spiking Neural Network," Future Internet, MDPI, vol. 14(12), pages 1-12, December.
    17. Johannes Friedrich & Pengcheng Zhou & Liam Paninski, 2017. "Fast online deconvolution of calcium imaging data," PLOS Computational Biology, Public Library of Science, vol. 13(3), pages 1-26, March.
    18. 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.
    19. Jason S Prentice & Olivier Marre & Mark L Ioffe & Adrianna R Loback & Gašper Tkačik & Michael J Berry II, 2016. "Error-Robust Modes of the Retinal Population Code," PLOS Computational Biology, Public Library of Science, vol. 12(11), pages 1-32, November.
    20. Joseph D Taylor & Samuel Winnall & Alain Nogaret, 2020. "Estimation of neuron parameters from imperfect observations," PLOS Computational Biology, Public Library of Science, vol. 16(7), pages 1-22, July.

    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:13:y:2022:i:1:d:10.1038_s41467-022-28635-8. 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.