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

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  • 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
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    1. 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.
    2. Toshihiko Hosoya & Stephen A. Baccus & Markus Meister, 2005. "Dynamic predictive coding by the retina," Nature, Nature, vol. 436(7047), pages 71-77, July.
    3. 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.
    4. 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.
    5. 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.
    6. 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.
    7. 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.
    8. Bilal Haider & Michael Häusser & Matteo Carandini, 2013. "Inhibition dominates sensory responses in the awake cortex," Nature, Nature, vol. 493(7430), pages 97-100, January.
    9. 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.
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