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Brightness illusions drive a neuronal response in the primary visual cortex under top-down modulation

Author

Listed:
  • Alireza Saeedi

    (Max Planck Institute for Biological Cybernetics
    Max Planck Institute for Neurobiology of Behavior – caesar)

  • Kun Wang

    (Max Planck Institute for Biological Cybernetics
    Songjiang District)

  • Ghazaleh Nikpourian

    (Max Planck Institute for Biological Cybernetics)

  • Andreas Bartels

    (Max Planck Institute for Biological Cybernetics
    University of Tübingen
    Bernstein Center for Computational Neuroscience)

  • Nikos K. Logothetis

    (Max Planck Institute for Biological Cybernetics
    Songjiang District
    University of Manchester)

  • Nelson K. Totah

    (Max Planck Institute for Biological Cybernetics
    University of Helsinki
    University of Helsinki
    University of Helsinki)

  • Masataka Watanabe

    (Max Planck Institute for Biological Cybernetics
    The University of Tokyo)

Abstract

Brightness illusions are a powerful tool in studying vision, yet their neural correlates are poorly understood. Based on a human paradigm, we presented illusory drifting gratings to mice. Primary visual cortex (V1) neurons responded to illusory gratings, matching their direction selectivity for real gratings, and they tracked the spatial phase offset between illusory and real gratings. Illusion responses were delayed compared to real gratings, in line with the theory that processing illusions requires feedback from higher visual areas (HVAs). We provide support for this theory by showing a reduced V1 response to illusions, but not real gratings, following HVAs optogenetic inhibition. Finally, we used the pupil response (PR) as an indirect perceptual report and showed that the mouse PR matches the human PR to perceived luminance changes. Our findings resolve debates over whether V1 neurons are involved in processing illusions and highlight the involvement of feedback from HVAs.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46885-6
    DOI: 10.1038/s41467-024-46885-6
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    References listed on IDEAS

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    1. Seung-Hee Lee & Alex C. Kwan & Yang Dan, 2014. "Interneuron subtypes and orientation tuning," Nature, Nature, vol. 508(7494), pages 1-2, April.
    2. Berens, Philipp, 2009. "CircStat: A MATLAB Toolbox for Circular Statistics," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 31(i10).
    3. Lauri Nurminen & Sam Merlin & Maryam Bijanzadeh & Frederick Federer & Alessandra Angelucci, 2018. "Top-down feedback controls spatial summation and response amplitude in primate visual cortex," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    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. Hillel Adesnik & William Bruns & Hiroki Taniguchi & Z. Josh Huang & Massimo Scanziani, 2012. "A neural circuit for spatial summation in visual cortex," Nature, Nature, vol. 490(7419), pages 226-231, October.
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