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Unifying model for three forms of contextual modulation including feedback input from higher visual areas

View ORCID ProfileSerena Di Santo, Mario Dipoppa, Andreas Keller, Morgane Roth, Massimo Scanziani, Kenneth D. Miller
doi: https://doi.org/10.1101/2022.05.27.493753
Serena Di Santo
1Center for Theoretical Neuroscience, College of Physicians and Surgeons and Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University, New York City, NY 10027, USA
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  • ORCID record for Serena Di Santo
  • For correspondence: sd3362@columbia.edu
Mario Dipoppa
1Center for Theoretical Neuroscience, College of Physicians and Surgeons and Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University, New York City, NY 10027, USA
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Andreas Keller
2Institute of Molecular and Clinical Ophthalmology, Mittlere Strasse 91, CH-4031 Basel, Switzerland
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Morgane Roth
2Institute of Molecular and Clinical Ophthalmology, Mittlere Strasse 91, CH-4031 Basel, Switzerland
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Massimo Scanziani
3Department of Physiology, University of California, San Francisco, San Francisco, CA 94158-0444, USA
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Kenneth D. Miller
1Center for Theoretical Neuroscience, College of Physicians and Surgeons and Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University, New York City, NY 10027, USA
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Abstract

Neural responses to a localized visual stimulus are modulated by the content of its surrounding. This phenomenon manifests in several forms of contextual modulation, including three interrelated properties of the visual cortex: surround suppression, inverse response and surround facilitation. We devise a unified biologically realistic circuit model accounting for all these phenomena and show that i) surround suppression in L2/3 is only partially due to the recruitment of lateral inhibition; ii) long-range feedback projections are necessary for inverse response and iii) the width of the response profile in the feedback layer determines inverse size tuning. The model predicts the modulations induced by silencing somatostatin-expressing cells or higher visual areas or changing the stimulus contrast. These predictions are consistent with the experimental observations when available and can be tested in existing setups otherwise. We then show the robustness of the identified mechanisms in a model with three interneuron subclasses, built to fit the classical responses and able to predict inverse size-tuning curves.

Highlights

  • One model explains three different types of contextual modulation: (classical) surround suppression, (inverse) response to ‘holes’ in full field drifting gratings and cross orientation surround facilitation.

  • Feedback, feedforward and lateral inhibitory inputs contribute to classical surround suppression in L2/3 of mouse V1 in different amounts.

  • Observed responses to ‘holes’ in full field drifting gratings require long-range feedback projections.

  • Surround modulation to the response to ‘holes’ in full field drifting gratings requires an increase in the characteristic length scale of the spatial pattern of activity in higher visual areas.

  • The mechanisms uncovered by an analytically tractable model are also at work in a cell-type specific model that predicts response to a ‘hole’ stimulus.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-ND 4.0 International license.
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Posted May 28, 2022.
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Unifying model for three forms of contextual modulation including feedback input from higher visual areas
Serena Di Santo, Mario Dipoppa, Andreas Keller, Morgane Roth, Massimo Scanziani, Kenneth D. Miller
bioRxiv 2022.05.27.493753; doi: https://doi.org/10.1101/2022.05.27.493753
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Unifying model for three forms of contextual modulation including feedback input from higher visual areas
Serena Di Santo, Mario Dipoppa, Andreas Keller, Morgane Roth, Massimo Scanziani, Kenneth D. Miller
bioRxiv 2022.05.27.493753; doi: https://doi.org/10.1101/2022.05.27.493753

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