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Targeted cortical stimulation reveals principles of cortical contextual interactions

View ORCID ProfileShen Wang, View ORCID ProfileAgostina Palmigiano, Kenneth D. Miller, View ORCID ProfileStephen D. Van Hooser
doi: https://doi.org/10.1101/2022.06.22.497254
Shen Wang
1Department of Biology; Waltham, MA, USA
2Volen Center for Complex Systems; Waltham, MA, USA
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  • ORCID record for Shen Wang
Agostina Palmigiano
4Center for Theoretical Neuroscience, Columbia University, New York, NY, USA
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Kenneth D. Miller
4Center for Theoretical Neuroscience, Columbia University, New York, NY, USA
5Dept. of Neuroscience, Swartz Program in Theoretical Neuroscience, Kavli Institute for Brain Science, College of Physicians and Surgeons and Mortimer B. Zuckerman Mind Brain Behavior Institute at Columbia University, New York, NY, USA
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Stephen D. Van Hooser
1Department of Biology; Waltham, MA, USA
2Volen Center for Complex Systems; Waltham, MA, USA
3Sloan-Swartz Center for Theoretical Neurobiology Brandeis University, Waltham, MA, USA
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  • For correspondence: vanhoosr@brandeis.edu
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Abstract

Cross-orientation suppression is a classic form of contextual normalization in visual cortex, yet the degree to which cortical circuits participate in the normalization computation is unclear. We visualized orientation maps of individual ferrets, and provided patterned optogenetic stimulation to both excitatory and inhibitory cells in orientation columns that either matched or were orthogonal to the preferred visual orientation of neurons recorded with electrodes. When visual or optogenetic stimulation of columns preferring one orientation was combined with optogenetic stimulation of columns preferring the orthogonal orientation, we observed less suppression than when orthogonal stimulation was provided visually, suggesting that cortical circuits do not provide a large fraction of visual cross-orientation suppression. Integration of visual and optogenetic signals was linear when neurons exhibited low firing rates and became sublinear when neurons exhibited higher firing rates. We probed the nature of sublinearities in cortex by examining the influence of optogenetic stimulation of cortical interneurons. We observed a range of responses, including evidence for paradoxical responses in which interneuron stimulation caused a decrease in inhibitory firing rate, presumably due to the withdrawal of recurrent excitation. These results are compatible with cortical circuits that exhibit strong recurrent excitation with stabilizing inhibition that provides normalization, albeit normalization that is too weak across columns to account for cross-orientation suppression.

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-NC-ND 4.0 International license.
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Posted June 24, 2022.
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Targeted cortical stimulation reveals principles of cortical contextual interactions
Shen Wang, Agostina Palmigiano, Kenneth D. Miller, Stephen D. Van Hooser
bioRxiv 2022.06.22.497254; doi: https://doi.org/10.1101/2022.06.22.497254
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Targeted cortical stimulation reveals principles of cortical contextual interactions
Shen Wang, Agostina Palmigiano, Kenneth D. Miller, Stephen D. Van Hooser
bioRxiv 2022.06.22.497254; doi: https://doi.org/10.1101/2022.06.22.497254

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