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Mechanisms underlying reshuffling of visual responses by optogenetic stimulation in mice and monkeys

View ORCID ProfileA. Sanzeni, View ORCID ProfileA. Palmigiano, View ORCID ProfileT.H. Nguyen, J. Luo, View ORCID ProfileJ.J. Nassi, View ORCID ProfileJ.H. Reynolds, View ORCID ProfileM.H. Histed, View ORCID ProfileK.D. Miller, View ORCID ProfileN. Brunel
doi: https://doi.org/10.1101/2022.07.13.499597
A. Sanzeni
1Department of Computing Sciences, Bocconi University, Milan, Italy
2Center for Theoretical Neuroscience and Mortimer B Zuckerman Mind Brain Behavior Institute, Columbia University, New York, NY, USA
3Department of Neurobiology, Duke University, Durham, NC, USA
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  • For correspondence: alessandro.sanzeni@gmail.com
A. Palmigiano
2Center for Theoretical Neuroscience and Mortimer B Zuckerman Mind Brain Behavior Institute, Columbia University, New York, NY, USA
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T.H. Nguyen
2Center for Theoretical Neuroscience and Mortimer B Zuckerman Mind Brain Behavior Institute, Columbia University, New York, NY, USA
4Department of Physics, Columbia University, New York, NY, USA
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J. Luo
5Systems Neurobiology Laboratory, The Salk Institute for Biological Studies, La Jolla, CA, USA
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J.J. Nassi
5Systems Neurobiology Laboratory, The Salk Institute for Biological Studies, La Jolla, CA, USA
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J.H. Reynolds
5Systems Neurobiology Laboratory, The Salk Institute for Biological Studies, La Jolla, CA, USA
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M.H. Histed
6National Institute of Mental Health Intramural Program, NIH, Bethesda, MD, USA
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  • ORCID record for M.H. Histed
K.D. Miller
2Center for Theoretical Neuroscience and Mortimer B Zuckerman Mind Brain Behavior Institute, Columbia University, New York, NY, USA
7Department 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, Columbia University, New York City, NY, USA
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N. Brunel
3Department of Neurobiology, Duke University, Durham, NC, USA
8Department of Physics, Duke University, Durham, NC, USA
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Abstract

The ability to optogenetically perturb neural circuits opens an unprecedented window into mechanisms governing circuit function. We analyzed and theoretically modeled neuronal responses to visual and optogenetic inputs in mouse and monkey V1. In both species, optogenetic stimulation of excitatory neurons strongly modulated the activity of single neurons, yet had weak or no effects on the distribution of firing rates across the population. Thus, the optogenetic inputs reshuffled firing rates across the network. Key statistics of mouse and monkey responses lay on a continuum, with mice/monkeys occupying the low/high rate regions, respectively. We show that neuronal reshuffling emerges generically in randomly connected excitatory/inhibitory networks, provided the coupling strength (combination of recurrent coupling and external input) is sufficient that powerful inhibitory feedback cancels the mean optogenetic input. A more realistic model, distinguishing tuned visual vs. untuned optogenetic input in a structured network, reduces the coupling strength needed to explain reshuffling.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • This version of the manuscript includes: new theoretical results obtained in models with structured connectivity; improved fits of the model to the experimental data; substantial modifications of the text.

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 November 08, 2022.
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Mechanisms underlying reshuffling of visual responses by optogenetic stimulation in mice and monkeys
A. Sanzeni, A. Palmigiano, T.H. Nguyen, J. Luo, J.J. Nassi, J.H. Reynolds, M.H. Histed, K.D. Miller, N. Brunel
bioRxiv 2022.07.13.499597; doi: https://doi.org/10.1101/2022.07.13.499597
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Mechanisms underlying reshuffling of visual responses by optogenetic stimulation in mice and monkeys
A. Sanzeni, A. Palmigiano, T.H. Nguyen, J. Luo, J.J. Nassi, J.H. Reynolds, M.H. Histed, K.D. Miller, N. Brunel
bioRxiv 2022.07.13.499597; doi: https://doi.org/10.1101/2022.07.13.499597

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