A Disinhibitory Circuit for Contextual Modulation in Primary Visual Cortex
Context guides perception by influencing stimulus saliency. Accordingly, in visual cortex, responses to a stimulus are modulated by context, the visual scene surrounding the stimulus. Responses are suppressed when stimulus and surround are similar but not when they differ. The underlying mechanisms...
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| Published in | Neuron (Cambridge, Mass.) Vol. 108; no. 6; pp. 1181 - 1193.e8 |
|---|---|
| Main Authors | , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
23.12.2020
Elsevier Limited |
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| Online Access | Get full text |
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| Abstract | Context guides perception by influencing stimulus saliency. Accordingly, in visual cortex, responses to a stimulus are modulated by context, the visual scene surrounding the stimulus. Responses are suppressed when stimulus and surround are similar but not when they differ. The underlying mechanisms remain unclear. Here, we use optical recordings, manipulations, and computational modeling to show that disinhibitory circuits consisting of vasoactive intestinal peptide (VIP)-expressing and somatostatin (SOM)-expressing inhibitory neurons modulate responses in mouse visual cortex depending on similarity between stimulus and surround, primarily by modulating recurrent excitation. When stimulus and surround are similar, VIP neurons are inactive, and activity of SOM neurons leads to suppression of excitatory neurons. However, when stimulus and surround differ, VIP neurons are active, inhibiting SOM neurons, which leads to relief of excitatory neurons from suppression. We have identified a canonical cortical disinhibitory circuit that contributes to contextual modulation and may regulate perceptual saliency.
•Visual context modulates the response of SOM oppositely to all other V1 neurons•The VIP-SOM disinhibitory circuit controls the impact of context on V1 responses•The VIP-SOM disinhibitory circuit controls V1 by modulating recurrent excitation•As we predict by modeling, silencing of VIP neurons reduces contextual modulation
Context provides meaning by influencing perception. In the visual world, context is the visual environment surrounding a visual scene. Here, Keller et al. report that a canonical disinhibitory circuit controls the response of mouse visual cortex to a visual stimulus depending on the context within which that stimulus is presented. |
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| AbstractList | Context guides perception by influencing stimulus saliency. Accordingly, in visual cortex, responses to a stimulus are modulated by context, the visual scene surrounding the stimulus. Responses are suppressed when stimulus and surround are similar but not when they differ. The underlying mechanisms remain unclear. Here, we use optical recordings, manipulations, and computational modeling to show that disinhibitory circuits consisting of vasoactive intestinal peptide (VIP)-expressing and somatostatin (SOM)-expressing inhibitory neurons modulate responses in mouse visual cortex depending on similarity between stimulus and surround, primarily by modulating recurrent excitation. When stimulus and surround are similar, VIP neurons are inactive, and activity of SOM neurons leads to suppression of excitatory neurons. However, when stimulus and surround differ, VIP neurons are active, inhibiting SOM neurons, which leads to relief of excitatory neurons from suppression. We have identified a canonical cortical disinhibitory circuit that contributes to contextual modulation and may regulate perceptual saliency. Context guides perception by influencing stimulus saliency. Accordingly, in visual cortex, responses to a stimulus are modulated by context, the visual scene surrounding the stimulus. Responses are suppressed when stimulus and surround are similar but not when they differ. The underlying mechanisms remain unclear. Here we use optical recordings, manipulations, and computational modelling to show that disinhibitory circuits consisting of vasoactive intestinal peptide expressing (VIP) and somatostatin expressing (SOM) inhibitory neurons modulate responses in mouse visual cortex depending on similarity between stimulus and surround, primarily by modulating recurrent excitation. When stimulus and surround are similar, VIP neurons are inactive and activity of SOM neurons leads to suppression of excitatory neurons. However, when stimulus and surround differ, VIP neurons are active, inhibiting SOM neurons, which leads to relief of excitatory neurons from suppression. We have identified a canonical cortical disinhibitory circuit which contributes to contextual modulation and may regulate perceptual saliency. Context provides meaning by influencing perception. In the visual world, context is the visual environment surrounding a visual scene. Here, Keller et al. report that a canonical disinhibitory circuit controls the response of mouse visual cortex to a visual stimulus depending on the context within which that stimulus is presented. SummaryContext guides perception by influencing stimulus saliency. Accordingly, in visual cortex, responses to a stimulus are modulated by context, the visual scene surrounding the stimulus. Responses are suppressed when stimulus and surround are similar but not when they differ. The underlying mechanisms remain unclear. Here, we use optical recordings, manipulations, and computational modeling to show that disinhibitory circuits consisting of vasoactive intestinal peptide (VIP)-expressing and somatostatin (SOM)-expressing inhibitory neurons modulate responses in mouse visual cortex depending on similarity between stimulus and surround, primarily by modulating recurrent excitation. When stimulus and surround are similar, VIP neurons are inactive, and activity of SOM neurons leads to suppression of excitatory neurons. However, when stimulus and surround differ, VIP neurons are active, inhibiting SOM neurons, which leads to relief of excitatory neurons from suppression. We have identified a canonical cortical disinhibitory circuit that contributes to contextual modulation and may regulate perceptual saliency. Context guides perception by influencing stimulus saliency. Accordingly, in visual cortex, responses to a stimulus are modulated by context, the visual scene surrounding the stimulus. Responses are suppressed when stimulus and surround are similar but not when they differ. The underlying mechanisms remain unclear. Here, we use optical recordings, manipulations, and computational modeling to show that disinhibitory circuits consisting of vasoactive intestinal peptide (VIP)-expressing and somatostatin (SOM)-expressing inhibitory neurons modulate responses in mouse visual cortex depending on similarity between stimulus and surround, primarily by modulating recurrent excitation. When stimulus and surround are similar, VIP neurons are inactive, and activity of SOM neurons leads to suppression of excitatory neurons. However, when stimulus and surround differ, VIP neurons are active, inhibiting SOM neurons, which leads to relief of excitatory neurons from suppression. We have identified a canonical cortical disinhibitory circuit that contributes to contextual modulation and may regulate perceptual saliency. •Visual context modulates the response of SOM oppositely to all other V1 neurons•The VIP-SOM disinhibitory circuit controls the impact of context on V1 responses•The VIP-SOM disinhibitory circuit controls V1 by modulating recurrent excitation•As we predict by modeling, silencing of VIP neurons reduces contextual modulation Context provides meaning by influencing perception. In the visual world, context is the visual environment surrounding a visual scene. Here, Keller et al. report that a canonical disinhibitory circuit controls the response of mouse visual cortex to a visual stimulus depending on the context within which that stimulus is presented. |
| Author | Keller, Andreas J. Scanziani, Massimo Dipoppa, Mario Miller, Kenneth D. Roth, Morgane M. Caudill, Matthew S. Ingrosso, Alessandro |
| AuthorAffiliation | 9 These authors contributed equally 2 Center for Neural Circuits and Behavior, Neurobiology Section and Department of Neuroscience, University of California San Diego, La Jolla, California 92093-0634, USA 7 Present Address: Quantitative Life Sciences, The Abdus Salam International Centre for Theoretical Physics - ICTP, Trieste 34151, Italy 5 Dept. 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, New York, USA 4 Center for Theoretical Neuroscience, College of Physicians and Surgeons and Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University, New York City, New York 10027, USA 6 Present Address: Department of Neuroscience, Baylor College of Medicine, Houston, Texas 77030, USA, and Jan and Dan Duncan Neurological Research Institute at Texas Children’s Hospital, Houston, Texas 77030, USA 1 Department of Ph |
| AuthorAffiliation_xml | – name: 9 These authors contributed equally – name: 1 Department of Physiology, University of California San Francisco, San Francisco, California 94158-0444, USA – name: 6 Present Address: Department of Neuroscience, Baylor College of Medicine, Houston, Texas 77030, USA, and Jan and Dan Duncan Neurological Research Institute at Texas Children’s Hospital, Houston, Texas 77030, USA – name: 8 These authors contributed equally – name: 3 Howard Hughes Medical Institute, University of California San Francisco, San Francisco, California, USA – name: 4 Center for Theoretical Neuroscience, College of Physicians and Surgeons and Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University, New York City, New York 10027, USA – name: 5 Dept. 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, New York, USA – name: 10 Lead Contact – name: 2 Center for Neural Circuits and Behavior, Neurobiology Section and Department of Neuroscience, University of California San Diego, La Jolla, California 92093-0634, USA – name: 7 Present Address: Quantitative Life Sciences, The Abdus Salam International Centre for Theoretical Physics - ICTP, Trieste 34151, Italy |
| Author_xml | – sequence: 1 givenname: Andreas J. orcidid: 0000-0001-7997-6118 surname: Keller fullname: Keller, Andreas J. email: andreasjakob.keller@ucsf.edu organization: Department of Physiology, University of California, San Francisco, San Francisco, CA 94158-0444, USA – sequence: 2 givenname: Mario orcidid: 0000-0002-4454-4224 surname: Dipoppa fullname: Dipoppa, Mario email: md3681@columbia.edu organization: Center for Theoretical Neuroscience, College of Physicians and Surgeons and Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University, New York City, NY 10027, USA – sequence: 3 givenname: Morgane M. surname: Roth fullname: Roth, Morgane M. email: morgane.roth@ucsf.edu organization: Department of Physiology, University of California, San Francisco, San Francisco, CA 94158-0444, USA – sequence: 4 givenname: Matthew S. surname: Caudill fullname: Caudill, Matthew S. organization: Center for Neural Circuits and Behavior, Neurobiology Section and Department of Neuroscience, University of California, San Diego, La Jolla, CA 92093-0634, USA – sequence: 5 givenname: Alessandro orcidid: 0000-0001-5430-7559 surname: Ingrosso fullname: Ingrosso, Alessandro organization: Center for Theoretical Neuroscience, College of Physicians and Surgeons and Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University, New York City, NY 10027, USA – sequence: 6 givenname: Kenneth D. surname: Miller fullname: Miller, Kenneth D. email: kdm2103@columbia.edu organization: Center for Theoretical Neuroscience, College of Physicians and Surgeons and Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University, New York City, NY 10027, USA – sequence: 7 givenname: Massimo surname: Scanziani fullname: Scanziani, Massimo email: massimo@ucsf.edu organization: Department of Physiology, University of California, San Francisco, San Francisco, CA 94158-0444, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/33301712$$D View this record in MEDLINE/PubMed |
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| Keywords | figure-ground segregation recurrent neural network visual cortex canonical disinhibitory circuit computational modeling contextual modulation pop-out effects saliency inhibitory neurons stabilized supralinear network |
| Language | English |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Author contributions. M.S., A.J.K., and M.S.C. designed the experimental study. A.J.K. and M.M.R. conducted all experiments and experimental data analysis. M.S.C. performed preliminary experiments. M.D. and K.D.M. designed the model. M.D. and A.I. developed the training algorithm of the model. M.D. performed the numerical simulations and, with K.D.M., analyzed the model results. A.J.K., M.M.R., M.D., K.D.M., and M.S. wrote the manuscript. |
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| SubjectTerms | Animals Calcium - metabolism canonical disinhibitory circuit computational modeling Computational neuroscience contextual modulation figure-ground segregation inhibitory neurons Intestine Mice Models, Neurological Neural Inhibition - physiology Neurons Neurons - metabolism Photic Stimulation pop-out effects recurrent neural network saliency Somatostatin Somatostatin - metabolism stabilized supralinear network Vasoactive agents Vasoactive intestinal peptide Vasoactive Intestinal Peptide - metabolism Visual cortex Visual Cortex - metabolism Visual Cortex - physiology Visual pathways Visual Pathways - metabolism Visual Pathways - physiology Visual Perception - physiology Visual stimuli |
| Title | A Disinhibitory Circuit for Contextual Modulation in Primary Visual Cortex |
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