Skip to main content
bioRxiv
  • Home
  • About
  • Submit
  • ALERTS / RSS
Advanced Search
New Results

Pattern completion and disruption characterize contextual modulation in the visual cortex

View ORCID ProfileJiakun Fu, Suhas Shrinivasan, Luca Baroni, Zhuokun Ding, View ORCID ProfilePaul G. Fahey, Paweł A. Pierzchlewicz, View ORCID ProfileKayla Ponder, Rachel Froebe, Lydia Ntanavara, View ORCID ProfileTaliah Muhammad, Konstantin F. Willeke, View ORCID ProfileEric Wang, View ORCID ProfileZhiwei Ding, Dat T. Tran, View ORCID ProfileStelios Papadopoulos, View ORCID ProfileSaumil Patel, View ORCID ProfileJacob Reimer, View ORCID ProfileAlexander S. Ecker, View ORCID ProfileXaq Pitkow, Jan Antolik, View ORCID ProfileFabian H. Sinz, View ORCID ProfileRalf M. Häfner, View ORCID ProfileAndreas S. Tolias, View ORCID ProfileKatrin Franke
doi: https://doi.org/10.1101/2023.03.13.532473
Jiakun Fu
1Department of Neuroscience & center for Neuroscience and Artificial Intelligence, Baylor College of Medicine, Houston, Texas, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Jiakun Fu
Suhas Shrinivasan
2Institute of Computer Science and Campus Institute Data Science, University of Göttingen, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Luca Baroni
8Faculty of Mathematics and Physics, Charles University, Prague, Czech Republic
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Zhuokun Ding
1Department of Neuroscience & center for Neuroscience and Artificial Intelligence, Baylor College of Medicine, Houston, Texas, USA
9Department of Ophthalmology, Byers Eye Institute, Stanford University School of Medicine, Stanford, CA, US
10Stanford Bio-X, Stanford University, Stanford, CA, US
11Wu Tsai Neurosciences Institute, Stanford University, Stanford, CA, US
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Paul G. Fahey
1Department of Neuroscience & center for Neuroscience and Artificial Intelligence, Baylor College of Medicine, Houston, Texas, USA
9Department of Ophthalmology, Byers Eye Institute, Stanford University School of Medicine, Stanford, CA, US
10Stanford Bio-X, Stanford University, Stanford, CA, US
11Wu Tsai Neurosciences Institute, Stanford University, Stanford, CA, US
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Paul G. Fahey
Paweł A. Pierzchlewicz
2Institute of Computer Science and Campus Institute Data Science, University of Göttingen, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Kayla Ponder
1Department of Neuroscience & center for Neuroscience and Artificial Intelligence, Baylor College of Medicine, Houston, Texas, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Kayla Ponder
Rachel Froebe
1Department of Neuroscience & center for Neuroscience and Artificial Intelligence, Baylor College of Medicine, Houston, Texas, USA
9Department of Ophthalmology, Byers Eye Institute, Stanford University School of Medicine, Stanford, CA, US
10Stanford Bio-X, Stanford University, Stanford, CA, US
11Wu Tsai Neurosciences Institute, Stanford University, Stanford, CA, US
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Lydia Ntanavara
1Department of Neuroscience & center for Neuroscience and Artificial Intelligence, Baylor College of Medicine, Houston, Texas, USA
9Department of Ophthalmology, Byers Eye Institute, Stanford University School of Medicine, Stanford, CA, US
10Stanford Bio-X, Stanford University, Stanford, CA, US
11Wu Tsai Neurosciences Institute, Stanford University, Stanford, CA, US
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Taliah Muhammad
1Department of Neuroscience & center for Neuroscience and Artificial Intelligence, Baylor College of Medicine, Houston, Texas, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Taliah Muhammad
Konstantin F. Willeke
2Institute of Computer Science and Campus Institute Data Science, University of Göttingen, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Eric Wang
1Department of Neuroscience & center for Neuroscience and Artificial Intelligence, Baylor College of Medicine, Houston, Texas, USA
9Department of Ophthalmology, Byers Eye Institute, Stanford University School of Medicine, Stanford, CA, US
10Stanford Bio-X, Stanford University, Stanford, CA, US
11Wu Tsai Neurosciences Institute, Stanford University, Stanford, CA, US
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Eric Wang
Zhiwei Ding
1Department of Neuroscience & center for Neuroscience and Artificial Intelligence, Baylor College of Medicine, Houston, Texas, USA
9Department of Ophthalmology, Byers Eye Institute, Stanford University School of Medicine, Stanford, CA, US
10Stanford Bio-X, Stanford University, Stanford, CA, US
11Wu Tsai Neurosciences Institute, Stanford University, Stanford, CA, US
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Zhiwei Ding
Dat T. Tran
1Department of Neuroscience & center for Neuroscience and Artificial Intelligence, Baylor College of Medicine, Houston, Texas, USA
9Department of Ophthalmology, Byers Eye Institute, Stanford University School of Medicine, Stanford, CA, US
10Stanford Bio-X, Stanford University, Stanford, CA, US
11Wu Tsai Neurosciences Institute, Stanford University, Stanford, CA, US
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Stelios Papadopoulos
1Department of Neuroscience & center for Neuroscience and Artificial Intelligence, Baylor College of Medicine, Houston, Texas, USA
9Department of Ophthalmology, Byers Eye Institute, Stanford University School of Medicine, Stanford, CA, US
10Stanford Bio-X, Stanford University, Stanford, CA, US
11Wu Tsai Neurosciences Institute, Stanford University, Stanford, CA, US
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Stelios Papadopoulos
Saumil Patel
1Department of Neuroscience & center for Neuroscience and Artificial Intelligence, Baylor College of Medicine, Houston, Texas, USA
9Department of Ophthalmology, Byers Eye Institute, Stanford University School of Medicine, Stanford, CA, US
10Stanford Bio-X, Stanford University, Stanford, CA, US
11Wu Tsai Neurosciences Institute, Stanford University, Stanford, CA, US
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Saumil Patel
Jacob Reimer
1Department of Neuroscience & center for Neuroscience and Artificial Intelligence, Baylor College of Medicine, Houston, Texas, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Jacob Reimer
Alexander S. Ecker
2Institute of Computer Science and Campus Institute Data Science, University of Göttingen, Germany
3Max Planck Institute for Dynamics and Self-Organization, Göttingen, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Alexander S. Ecker
Xaq Pitkow
1Department of Neuroscience & center for Neuroscience and Artificial Intelligence, Baylor College of Medicine, Houston, Texas, USA
6Neuroscience Institute, Carnegie Mellon University, Pittsburgh, USA
7Department of Machine Learning, Carnegie Mellon University, Pittsburgh, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Xaq Pitkow
Jan Antolik
8Faculty of Mathematics and Physics, Charles University, Prague, Czech Republic
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Fabian H. Sinz
1Department of Neuroscience & center for Neuroscience and Artificial Intelligence, Baylor College of Medicine, Houston, Texas, USA
2Institute of Computer Science and Campus Institute Data Science, University of Göttingen, Germany
5Institute for Bioinformatics and Medical Informatics, University of Tübingen, Tübingen, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Fabian H. Sinz
Ralf M. Häfner
4Brain and Cognitive Sciences, Center for Visual Science, University of Rochester, Rochester, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Ralf M. Häfner
Andreas S. Tolias
1Department of Neuroscience & center for Neuroscience and Artificial Intelligence, Baylor College of Medicine, Houston, Texas, USA
9Department of Ophthalmology, Byers Eye Institute, Stanford University School of Medicine, Stanford, CA, US
10Stanford Bio-X, Stanford University, Stanford, CA, US
11Wu Tsai Neurosciences Institute, Stanford University, Stanford, CA, US
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Andreas S. Tolias
  • For correspondence: kafranke{at}stanford.edu tolias{at}stanford.edu
Katrin Franke
1Department of Neuroscience & center for Neuroscience and Artificial Intelligence, Baylor College of Medicine, Houston, Texas, USA
9Department of Ophthalmology, Byers Eye Institute, Stanford University School of Medicine, Stanford, CA, US
10Stanford Bio-X, Stanford University, Stanford, CA, US
11Wu Tsai Neurosciences Institute, Stanford University, Stanford, CA, US
12Department of Electrical Engineering, Stanford University, Stanford, CA, US
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Katrin Franke
  • For correspondence: kafranke{at}stanford.edu tolias{at}stanford.edu
  • Abstract
  • Full Text
  • Info/History
  • Metrics
  • Preview PDF
Loading

Abstract

Vision is fundamentally context-dependent, with neuronal responses influenced not just by local features but also by surrounding contextual information. In the visual cortex, studies using simple grating stimuli indicate that congruent stimuli—where the center and surround share the same orientation—are more inhibitory than when orientations are orthogonal, potentially serving redundancy reduction and predictive coding. Understanding these center-surround interactions in relation to natural image statistics is challenging due to the high dimensionality of the stimulus space, yet crucial for deciphering the neuronal code of real-world sensory processing. Utilizing large-scale recordings from mouse V1, we trained convolutional neural networks (CNNs) to predict and synthesize surround patterns that either optimally suppressed or enhanced responses to center stimuli, confirmed by in v ivo experiments. Contrary to the notion that congruent stimuli are suppressive, we found that surrounds that completed patterns based on natural image statistics were facilitatory, while disruptive surrounds were suppressive. Applying our CNN image synthesis method in macaque V1, we discovered that pattern completion within the near surround occurred more frequently with excitatory than with inhibitory surrounds, suggesting that our results in mice are conserved in macaques. Further, experiments and model analyses confirmed previous studies reporting the opposite effect with grating stimuli in both species. Using the MICrONS functional connectomics dataset, we observed that neurons with similar feature selectivity formed excitatory connections regardless of their receptive field overlap, aligning with the pattern completion phenomenon observed for excitatory surrounds. Finally, our empirical results emerged in a normative model of perception implementing Bayesian inference, where neuronal responses are modulated by prior knowledge of natural scene statistics. In summary, our findings identify a novel relationship between contextual information and natural scene statistics and provide evidence for a role of contextual modulation in hierarchical inference.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵† Senior authors

  • To compare our results to previous work using parametric stimuli, we performed new experiments with center-surround grating stimuli in mice (Fig. 4). In addition, we used an existing dataset of macaque V1 responses to natural images, which we had previously recorded, to study species-specific differences in surround modulation (Fig. 5, Suppl. Fig. 6). Authors and affiliations updated.

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.
Back to top
PreviousNext
Posted May 09, 2024.
Download PDF
Email

Thank you for your interest in spreading the word about bioRxiv.

NOTE: Your email address is requested solely to identify you as the sender of this article.

Enter multiple addresses on separate lines or separate them with commas.
Pattern completion and disruption characterize contextual modulation in the visual cortex
(Your Name) has forwarded a page to you from bioRxiv
(Your Name) thought you would like to see this page from the bioRxiv website.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Share
Pattern completion and disruption characterize contextual modulation in the visual cortex
Jiakun Fu, Suhas Shrinivasan, Luca Baroni, Zhuokun Ding, Paul G. Fahey, Paweł A. Pierzchlewicz, Kayla Ponder, Rachel Froebe, Lydia Ntanavara, Taliah Muhammad, Konstantin F. Willeke, Eric Wang, Zhiwei Ding, Dat T. Tran, Stelios Papadopoulos, Saumil Patel, Jacob Reimer, Alexander S. Ecker, Xaq Pitkow, Jan Antolik, Fabian H. Sinz, Ralf M. Häfner, Andreas S. Tolias, Katrin Franke
bioRxiv 2023.03.13.532473; doi: https://doi.org/10.1101/2023.03.13.532473
Twitter logo Facebook logo LinkedIn logo Mendeley logo
Citation Tools
Pattern completion and disruption characterize contextual modulation in the visual cortex
Jiakun Fu, Suhas Shrinivasan, Luca Baroni, Zhuokun Ding, Paul G. Fahey, Paweł A. Pierzchlewicz, Kayla Ponder, Rachel Froebe, Lydia Ntanavara, Taliah Muhammad, Konstantin F. Willeke, Eric Wang, Zhiwei Ding, Dat T. Tran, Stelios Papadopoulos, Saumil Patel, Jacob Reimer, Alexander S. Ecker, Xaq Pitkow, Jan Antolik, Fabian H. Sinz, Ralf M. Häfner, Andreas S. Tolias, Katrin Franke
bioRxiv 2023.03.13.532473; doi: https://doi.org/10.1101/2023.03.13.532473

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
  • Tweet Widget
  • Facebook Like
  • Google Plus One

Subject Area

  • Neuroscience
Subject Areas
All Articles
  • Animal Behavior and Cognition (7799)
  • Biochemistry (18204)
  • Bioengineering (14381)
  • Bioinformatics (43089)
  • Biophysics (21969)
  • Cancer Biology (19100)
  • Cell Biology (26172)
  • Clinical Trials (138)
  • Developmental Biology (13646)
  • Ecology (20385)
  • Epidemiology (2067)
  • Evolutionary Biology (24840)
  • Genetics (15841)
  • Genomics (22973)
  • Immunology (18195)
  • Microbiology (41339)
  • Molecular Biology (17538)
  • Neuroscience (90808)
  • Paleontology (679)
  • Pathology (2904)
  • Pharmacology and Toxicology (4946)
  • Physiology (7869)
  • Plant Biology (15502)
  • Scientific Communication and Education (2066)
  • Synthetic Biology (4431)
  • Systems Biology (10008)
  • Zoology (2314)