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Pop-in: the inversion of pop-out for a feature dimension during visual search in area V4 of the monkey cortex

View ORCID ProfileP. Christiaan Klink, Rob R.M. Teeuwen, View ORCID ProfileJeannette A.M. Lorteije, View ORCID ProfilePieter R. Roelfsema
doi: https://doi.org/10.1101/2022.06.23.497353
P. Christiaan Klink
1Dept. Vision & Cognition, Netherlands Institute for Neuroscience, Royal Netherlands Academy of Arts & Sciences, Amsterdam, The Netherlands
2Experimental Psychology, Helmholtz Institute, Utrecht University, Utrecht, The Netherlands
3Laboratory of Visual Brain Therapy, Sorbonne Université, Institut National de la Santé et de la Recherche Médicale, Centre National de la Recherche Scientifique, Institut de la Vision, Paris F-75012, France
4Dept. of Integrative Neurophysiology, Centre for Neurogenomics and Cognitive Research, VU University, Amsterdam, The Netherlands
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  • For correspondence: c.klink@nin.knaw.nl p.roelfsema@nin.knaw.nl
Rob R.M. Teeuwen
1Dept. Vision & Cognition, Netherlands Institute for Neuroscience, Royal Netherlands Academy of Arts & Sciences, Amsterdam, The Netherlands
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Jeannette A.M. Lorteije
1Dept. Vision & Cognition, Netherlands Institute for Neuroscience, Royal Netherlands Academy of Arts & Sciences, Amsterdam, The Netherlands
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Pieter R. Roelfsema
1Dept. Vision & Cognition, Netherlands Institute for Neuroscience, Royal Netherlands Academy of Arts & Sciences, Amsterdam, The Netherlands
3Laboratory of Visual Brain Therapy, Sorbonne Université, Institut National de la Santé et de la Recherche Médicale, Centre National de la Recherche Scientifique, Institut de la Vision, Paris F-75012, France
4Dept. of Integrative Neurophysiology, Centre for Neurogenomics and Cognitive Research, VU University, Amsterdam, The Netherlands
5Dept. of Psychiatry, Academic Medical Center, University of Amsterdam. Amsterdam, The Netherlands
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  • For correspondence: c.klink@nin.knaw.nl p.roelfsema@nin.knaw.nl
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Abstract

During visual search, it is important to reduce the interference of distracting objects in the scene. The neuronal responses elicited by the search target stimulus are typically enhanced. However, it is equally important to suppress the representations of distracting stimuli, especially if they are salient and capture attention. We trained monkeys to make an eye movement to a unique ‘pop-out’ shape stimulus among an array of distracting stimuli. One of these distractors had a salient color that varied across trials and differed from the color of the other stimuli, causing it to also pop-out. The monkeys were able to select the pop-out shape target with high accuracy and actively avoided the pop-out color distractor. This behavioral pattern was reflected in the activity of neurons in area V4. Responses to the shape targets were enhanced, while the activity evoked by the pop-out color distractor was only briefly enhanced, directly followed by a sustained period of pronounced suppression. These behavioral and neuronal results demonstrate a cortical selection mechanism that rapidly inverts a pop-out signal to ‘pop-in’ for an entire feature dimension thereby facilitating goal-directed visual search in the presence of salient distractors.

Significance statement Goal-directed behaviors like visual search involve both the selection of behaviorally relevant targets and the suppression of task-irrelevant distractors. This is especially important if distractors are salient and capture attention. Here we demonstrate that non-human primates suppress a salient color distractor while searching for a target that is defined by shape, i.e. another feature dimension. The neuronal activity of V4 neurons revealed the temporal evolution of target selection and distractor suppression. The neuronal responses elicited by the pop-out target stimuli were enhanced whereas responses elicited by salient pop-out color distractors were suppressed, after an initial brief phase of response enhancement. Our results reveal a ‘pop-in’ mechanism by which the visual cortex inverts an attentional capture signal into suppression to facilitate visual search.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Competing Interest Statement: No competing interests.

  • Data deposition: All Data & Analysis Code reported in this paper are available on GIN (https://gin.g-node.org/ChrisKlink/NHP_VisualSearch_Pop-in). A doi will be associated with the dataset upon acceptance of the final version of this manuscript.

  • Manuscript updated after peer review. Mainly: theoretical framework in intro and discussion expanded.

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 27, 2022.
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Pop-in: the inversion of pop-out for a feature dimension during visual search in area V4 of the monkey cortex
P. Christiaan Klink, Rob R.M. Teeuwen, Jeannette A.M. Lorteije, Pieter R. Roelfsema
bioRxiv 2022.06.23.497353; doi: https://doi.org/10.1101/2022.06.23.497353
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Pop-in: the inversion of pop-out for a feature dimension during visual search in area V4 of the monkey cortex
P. Christiaan Klink, Rob R.M. Teeuwen, Jeannette A.M. Lorteije, Pieter R. Roelfsema
bioRxiv 2022.06.23.497353; doi: https://doi.org/10.1101/2022.06.23.497353

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