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Attention to visual motion suppresses neuronal and behavioral sensitivity in nearby feature space

BACKGROUND: Feature-based attention prioritizes the processing of the attended feature while strongly suppressing the processing of nearby ones. This creates a non-linearity or “attentional suppressive surround” predicted by the Selective Tuning model of visual attention. However, previously reporte...

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Autores principales: Yoo, Sang-Ah, Martinez-Trujillo, Julio C., Treue, Stefan, Tsotsos, John K., Fallah, Mazyar
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9535987/
https://www.ncbi.nlm.nih.gov/pubmed/36199136
http://dx.doi.org/10.1186/s12915-022-01428-7
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author Yoo, Sang-Ah
Martinez-Trujillo, Julio C.
Treue, Stefan
Tsotsos, John K.
Fallah, Mazyar
author_facet Yoo, Sang-Ah
Martinez-Trujillo, Julio C.
Treue, Stefan
Tsotsos, John K.
Fallah, Mazyar
author_sort Yoo, Sang-Ah
collection PubMed
description BACKGROUND: Feature-based attention prioritizes the processing of the attended feature while strongly suppressing the processing of nearby ones. This creates a non-linearity or “attentional suppressive surround” predicted by the Selective Tuning model of visual attention. However, previously reported effects of feature-based attention on neuronal responses are linear, e.g., feature-similarity gain. Here, we investigated this apparent contradiction by neurophysiological and psychophysical approaches. RESULTS: Responses of motion direction-selective neurons in area MT/MST of monkeys were recorded during a motion task. When attention was allocated to a stimulus moving in the neurons’ preferred direction, response tuning curves showed its minimum for directions 60–90° away from the preferred direction, an attentional suppressive surround. This effect was modeled via the interaction of two Gaussian fields representing excitatory narrowly tuned and inhibitory widely tuned inputs into a neuron, with feature-based attention predominantly increasing the gain of inhibitory inputs. We further showed using a motion repulsion paradigm in humans that feature-based attention produces a similar non-linearity on motion discrimination performance. CONCLUSIONS: Our results link the gain modulation of neuronal inputs and tuning curves examined through the feature-similarity gain lens to the attentional impact on neural population responses predicted by the Selective Tuning model, providing a unified framework for the documented effects of feature-based attention on neuronal responses and behavior. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-022-01428-7.
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spelling pubmed-95359872022-10-07 Attention to visual motion suppresses neuronal and behavioral sensitivity in nearby feature space Yoo, Sang-Ah Martinez-Trujillo, Julio C. Treue, Stefan Tsotsos, John K. Fallah, Mazyar BMC Biol Research Article BACKGROUND: Feature-based attention prioritizes the processing of the attended feature while strongly suppressing the processing of nearby ones. This creates a non-linearity or “attentional suppressive surround” predicted by the Selective Tuning model of visual attention. However, previously reported effects of feature-based attention on neuronal responses are linear, e.g., feature-similarity gain. Here, we investigated this apparent contradiction by neurophysiological and psychophysical approaches. RESULTS: Responses of motion direction-selective neurons in area MT/MST of monkeys were recorded during a motion task. When attention was allocated to a stimulus moving in the neurons’ preferred direction, response tuning curves showed its minimum for directions 60–90° away from the preferred direction, an attentional suppressive surround. This effect was modeled via the interaction of two Gaussian fields representing excitatory narrowly tuned and inhibitory widely tuned inputs into a neuron, with feature-based attention predominantly increasing the gain of inhibitory inputs. We further showed using a motion repulsion paradigm in humans that feature-based attention produces a similar non-linearity on motion discrimination performance. CONCLUSIONS: Our results link the gain modulation of neuronal inputs and tuning curves examined through the feature-similarity gain lens to the attentional impact on neural population responses predicted by the Selective Tuning model, providing a unified framework for the documented effects of feature-based attention on neuronal responses and behavior. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-022-01428-7. BioMed Central 2022-10-05 /pmc/articles/PMC9535987/ /pubmed/36199136 http://dx.doi.org/10.1186/s12915-022-01428-7 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Yoo, Sang-Ah
Martinez-Trujillo, Julio C.
Treue, Stefan
Tsotsos, John K.
Fallah, Mazyar
Attention to visual motion suppresses neuronal and behavioral sensitivity in nearby feature space
title Attention to visual motion suppresses neuronal and behavioral sensitivity in nearby feature space
title_full Attention to visual motion suppresses neuronal and behavioral sensitivity in nearby feature space
title_fullStr Attention to visual motion suppresses neuronal and behavioral sensitivity in nearby feature space
title_full_unstemmed Attention to visual motion suppresses neuronal and behavioral sensitivity in nearby feature space
title_short Attention to visual motion suppresses neuronal and behavioral sensitivity in nearby feature space
title_sort attention to visual motion suppresses neuronal and behavioral sensitivity in nearby feature space
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9535987/
https://www.ncbi.nlm.nih.gov/pubmed/36199136
http://dx.doi.org/10.1186/s12915-022-01428-7
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