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Previously Reward-Associated Stimuli Capture Spatial Attention in the Absence of Changes in the Corresponding Sensory Representations as Measured with MEG

Studies of selective attention typically consider the role of task goals or physical salience, but attention can also be captured by previously reward-associated stimuli, even if they are currently task irrelevant. One theory underlying this value-driven attentional capture (VDAC) is that reward-ass...

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Autores principales: Tankelevitch, Lev, Spaak, Eelke, Rushworth, Matthew F.S., Stokes, Mark G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7314418/
https://www.ncbi.nlm.nih.gov/pubmed/32366722
http://dx.doi.org/10.1523/JNEUROSCI.1172-19.2020
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author Tankelevitch, Lev
Spaak, Eelke
Rushworth, Matthew F.S.
Stokes, Mark G.
author_facet Tankelevitch, Lev
Spaak, Eelke
Rushworth, Matthew F.S.
Stokes, Mark G.
author_sort Tankelevitch, Lev
collection PubMed
description Studies of selective attention typically consider the role of task goals or physical salience, but attention can also be captured by previously reward-associated stimuli, even if they are currently task irrelevant. One theory underlying this value-driven attentional capture (VDAC) is that reward-associated stimulus representations undergo plasticity in sensory cortex, thereby automatically capturing attention during early processing. To test this, we used magnetoencephalography to probe whether stimulus location and identity representations in sensory cortex are modulated by reward learning. We furthermore investigated the time course of these neural effects, and their relationship to behavioral VDAC. Male and female human participants first learned stimulus–reward associations. Next, we measured VDAC in a separate task by presenting these stimuli in the absence of reward contingency and probing their effects on the processing of separate target stimuli presented at different time lags. Using time-resolved multivariate pattern analysis, we found that learned value modulated the spatial selection of previously rewarded stimuli in posterior visual and parietal cortex from ∼260 ms after stimulus onset. This value modulation was related to the strength of participants' behavioral VDAC effect and persisted into subsequent target processing. Importantly, learned value did not influence cortical signatures of early processing (i.e., earlier than ∼200 ms); nor did it influence the decodability of stimulus identity. Our results suggest that VDAC is underpinned by learned value signals that modulate spatial selection throughout posterior visual and parietal cortex. We further suggest that VDAC can occur in the absence of changes in early visual processing in cortex. SIGNIFICANCE STATEMENT Attention is our ability to focus on relevant information at the expense of irrelevant information. It can be affected by previously learned but currently irrelevant stimulus–reward associations, a phenomenon termed “value-driven attentional capture” (VDAC). The neural mechanisms underlying VDAC remain unclear. It has been speculated that reward learning induces visual cortical plasticity, which modulates early visual processing to capture attention. Although we find that learned value modulates spatial signals in visual cortical areas, an effect that correlates with VDAC, we find no relevant signatures of changes in early visual processing in cortex.
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spelling pubmed-73144182020-06-25 Previously Reward-Associated Stimuli Capture Spatial Attention in the Absence of Changes in the Corresponding Sensory Representations as Measured with MEG Tankelevitch, Lev Spaak, Eelke Rushworth, Matthew F.S. Stokes, Mark G. J Neurosci Research Articles Studies of selective attention typically consider the role of task goals or physical salience, but attention can also be captured by previously reward-associated stimuli, even if they are currently task irrelevant. One theory underlying this value-driven attentional capture (VDAC) is that reward-associated stimulus representations undergo plasticity in sensory cortex, thereby automatically capturing attention during early processing. To test this, we used magnetoencephalography to probe whether stimulus location and identity representations in sensory cortex are modulated by reward learning. We furthermore investigated the time course of these neural effects, and their relationship to behavioral VDAC. Male and female human participants first learned stimulus–reward associations. Next, we measured VDAC in a separate task by presenting these stimuli in the absence of reward contingency and probing their effects on the processing of separate target stimuli presented at different time lags. Using time-resolved multivariate pattern analysis, we found that learned value modulated the spatial selection of previously rewarded stimuli in posterior visual and parietal cortex from ∼260 ms after stimulus onset. This value modulation was related to the strength of participants' behavioral VDAC effect and persisted into subsequent target processing. Importantly, learned value did not influence cortical signatures of early processing (i.e., earlier than ∼200 ms); nor did it influence the decodability of stimulus identity. Our results suggest that VDAC is underpinned by learned value signals that modulate spatial selection throughout posterior visual and parietal cortex. We further suggest that VDAC can occur in the absence of changes in early visual processing in cortex. SIGNIFICANCE STATEMENT Attention is our ability to focus on relevant information at the expense of irrelevant information. It can be affected by previously learned but currently irrelevant stimulus–reward associations, a phenomenon termed “value-driven attentional capture” (VDAC). The neural mechanisms underlying VDAC remain unclear. It has been speculated that reward learning induces visual cortical plasticity, which modulates early visual processing to capture attention. Although we find that learned value modulates spatial signals in visual cortical areas, an effect that correlates with VDAC, we find no relevant signatures of changes in early visual processing in cortex. Society for Neuroscience 2020-06-24 /pmc/articles/PMC7314418/ /pubmed/32366722 http://dx.doi.org/10.1523/JNEUROSCI.1172-19.2020 Text en Copyright © 2020 Tankelevitch et al. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License Creative Commons Attribution 4.0 International (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Articles
Tankelevitch, Lev
Spaak, Eelke
Rushworth, Matthew F.S.
Stokes, Mark G.
Previously Reward-Associated Stimuli Capture Spatial Attention in the Absence of Changes in the Corresponding Sensory Representations as Measured with MEG
title Previously Reward-Associated Stimuli Capture Spatial Attention in the Absence of Changes in the Corresponding Sensory Representations as Measured with MEG
title_full Previously Reward-Associated Stimuli Capture Spatial Attention in the Absence of Changes in the Corresponding Sensory Representations as Measured with MEG
title_fullStr Previously Reward-Associated Stimuli Capture Spatial Attention in the Absence of Changes in the Corresponding Sensory Representations as Measured with MEG
title_full_unstemmed Previously Reward-Associated Stimuli Capture Spatial Attention in the Absence of Changes in the Corresponding Sensory Representations as Measured with MEG
title_short Previously Reward-Associated Stimuli Capture Spatial Attention in the Absence of Changes in the Corresponding Sensory Representations as Measured with MEG
title_sort previously reward-associated stimuli capture spatial attention in the absence of changes in the corresponding sensory representations as measured with meg
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7314418/
https://www.ncbi.nlm.nih.gov/pubmed/32366722
http://dx.doi.org/10.1523/JNEUROSCI.1172-19.2020
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