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Interactions between Conscious and Subconscious Signals: Selective Attention under Feature-Based Competition Increases Neural Selectivity during Brain Adaptation

Efficient perception in natural environments depends on neural interactions between voluntary processes within cognitive control, such as attention, and those that are automatic and subconscious, such as brain adaptation to predictable input (also called repetition suppression). Although both attent...

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Autores principales: Kikuchi, Yukiko, Ip, Jennifer, Lagier, Gaëtan, Mossom, James C., Kumar, Sukhbinder, Petkov, Christopher I., Barraclough, Nick E., Vuong, Quoc C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6616293/
https://www.ncbi.nlm.nih.gov/pubmed/31068438
http://dx.doi.org/10.1523/JNEUROSCI.3052-18.2019
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author Kikuchi, Yukiko
Ip, Jennifer
Lagier, Gaëtan
Mossom, James C.
Kumar, Sukhbinder
Petkov, Christopher I.
Barraclough, Nick E.
Vuong, Quoc C.
author_facet Kikuchi, Yukiko
Ip, Jennifer
Lagier, Gaëtan
Mossom, James C.
Kumar, Sukhbinder
Petkov, Christopher I.
Barraclough, Nick E.
Vuong, Quoc C.
author_sort Kikuchi, Yukiko
collection PubMed
description Efficient perception in natural environments depends on neural interactions between voluntary processes within cognitive control, such as attention, and those that are automatic and subconscious, such as brain adaptation to predictable input (also called repetition suppression). Although both attention and adaptation have been studied separately and there is considerable knowledge of the neurobiology involved in each of these processes, how attention interacts with adaptation remains equivocal. We examined how attention interacts with visual and auditory adaptation by measuring neuroimaging effects consistent with changes in either neural gain or selectivity. Male and female human participants were scanned with functional magnetic resonance imaging (fMRI) first while they discriminated repetition of morphed faces or voices and either directed their attention to stimulus identity or spatial location. Attention to face or voice identity, while ignoring stimulus location, solely increased the gain of respectively face- or voice-sensitive cortex. The results were strikingly different in an experiment when participants attended to voice identity versus stimulus loudness. In this case, attention to voice while ignoring sound loudness increased neural selectivity. The combined results show that how attention affects adaptation depends on the level of feature-based competition, reconciling prior conflicting observations. The findings are theoretically important and are discussed in relation to neurobiological interactions between attention and different types of predictive signals. SIGNIFICANCE STATEMENT Adaptation to repeated environmental events is ubiquitous in the animal brain, an automatic typically subconscious, predictive signal. Cognitive influences, such as by attention, powerfully affect sensory processing and can overcome brain adaptation. However, how neural interactions occur between adaptation and attention remains controversial. We conducted fMRI experiments regulating the focus of attention during adaptation to repeated stimuli with perceptually balanced stimulus expectancy. We observed an interaction between attention and adaptation consistent with increased neural selectivity, but only under conditions of feature-based competition, challenging the notion that attention interacts with brain adaptation by only affecting response gain. This demonstrates that attention retains its full complement of mechanistic influences on sensory cortex even as it interacts with more automatic or subconscious predictive processes.
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spelling pubmed-66162932019-07-15 Interactions between Conscious and Subconscious Signals: Selective Attention under Feature-Based Competition Increases Neural Selectivity during Brain Adaptation Kikuchi, Yukiko Ip, Jennifer Lagier, Gaëtan Mossom, James C. Kumar, Sukhbinder Petkov, Christopher I. Barraclough, Nick E. Vuong, Quoc C. J Neurosci Research Articles Efficient perception in natural environments depends on neural interactions between voluntary processes within cognitive control, such as attention, and those that are automatic and subconscious, such as brain adaptation to predictable input (also called repetition suppression). Although both attention and adaptation have been studied separately and there is considerable knowledge of the neurobiology involved in each of these processes, how attention interacts with adaptation remains equivocal. We examined how attention interacts with visual and auditory adaptation by measuring neuroimaging effects consistent with changes in either neural gain or selectivity. Male and female human participants were scanned with functional magnetic resonance imaging (fMRI) first while they discriminated repetition of morphed faces or voices and either directed their attention to stimulus identity or spatial location. Attention to face or voice identity, while ignoring stimulus location, solely increased the gain of respectively face- or voice-sensitive cortex. The results were strikingly different in an experiment when participants attended to voice identity versus stimulus loudness. In this case, attention to voice while ignoring sound loudness increased neural selectivity. The combined results show that how attention affects adaptation depends on the level of feature-based competition, reconciling prior conflicting observations. The findings are theoretically important and are discussed in relation to neurobiological interactions between attention and different types of predictive signals. SIGNIFICANCE STATEMENT Adaptation to repeated environmental events is ubiquitous in the animal brain, an automatic typically subconscious, predictive signal. Cognitive influences, such as by attention, powerfully affect sensory processing and can overcome brain adaptation. However, how neural interactions occur between adaptation and attention remains controversial. We conducted fMRI experiments regulating the focus of attention during adaptation to repeated stimuli with perceptually balanced stimulus expectancy. We observed an interaction between attention and adaptation consistent with increased neural selectivity, but only under conditions of feature-based competition, challenging the notion that attention interacts with brain adaptation by only affecting response gain. This demonstrates that attention retains its full complement of mechanistic influences on sensory cortex even as it interacts with more automatic or subconscious predictive processes. Society for Neuroscience 2019-07-10 /pmc/articles/PMC6616293/ /pubmed/31068438 http://dx.doi.org/10.1523/JNEUROSCI.3052-18.2019 Text en Copyright © 2019 Kikuchi 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
Kikuchi, Yukiko
Ip, Jennifer
Lagier, Gaëtan
Mossom, James C.
Kumar, Sukhbinder
Petkov, Christopher I.
Barraclough, Nick E.
Vuong, Quoc C.
Interactions between Conscious and Subconscious Signals: Selective Attention under Feature-Based Competition Increases Neural Selectivity during Brain Adaptation
title Interactions between Conscious and Subconscious Signals: Selective Attention under Feature-Based Competition Increases Neural Selectivity during Brain Adaptation
title_full Interactions between Conscious and Subconscious Signals: Selective Attention under Feature-Based Competition Increases Neural Selectivity during Brain Adaptation
title_fullStr Interactions between Conscious and Subconscious Signals: Selective Attention under Feature-Based Competition Increases Neural Selectivity during Brain Adaptation
title_full_unstemmed Interactions between Conscious and Subconscious Signals: Selective Attention under Feature-Based Competition Increases Neural Selectivity during Brain Adaptation
title_short Interactions between Conscious and Subconscious Signals: Selective Attention under Feature-Based Competition Increases Neural Selectivity during Brain Adaptation
title_sort interactions between conscious and subconscious signals: selective attention under feature-based competition increases neural selectivity during brain adaptation
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6616293/
https://www.ncbi.nlm.nih.gov/pubmed/31068438
http://dx.doi.org/10.1523/JNEUROSCI.3052-18.2019
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