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Being First Matters: Topographical Representational Similarity Analysis of ERP Signals Reveals Separate Networks for Audiovisual Temporal Binding Depending on the Leading Sense

In multisensory integration, processing in one sensory modality is enhanced by complementary information from other modalities. Intersensory timing is crucial in this process because only inputs reaching the brain within a restricted temporal window are perceptually bound. Previous research in the a...

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Autores principales: Cecere, Roberto, Gross, Joachim, Willis, Ashleigh, Thut, Gregor
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5456109/
https://www.ncbi.nlm.nih.gov/pubmed/28450537
http://dx.doi.org/10.1523/JNEUROSCI.2926-16.2017
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author Cecere, Roberto
Gross, Joachim
Willis, Ashleigh
Thut, Gregor
author_facet Cecere, Roberto
Gross, Joachim
Willis, Ashleigh
Thut, Gregor
author_sort Cecere, Roberto
collection PubMed
description In multisensory integration, processing in one sensory modality is enhanced by complementary information from other modalities. Intersensory timing is crucial in this process because only inputs reaching the brain within a restricted temporal window are perceptually bound. Previous research in the audiovisual field has investigated various features of the temporal binding window, revealing asymmetries in its size and plasticity depending on the leading input: auditory–visual (AV) or visual–auditory (VA). Here, we tested whether separate neuronal mechanisms underlie this AV–VA dichotomy in humans. We recorded high-density EEG while participants performed an audiovisual simultaneity judgment task including various AV–VA asynchronies and unisensory control conditions (visual-only, auditory-only) and tested whether AV and VA processing generate different patterns of brain activity. After isolating the multisensory components of AV–VA event-related potentials (ERPs) from the sum of their unisensory constituents, we ran a time-resolved topographical representational similarity analysis (tRSA) comparing the AV and VA ERP maps. Spatial cross-correlation matrices were built from real data to index the similarity between the AV and VA maps at each time point (500 ms window after stimulus) and then correlated with two alternative similarity model matrices: AV(maps) = VA(maps) versus AV(maps) ≠ VA(maps). The tRSA results favored the AV(maps) ≠ VA(maps) model across all time points, suggesting that audiovisual temporal binding (indexed by synchrony perception) engages different neural pathways depending on the leading sense. The existence of such dual route supports recent theoretical accounts proposing that multiple binding mechanisms are implemented in the brain to accommodate different information parsing strategies in auditory and visual sensory systems. SIGNIFICANCE STATEMENT Intersensory timing is a crucial aspect of multisensory integration, determining whether and how inputs in one modality enhance stimulus processing in another modality. Our research demonstrates that evaluating synchrony of auditory-leading (AV) versus visual-leading (VA) audiovisual stimulus pairs is characterized by two distinct patterns of brain activity. This suggests that audiovisual integration is not a unitary process and that different binding mechanisms are recruited in the brain based on the leading sense. These mechanisms may be relevant for supporting different classes of multisensory operations, for example, auditory enhancement of visual attention (AV) and visual enhancement of auditory speech (VA).
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spelling pubmed-54561092017-06-05 Being First Matters: Topographical Representational Similarity Analysis of ERP Signals Reveals Separate Networks for Audiovisual Temporal Binding Depending on the Leading Sense Cecere, Roberto Gross, Joachim Willis, Ashleigh Thut, Gregor J Neurosci Research Articles In multisensory integration, processing in one sensory modality is enhanced by complementary information from other modalities. Intersensory timing is crucial in this process because only inputs reaching the brain within a restricted temporal window are perceptually bound. Previous research in the audiovisual field has investigated various features of the temporal binding window, revealing asymmetries in its size and plasticity depending on the leading input: auditory–visual (AV) or visual–auditory (VA). Here, we tested whether separate neuronal mechanisms underlie this AV–VA dichotomy in humans. We recorded high-density EEG while participants performed an audiovisual simultaneity judgment task including various AV–VA asynchronies and unisensory control conditions (visual-only, auditory-only) and tested whether AV and VA processing generate different patterns of brain activity. After isolating the multisensory components of AV–VA event-related potentials (ERPs) from the sum of their unisensory constituents, we ran a time-resolved topographical representational similarity analysis (tRSA) comparing the AV and VA ERP maps. Spatial cross-correlation matrices were built from real data to index the similarity between the AV and VA maps at each time point (500 ms window after stimulus) and then correlated with two alternative similarity model matrices: AV(maps) = VA(maps) versus AV(maps) ≠ VA(maps). The tRSA results favored the AV(maps) ≠ VA(maps) model across all time points, suggesting that audiovisual temporal binding (indexed by synchrony perception) engages different neural pathways depending on the leading sense. The existence of such dual route supports recent theoretical accounts proposing that multiple binding mechanisms are implemented in the brain to accommodate different information parsing strategies in auditory and visual sensory systems. SIGNIFICANCE STATEMENT Intersensory timing is a crucial aspect of multisensory integration, determining whether and how inputs in one modality enhance stimulus processing in another modality. Our research demonstrates that evaluating synchrony of auditory-leading (AV) versus visual-leading (VA) audiovisual stimulus pairs is characterized by two distinct patterns of brain activity. This suggests that audiovisual integration is not a unitary process and that different binding mechanisms are recruited in the brain based on the leading sense. These mechanisms may be relevant for supporting different classes of multisensory operations, for example, auditory enhancement of visual attention (AV) and visual enhancement of auditory speech (VA). Society for Neuroscience 2017-05-24 /pmc/articles/PMC5456109/ /pubmed/28450537 http://dx.doi.org/10.1523/JNEUROSCI.2926-16.2017 Text en Copyright © 2017 Cecere 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
Cecere, Roberto
Gross, Joachim
Willis, Ashleigh
Thut, Gregor
Being First Matters: Topographical Representational Similarity Analysis of ERP Signals Reveals Separate Networks for Audiovisual Temporal Binding Depending on the Leading Sense
title Being First Matters: Topographical Representational Similarity Analysis of ERP Signals Reveals Separate Networks for Audiovisual Temporal Binding Depending on the Leading Sense
title_full Being First Matters: Topographical Representational Similarity Analysis of ERP Signals Reveals Separate Networks for Audiovisual Temporal Binding Depending on the Leading Sense
title_fullStr Being First Matters: Topographical Representational Similarity Analysis of ERP Signals Reveals Separate Networks for Audiovisual Temporal Binding Depending on the Leading Sense
title_full_unstemmed Being First Matters: Topographical Representational Similarity Analysis of ERP Signals Reveals Separate Networks for Audiovisual Temporal Binding Depending on the Leading Sense
title_short Being First Matters: Topographical Representational Similarity Analysis of ERP Signals Reveals Separate Networks for Audiovisual Temporal Binding Depending on the Leading Sense
title_sort being first matters: topographical representational similarity analysis of erp signals reveals separate networks for audiovisual temporal binding depending on the leading sense
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5456109/
https://www.ncbi.nlm.nih.gov/pubmed/28450537
http://dx.doi.org/10.1523/JNEUROSCI.2926-16.2017
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