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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...
Autores principales: | , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Society for Neuroscience
2017
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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). |
format | Online Article Text |
id | pubmed-5456109 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2017 |
publisher | Society for Neuroscience |
record_format | MEDLINE/PubMed |
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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