Early beta oscillations in multisensory association areas underlie crossmodal performance enhancement

The combination of signals from different sensory modalities can enhance perception and facilitate behavioral responses. While previous research described crossmodal influences in a wide range of tasks, it remains unclear how such influences drive performance enhancements. In particular, the neural...

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Main Authors: Georgios Michail, Daniel Senkowski, Martin Holtkamp, Bettina Wächter, Julian Keil
Format: Article
Language:English
Published: Elsevier 2022-08-01
Series:NeuroImage
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S1053811922004268
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author Georgios Michail
Daniel Senkowski
Martin Holtkamp
Bettina Wächter
Julian Keil
author_facet Georgios Michail
Daniel Senkowski
Martin Holtkamp
Bettina Wächter
Julian Keil
author_sort Georgios Michail
collection DOAJ
description The combination of signals from different sensory modalities can enhance perception and facilitate behavioral responses. While previous research described crossmodal influences in a wide range of tasks, it remains unclear how such influences drive performance enhancements. In particular, the neural mechanisms underlying performance-relevant crossmodal influences, as well as the latency and spatial profile of such influences are not well understood. Here, we examined data from high-density electroencephalography (N = 30) recordings to characterize the oscillatory signatures of crossmodal facilitation of response speed, as manifested in the speeding of visual responses by concurrent task-irrelevant auditory information. Using a data-driven analysis approach, we found that individual gains in response speed correlated with larger beta power difference (13–25 Hz) between the audiovisual and the visual condition, starting within 80 ms after stimulus onset in the secondary visual cortex and in multisensory association areas in the parietal cortex. In addition, we examined data from electrocorticography (ECoG) recordings in four epileptic patients in a comparable paradigm. These ECoG data revealed reduced beta power in audiovisual compared with visual trials in the superior temporal gyrus (STG). Collectively, our data suggest that the crossmodal facilitation of response speed is associated with reduced early beta power in multisensory association and secondary visual areas. The reduced early beta power may reflect an auditory-driven feedback signal to improve visual processing through attentional gating. These findings improve our understanding of the neural mechanisms underlying crossmodal response speed facilitation and highlight the critical role of beta oscillations in mediating behaviorally relevant multisensory processing.
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spelling doaj.art-3fcce0f242cf480bb2e9345faec0f58b2022-12-22T03:36:18ZengElsevierNeuroImage1095-95722022-08-01257119307Early beta oscillations in multisensory association areas underlie crossmodal performance enhancementGeorgios Michail0Daniel Senkowski1Martin Holtkamp2Bettina Wächter3Julian Keil4Department of Psychiatry and Psychotherapy, Charité Campus Mitte (CCM), Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Charitéplatz 1, Berlin 10117, Germany; Corresponding author.Department of Psychiatry and Psychotherapy, Charité Campus Mitte (CCM), Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Charitéplatz 1, Berlin 10117, GermanyEpilepsy-Center Berlin-Brandenburg, Institute for Diagnostics of Epilepsy, Berlin 10365, Germany; Department of Neurology, Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Charité Campus Mitte (CCM), Charitéplatz 1, Berlin 10117, GermanyEpilepsy-Center Berlin-Brandenburg, Institute for Diagnostics of Epilepsy, Berlin 10365, GermanyBiological Psychology, Christian–Albrechts–University Kiel, Kiel 24118, GermanyThe combination of signals from different sensory modalities can enhance perception and facilitate behavioral responses. While previous research described crossmodal influences in a wide range of tasks, it remains unclear how such influences drive performance enhancements. In particular, the neural mechanisms underlying performance-relevant crossmodal influences, as well as the latency and spatial profile of such influences are not well understood. Here, we examined data from high-density electroencephalography (N = 30) recordings to characterize the oscillatory signatures of crossmodal facilitation of response speed, as manifested in the speeding of visual responses by concurrent task-irrelevant auditory information. Using a data-driven analysis approach, we found that individual gains in response speed correlated with larger beta power difference (13–25 Hz) between the audiovisual and the visual condition, starting within 80 ms after stimulus onset in the secondary visual cortex and in multisensory association areas in the parietal cortex. In addition, we examined data from electrocorticography (ECoG) recordings in four epileptic patients in a comparable paradigm. These ECoG data revealed reduced beta power in audiovisual compared with visual trials in the superior temporal gyrus (STG). Collectively, our data suggest that the crossmodal facilitation of response speed is associated with reduced early beta power in multisensory association and secondary visual areas. The reduced early beta power may reflect an auditory-driven feedback signal to improve visual processing through attentional gating. These findings improve our understanding of the neural mechanisms underlying crossmodal response speed facilitation and highlight the critical role of beta oscillations in mediating behaviorally relevant multisensory processing.http://www.sciencedirect.com/science/article/pii/S1053811922004268AudiovisualBeta bandFacilitationResponse speedOscillationsECoG
spellingShingle Georgios Michail
Daniel Senkowski
Martin Holtkamp
Bettina Wächter
Julian Keil
Early beta oscillations in multisensory association areas underlie crossmodal performance enhancement
NeuroImage
Audiovisual
Beta band
Facilitation
Response speed
Oscillations
ECoG
title Early beta oscillations in multisensory association areas underlie crossmodal performance enhancement
title_full Early beta oscillations in multisensory association areas underlie crossmodal performance enhancement
title_fullStr Early beta oscillations in multisensory association areas underlie crossmodal performance enhancement
title_full_unstemmed Early beta oscillations in multisensory association areas underlie crossmodal performance enhancement
title_short Early beta oscillations in multisensory association areas underlie crossmodal performance enhancement
title_sort early beta oscillations in multisensory association areas underlie crossmodal performance enhancement
topic Audiovisual
Beta band
Facilitation
Response speed
Oscillations
ECoG
url http://www.sciencedirect.com/science/article/pii/S1053811922004268
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AT martinholtkamp earlybetaoscillationsinmultisensoryassociationareasunderliecrossmodalperformanceenhancement
AT bettinawachter earlybetaoscillationsinmultisensoryassociationareasunderliecrossmodalperformanceenhancement
AT juliankeil earlybetaoscillationsinmultisensoryassociationareasunderliecrossmodalperformanceenhancement