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Emotional speech synchronizes brains across listeners and engages large-scale dynamic brain networks

Speech provides a powerful means for sharing emotions. Here we implement novel intersubject phase synchronization and whole-brain dynamic connectivity measures to show that networks of brain areas become synchronized across participants who are listening to emotional episodes in spoken narratives. T...

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Autores principales: Nummenmaa, Lauri, Saarimäki, Heini, Glerean, Enrico, Gotsopoulos, Athanasios, Jääskeläinen, Iiro P., Hari, Riitta, Sams, Mikko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Academic Press 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4229500/
https://www.ncbi.nlm.nih.gov/pubmed/25128711
http://dx.doi.org/10.1016/j.neuroimage.2014.07.063
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author Nummenmaa, Lauri
Saarimäki, Heini
Glerean, Enrico
Gotsopoulos, Athanasios
Jääskeläinen, Iiro P.
Hari, Riitta
Sams, Mikko
author_facet Nummenmaa, Lauri
Saarimäki, Heini
Glerean, Enrico
Gotsopoulos, Athanasios
Jääskeläinen, Iiro P.
Hari, Riitta
Sams, Mikko
author_sort Nummenmaa, Lauri
collection PubMed
description Speech provides a powerful means for sharing emotions. Here we implement novel intersubject phase synchronization and whole-brain dynamic connectivity measures to show that networks of brain areas become synchronized across participants who are listening to emotional episodes in spoken narratives. Twenty participants' hemodynamic brain activity was measured with functional magnetic resonance imaging (fMRI) while they listened to 45-s narratives describing unpleasant, neutral, and pleasant events spoken in neutral voice. After scanning, participants listened to the narratives again and rated continuously their feelings of pleasantness–unpleasantness (valence) and of arousal–calmness. Instantaneous intersubject phase synchronization (ISPS) measures were computed to derive both multi-subject voxel-wise similarity measures of hemodynamic activity and inter-area functional dynamic connectivity (seed-based phase synchronization, SBPS). Valence and arousal time series were subsequently used to predict the ISPS and SBPS time series. High arousal was associated with increased ISPS in the auditory cortices and in Broca's area, and negative valence was associated with enhanced ISPS in the thalamus, anterior cingulate, lateral prefrontal, and orbitofrontal cortices. Negative valence affected functional connectivity of fronto-parietal, limbic (insula, cingulum) and fronto-opercular circuitries, and positive arousal affected the connectivity of the striatum, amygdala, thalamus, cerebellum, and dorsal frontal cortex. Positive valence and negative arousal had markedly smaller effects. We propose that high arousal synchronizes the listeners' sound-processing and speech-comprehension networks, whereas negative valence synchronizes circuitries supporting emotional and self-referential processing.
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spelling pubmed-42295002014-11-15 Emotional speech synchronizes brains across listeners and engages large-scale dynamic brain networks Nummenmaa, Lauri Saarimäki, Heini Glerean, Enrico Gotsopoulos, Athanasios Jääskeläinen, Iiro P. Hari, Riitta Sams, Mikko Neuroimage Article Speech provides a powerful means for sharing emotions. Here we implement novel intersubject phase synchronization and whole-brain dynamic connectivity measures to show that networks of brain areas become synchronized across participants who are listening to emotional episodes in spoken narratives. Twenty participants' hemodynamic brain activity was measured with functional magnetic resonance imaging (fMRI) while they listened to 45-s narratives describing unpleasant, neutral, and pleasant events spoken in neutral voice. After scanning, participants listened to the narratives again and rated continuously their feelings of pleasantness–unpleasantness (valence) and of arousal–calmness. Instantaneous intersubject phase synchronization (ISPS) measures were computed to derive both multi-subject voxel-wise similarity measures of hemodynamic activity and inter-area functional dynamic connectivity (seed-based phase synchronization, SBPS). Valence and arousal time series were subsequently used to predict the ISPS and SBPS time series. High arousal was associated with increased ISPS in the auditory cortices and in Broca's area, and negative valence was associated with enhanced ISPS in the thalamus, anterior cingulate, lateral prefrontal, and orbitofrontal cortices. Negative valence affected functional connectivity of fronto-parietal, limbic (insula, cingulum) and fronto-opercular circuitries, and positive arousal affected the connectivity of the striatum, amygdala, thalamus, cerebellum, and dorsal frontal cortex. Positive valence and negative arousal had markedly smaller effects. We propose that high arousal synchronizes the listeners' sound-processing and speech-comprehension networks, whereas negative valence synchronizes circuitries supporting emotional and self-referential processing. Academic Press 2014-11-15 /pmc/articles/PMC4229500/ /pubmed/25128711 http://dx.doi.org/10.1016/j.neuroimage.2014.07.063 Text en © 2014 The Authors. Published by Elsevier Inc. https://creativecommons.org/licenses/by/3.0/This work is licensed under a Creative Commons Attribution 3.0 Unported License (https://creativecommons.org/licenses/by/3.0/) .
spellingShingle Article
Nummenmaa, Lauri
Saarimäki, Heini
Glerean, Enrico
Gotsopoulos, Athanasios
Jääskeläinen, Iiro P.
Hari, Riitta
Sams, Mikko
Emotional speech synchronizes brains across listeners and engages large-scale dynamic brain networks
title Emotional speech synchronizes brains across listeners and engages large-scale dynamic brain networks
title_full Emotional speech synchronizes brains across listeners and engages large-scale dynamic brain networks
title_fullStr Emotional speech synchronizes brains across listeners and engages large-scale dynamic brain networks
title_full_unstemmed Emotional speech synchronizes brains across listeners and engages large-scale dynamic brain networks
title_short Emotional speech synchronizes brains across listeners and engages large-scale dynamic brain networks
title_sort emotional speech synchronizes brains across listeners and engages large-scale dynamic brain networks
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4229500/
https://www.ncbi.nlm.nih.gov/pubmed/25128711
http://dx.doi.org/10.1016/j.neuroimage.2014.07.063
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