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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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.
•We model how emotional speech synchronizes brains across listeners.•Participants listened to emotional and neutral narratives during fMRI scan.•Arousal synchronized auditory cortices and Broca's area.•Valence synchronized limbic system, prefrontal, and orbitofrontal cortices.•Valence and arousal triggered distinct patterns of dynamic functional connectivity. |
doi_str_mv | 10.1016/j.neuroimage.2014.07.063 |
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•We model how emotional speech synchronizes brains across listeners.•Participants listened to emotional and neutral narratives during fMRI scan.•Arousal synchronized auditory cortices and Broca's area.•Valence synchronized limbic system, prefrontal, and orbitofrontal cortices.•Valence and arousal triggered distinct patterns of dynamic functional connectivity.</description><identifier>ISSN: 1053-8119</identifier><identifier>EISSN: 1095-9572</identifier><identifier>DOI: 10.1016/j.neuroimage.2014.07.063</identifier><identifier>PMID: 25128711</identifier><language>eng</language><publisher>Amsterdam: Elsevier Inc</publisher><subject>Adult ; Affect - physiology ; Arousal ; Biological and medical sciences ; Brain ; Brain - physiology ; Brain Mapping ; Connectivity ; Electroencephalography Phase Synchronization ; Emotion ; Emotions ; Evoked Potentials, Auditory ; Female ; Fundamental and applied biological sciences. Psychology ; Humans ; Language ; Listening ; Magnetic Resonance Imaging ; Male ; Medical imaging ; Narratives ; Nerve Net - physiology ; Network ; Social interaction ; Speech - physiology ; Speech comprehension ; Speech Perception - physiology ; Synchronization ; Vertebrates: nervous system and sense organs ; Young Adult</subject><ispartof>NeuroImage (Orlando, Fla.), 2014-11, Vol.102, p.498-509</ispartof><rights>2014</rights><rights>2015 INIST-CNRS</rights><rights>Copyright © 2014. Published by Elsevier Inc.</rights><rights>Copyright Elsevier Limited Nov 15, 2014</rights><rights>2014 The Authors. Published by Elsevier Inc. 2014</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c570t-c89fcca449fb0f59cf6bbaf194082b9cfce13d7b2d0b46a8f2e2c39dd8ee63af3</citedby><cites>FETCH-LOGICAL-c570t-c89fcca449fb0f59cf6bbaf194082b9cfce13d7b2d0b46a8f2e2c39dd8ee63af3</cites><orcidid>0000-0002-2497-9757 ; 0000-0003-0624-675X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.proquest.com/docview/1625937444?pq-origsite=primo$$EHTML$$P50$$Gproquest$$H</linktohtml><link.rule.ids>230,315,782,786,887,3552,27931,27932,46002,64392,64394,64396,72476</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=29053787$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25128711$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Nummenmaa, Lauri</creatorcontrib><creatorcontrib>Saarimäki, Heini</creatorcontrib><creatorcontrib>Glerean, Enrico</creatorcontrib><creatorcontrib>Gotsopoulos, Athanasios</creatorcontrib><creatorcontrib>Jääskeläinen, Iiro P.</creatorcontrib><creatorcontrib>Hari, Riitta</creatorcontrib><creatorcontrib>Sams, Mikko</creatorcontrib><title>Emotional speech synchronizes brains across listeners and engages large-scale dynamic brain networks</title><title>NeuroImage (Orlando, Fla.)</title><addtitle>Neuroimage</addtitle><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.
•We model how emotional speech synchronizes brains across listeners.•Participants listened to emotional and neutral narratives during fMRI scan.•Arousal synchronized auditory cortices and Broca's area.•Valence synchronized limbic system, prefrontal, and orbitofrontal cortices.•Valence and arousal triggered distinct patterns of dynamic functional connectivity.</description><subject>Adult</subject><subject>Affect - physiology</subject><subject>Arousal</subject><subject>Biological and medical sciences</subject><subject>Brain</subject><subject>Brain - physiology</subject><subject>Brain Mapping</subject><subject>Connectivity</subject><subject>Electroencephalography Phase Synchronization</subject><subject>Emotion</subject><subject>Emotions</subject><subject>Evoked Potentials, Auditory</subject><subject>Female</subject><subject>Fundamental and applied biological sciences. 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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.
•We model how emotional speech synchronizes brains across listeners.•Participants listened to emotional and neutral narratives during fMRI scan.•Arousal synchronized auditory cortices and Broca's area.•Valence synchronized limbic system, prefrontal, and orbitofrontal cortices.•Valence and arousal triggered distinct patterns of dynamic functional connectivity.</abstract><cop>Amsterdam</cop><pub>Elsevier Inc</pub><pmid>25128711</pmid><doi>10.1016/j.neuroimage.2014.07.063</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0002-2497-9757</orcidid><orcidid>https://orcid.org/0000-0003-0624-675X</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Adult Affect - physiology Arousal Biological and medical sciences Brain Brain - physiology Brain Mapping Connectivity Electroencephalography Phase Synchronization Emotion Emotions Evoked Potentials, Auditory Female Fundamental and applied biological sciences. Psychology Humans Language Listening Magnetic Resonance Imaging Male Medical imaging Narratives Nerve Net - physiology Network Social interaction Speech - physiology Speech comprehension Speech Perception - physiology Synchronization Vertebrates: nervous system and sense organs Young Adult |
title | Emotional speech synchronizes brains across listeners and engages large-scale dynamic brain networks |
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