Rapid encoding of musical tones discovered in whole-brain connectivity

Information encoding has received a wide neuroscientific attention, but the underlying rapid spatiotemporal brain dynamics remain largely unknown. Here, we investigated the rapid brain mechanisms for encoding of sounds forming a complex temporal sequence. Specifically, we used magnetoencephalography...

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Autores: Bonetti, Leonardo, Brattico, Elvira, Carlomagno, Francesco, Donati, Giovanni, Cabral, Jose, Haumann, Niels Trusbak, Deco, Gustavo, Vuust, Peter, Kringelbach, Morten L.
Formato: artículo
Estado:Versión publicada
Fecha de publicación:2021
País:España
Recursos:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
Repositorio:Recercat. Dipósit de la Recerca de Catalunya
OAI Identifier:oai:recercat.cat:10230/53538
Acesso em linha:http://hdl.handle.net/10230/53538
http://doi.org/10.1016/j.neuroimage.2021.118735
Access Level:acceso abierto
Palavra-chave:Sound encoding
Brain dynamics
Memory
Magnetoencephalography (MEG)
Whole-brain functional connectivity
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network_name_str España
repository_id_str
dc.title.none.fl_str_mv Rapid encoding of musical tones discovered in whole-brain connectivity
title Rapid encoding of musical tones discovered in whole-brain connectivity
spellingShingle Rapid encoding of musical tones discovered in whole-brain connectivity
Bonetti, Leonardo
Sound encoding
Brain dynamics
Memory
Magnetoencephalography (MEG)
Whole-brain functional connectivity
title_short Rapid encoding of musical tones discovered in whole-brain connectivity
title_full Rapid encoding of musical tones discovered in whole-brain connectivity
title_fullStr Rapid encoding of musical tones discovered in whole-brain connectivity
title_full_unstemmed Rapid encoding of musical tones discovered in whole-brain connectivity
title_sort Rapid encoding of musical tones discovered in whole-brain connectivity
dc.creator.none.fl_str_mv Bonetti, Leonardo
Brattico, Elvira
Carlomagno, Francesco
Donati, Giovanni
Cabral, Jose
Haumann, Niels Trusbak
Deco, Gustavo
Vuust, Peter
Kringelbach, Morten L.
author Bonetti, Leonardo
author_facet Bonetti, Leonardo
Brattico, Elvira
Carlomagno, Francesco
Donati, Giovanni
Cabral, Jose
Haumann, Niels Trusbak
Deco, Gustavo
Vuust, Peter
Kringelbach, Morten L.
author_role author
author2 Brattico, Elvira
Carlomagno, Francesco
Donati, Giovanni
Cabral, Jose
Haumann, Niels Trusbak
Deco, Gustavo
Vuust, Peter
Kringelbach, Morten L.
author2_role author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Sound encoding
Brain dynamics
Memory
Magnetoencephalography (MEG)
Whole-brain functional connectivity
topic Sound encoding
Brain dynamics
Memory
Magnetoencephalography (MEG)
Whole-brain functional connectivity
description Information encoding has received a wide neuroscientific attention, but the underlying rapid spatiotemporal brain dynamics remain largely unknown. Here, we investigated the rapid brain mechanisms for encoding of sounds forming a complex temporal sequence. Specifically, we used magnetoencephalography (MEG) to record the brain activity of 68 participants while they listened to a highly structured musical prelude. Functional connectivity analyses performed using phase synchronisation and graph theoretical measures showed a large network of brain areas recruited during encoding of sounds, comprising primary and secondary auditory cortices, frontal operculum, insula, hippocampus and basal ganglia. Moreover, our results highlighted the rapid transition of brain activity from primary auditory cortex to higher order association areas including insula and superior temporal pole within a whole-brain network, occurring during the first 220 ms of the encoding process. Further, we discovered that individual differences along cognitive abilities and musicianship modulated the degree centrality of the brain areas implicated in the encoding process. Indeed, participants with higher musical expertise presented a stronger centrality of superior temporal gyrus and insula, while individuals with high working memory abilities showed a stronger centrality of frontal operculum. In conclusion, our study revealed the rapid unfolding of brain network dynamics responsible for the encoding of sounds and their relationship with individual differences, showing a complex picture which extends beyond the well-known involvement of auditory areas. Indeed, our results expanded our understanding of the general mechanisms underlying auditory pattern encoding in the human brain
publishDate 2021
dc.date.none.fl_str_mv 2021
2022
2022
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10230/53538
http://doi.org/10.1016/j.neuroimage.2021.118735
url http://hdl.handle.net/10230/53538
http://doi.org/10.1016/j.neuroimage.2021.118735
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv NeuroImage. 2021;245:118735.
info:eu-repo/grantAgreement/EC/H2020/720270
info:eu-repo/grantAgreement/ES/1PE/PSI2016-75688-P
info:eu-repo/grantAgreement/EC/H2020/720270
info:eu-repo/grantAgreement/EC/H2020/785907
dc.rights.none.fl_str_mv http://creativecommons.org/licenses/by-nc-nd/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by-nc-nd/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
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dc.publisher.none.fl_str_mv Elsevier
publisher.none.fl_str_mv Elsevier
dc.source.none.fl_str_mv reponame:Recercat. Dipósit de la Recerca de Catalunya
instname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
instname_str Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
reponame_str Recercat. Dipósit de la Recerca de Catalunya
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spelling Rapid encoding of musical tones discovered in whole-brain connectivityBonetti, LeonardoBrattico, ElviraCarlomagno, FrancescoDonati, GiovanniCabral, JoseHaumann, Niels TrusbakDeco, GustavoVuust, PeterKringelbach, Morten L.Sound encodingBrain dynamicsMemoryMagnetoencephalography (MEG)Whole-brain functional connectivityInformation encoding has received a wide neuroscientific attention, but the underlying rapid spatiotemporal brain dynamics remain largely unknown. Here, we investigated the rapid brain mechanisms for encoding of sounds forming a complex temporal sequence. Specifically, we used magnetoencephalography (MEG) to record the brain activity of 68 participants while they listened to a highly structured musical prelude. Functional connectivity analyses performed using phase synchronisation and graph theoretical measures showed a large network of brain areas recruited during encoding of sounds, comprising primary and secondary auditory cortices, frontal operculum, insula, hippocampus and basal ganglia. Moreover, our results highlighted the rapid transition of brain activity from primary auditory cortex to higher order association areas including insula and superior temporal pole within a whole-brain network, occurring during the first 220 ms of the encoding process. Further, we discovered that individual differences along cognitive abilities and musicianship modulated the degree centrality of the brain areas implicated in the encoding process. Indeed, participants with higher musical expertise presented a stronger centrality of superior temporal gyrus and insula, while individuals with high working memory abilities showed a stronger centrality of frontal operculum. In conclusion, our study revealed the rapid unfolding of brain network dynamics responsible for the encoding of sounds and their relationship with individual differences, showing a complex picture which extends beyond the well-known involvement of auditory areas. Indeed, our results expanded our understanding of the general mechanisms underlying auditory pattern encoding in the human brainThe Center for Music in the Brain (MIB) is funded by the Danish National Research Foundation (project number DNRF117). LB is supported by Carlsberg Foundation (project number CF20-0239), Center for Music in the Brain and Linacre College of the University of Oxford. MLK is supported by the ERC Consolidator Grant: CAREGIVING (n. 615539), Center for Music in the Brain, and Center for Eudaimonia and Human Flourishing funded by the Pettit and Carlsberg Foundations. GD is supported by the Spanish Research Project PSI2016–75688-P (AEI/FEDER, EU), by the European Union's Horizon 2020 Research and Innovation Programme under grant agreements n. 720270 (HBP SGA1) and n. 785907 (HBP SGA2), and by the Catalan AGAUR Programme 2017 SGR 1545. JC is supported by Portuguese Foundation for Science and Technology CEECIND/03325/2017, Portugal. Additionally, we thank the Italian section of Mensa: The International High IQ Society for the economic support provided to the author Francesco Carlomagno and the University of Bologna for the economic support provided to the author Giulia Donati and the student assistants Riccardo Proietti and Giulio Carraturo.Elsevier202220222021info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttp://hdl.handle.net/10230/53538http://doi.org/10.1016/j.neuroimage.2021.118735reponame:Recercat. Dipósit de la Recerca de Catalunyainstname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)InglésNeuroImage. 2021;245:118735.info:eu-repo/grantAgreement/EC/H2020/720270info:eu-repo/grantAgreement/ES/1PE/PSI2016-75688-Pinfo:eu-repo/grantAgreement/EC/H2020/720270info:eu-repo/grantAgreement/EC/H2020/785907© 2021 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/)http://creativecommons.org/licenses/by-nc-nd/4.0/info:eu-repo/semantics/openAccessoai:recercat.cat:10230/535382026-05-29T05:05:01Z
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