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Autistic traits, resting-state connectivity, and absolute pitch in professional musicians: shared and distinct neural features

BACKGROUND: Recent studies indicate increased autistic traits in musicians with absolute pitch and a higher proportion of absolute pitch in people with autism. Theoretical accounts connect both of these with shared neural principles of local hyper- and global hypoconnectivity, enhanced perceptual fu...

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Autores principales: Wenhart, T., Bethlehem, R. A. I., Baron-Cohen, S., Altenmüller, E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6498518/
https://www.ncbi.nlm.nih.gov/pubmed/31073395
http://dx.doi.org/10.1186/s13229-019-0272-6
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author Wenhart, T.
Bethlehem, R. A. I.
Baron-Cohen, S.
Altenmüller, E.
author_facet Wenhart, T.
Bethlehem, R. A. I.
Baron-Cohen, S.
Altenmüller, E.
author_sort Wenhart, T.
collection PubMed
description BACKGROUND: Recent studies indicate increased autistic traits in musicians with absolute pitch and a higher proportion of absolute pitch in people with autism. Theoretical accounts connect both of these with shared neural principles of local hyper- and global hypoconnectivity, enhanced perceptual functioning, and a detail-focused cognitive style. This is the first study to investigate absolute pitch proficiency, autistic traits, and brain correlates in the same study. SAMPLE AND METHODS: Graph theoretical analysis was conducted on resting-state (eyes closed and eyes open) EEG connectivity (wPLI, weighted phase lag index) matrices obtained from 31 absolute pitch (AP) and 33 relative pitch (RP) professional musicians. Small-worldness, global clustering coefficient, and average path length were related to autistic traits, passive (tone identification) and active (pitch adjustment) absolute pitch proficiency, and onset of musical training using Welch two-sample tests, correlations, and general linear models. RESULTS: Analyses revealed increased path length (delta 2–4 Hz), reduced clustering (beta 13–18 Hz), reduced small-worldness (gamma 30–60 Hz), and increased autistic traits for AP compared to RP. Only clustering values (beta 13–18 Hz) were predicted by both AP proficiency and autistic traits. Post hoc single connection permutation tests among raw wPLI matrices in the beta band (13–18 Hz) revealed widely reduced interhemispheric connectivity between bilateral auditory-related electrode positions along with higher connectivity between F7–F8 and F8–P9 for AP. Pitch-naming ability and pitch adjustment ability were predicted by path length, clustering, autistic traits, and onset of musical training (for pitch adjustment) explaining 44% and 38% of variance, respectively. CONCLUSIONS: Results show both shared and distinct neural features between AP and autistic traits. Differences in the beta range were associated with higher autistic traits in the same population. In general, AP musicians exhibit a widely underconnected brain with reduced functional integration and reduced small-world property during resting state. This might be partly related to autism-specific brain connectivity, while differences in path length and small-worldness reflect other ability-specific influences. This is further evidenced for different pathways in the acquisition and development of absolute pitch, likely influenced by both genetic and environmental factors and their interaction.
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spelling pubmed-64985182019-05-09 Autistic traits, resting-state connectivity, and absolute pitch in professional musicians: shared and distinct neural features Wenhart, T. Bethlehem, R. A. I. Baron-Cohen, S. Altenmüller, E. Mol Autism Research BACKGROUND: Recent studies indicate increased autistic traits in musicians with absolute pitch and a higher proportion of absolute pitch in people with autism. Theoretical accounts connect both of these with shared neural principles of local hyper- and global hypoconnectivity, enhanced perceptual functioning, and a detail-focused cognitive style. This is the first study to investigate absolute pitch proficiency, autistic traits, and brain correlates in the same study. SAMPLE AND METHODS: Graph theoretical analysis was conducted on resting-state (eyes closed and eyes open) EEG connectivity (wPLI, weighted phase lag index) matrices obtained from 31 absolute pitch (AP) and 33 relative pitch (RP) professional musicians. Small-worldness, global clustering coefficient, and average path length were related to autistic traits, passive (tone identification) and active (pitch adjustment) absolute pitch proficiency, and onset of musical training using Welch two-sample tests, correlations, and general linear models. RESULTS: Analyses revealed increased path length (delta 2–4 Hz), reduced clustering (beta 13–18 Hz), reduced small-worldness (gamma 30–60 Hz), and increased autistic traits for AP compared to RP. Only clustering values (beta 13–18 Hz) were predicted by both AP proficiency and autistic traits. Post hoc single connection permutation tests among raw wPLI matrices in the beta band (13–18 Hz) revealed widely reduced interhemispheric connectivity between bilateral auditory-related electrode positions along with higher connectivity between F7–F8 and F8–P9 for AP. Pitch-naming ability and pitch adjustment ability were predicted by path length, clustering, autistic traits, and onset of musical training (for pitch adjustment) explaining 44% and 38% of variance, respectively. CONCLUSIONS: Results show both shared and distinct neural features between AP and autistic traits. Differences in the beta range were associated with higher autistic traits in the same population. In general, AP musicians exhibit a widely underconnected brain with reduced functional integration and reduced small-world property during resting state. This might be partly related to autism-specific brain connectivity, while differences in path length and small-worldness reflect other ability-specific influences. This is further evidenced for different pathways in the acquisition and development of absolute pitch, likely influenced by both genetic and environmental factors and their interaction. BioMed Central 2019-05-02 /pmc/articles/PMC6498518/ /pubmed/31073395 http://dx.doi.org/10.1186/s13229-019-0272-6 Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Wenhart, T.
Bethlehem, R. A. I.
Baron-Cohen, S.
Altenmüller, E.
Autistic traits, resting-state connectivity, and absolute pitch in professional musicians: shared and distinct neural features
title Autistic traits, resting-state connectivity, and absolute pitch in professional musicians: shared and distinct neural features
title_full Autistic traits, resting-state connectivity, and absolute pitch in professional musicians: shared and distinct neural features
title_fullStr Autistic traits, resting-state connectivity, and absolute pitch in professional musicians: shared and distinct neural features
title_full_unstemmed Autistic traits, resting-state connectivity, and absolute pitch in professional musicians: shared and distinct neural features
title_short Autistic traits, resting-state connectivity, and absolute pitch in professional musicians: shared and distinct neural features
title_sort autistic traits, resting-state connectivity, and absolute pitch in professional musicians: shared and distinct neural features
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6498518/
https://www.ncbi.nlm.nih.gov/pubmed/31073395
http://dx.doi.org/10.1186/s13229-019-0272-6
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