Short communication: Lifetime musical activity and resting-state functional connectivity in cognitive networks.


Journal

PloS one
ISSN: 1932-6203
Titre abrégé: PLoS One
Pays: United States
ID NLM: 101285081

Informations de publication

Date de publication:
2024
Historique:
received: 27 07 2023
accepted: 20 02 2024
medline: 2 5 2024
pubmed: 2 5 2024
entrez: 2 5 2024
Statut: epublish

Résumé

Participation in multimodal leisure activities, such as playing a musical instrument, may be protective against brain aging and dementia in older adults (OA). Potential neuroprotective correlates underlying musical activity remain unclear. This cross-sectional study investigated the association between lifetime musical activity and resting-state functional connectivity (RSFC) in three higher-order brain networks: the Default Mode, Fronto-Parietal, and Salience networks. We assessed 130 cognitively unimpaired participants (≥ 60 years) from the baseline cohort of the DZNE-Longitudinal Cognitive Impairment and Dementia Study (DELCODE) study. Lifetime musical activity was operationalized by the self-reported participation in musical instrument playing across early, middle, and late life stages using the Lifetime of Experiences Questionnaire (LEQ). Participants who reported musical activity during all life stages (n = 65) were compared to controls who were matched on demographic and reserve characteristics (including education, intelligence, socioeconomic status, self-reported physical activity, age, and sex) and never played a musical instrument (n = 65) in local (seed-to-voxel) and global (within-network and between-network) RSFC patterns using pre-specified network seeds. Older participants with lifetime musical activity showed significantly higher local RSFC between the medial prefrontal cortex (Default Mode Network seed) and temporal as well as frontal regions, namely the right temporal pole and the right precentral gyrus extending into the superior frontal gyrus, compared to matched controls. There were no significant group differences in global RSFC within or between the three networks. We show that playing a musical instrument during life relates to higher RSFC of the medial prefrontal cortex with distant brain regions involved in higher-order cognitive and motor processes. Preserved or enhanced functional connectivity could potentially contribute to better brain health and resilience in OA with a history in musical activity. German Clinical Trials Register (DRKS00007966, 04/05/2015).

Sections du résumé

BACKGROUND BACKGROUND
Participation in multimodal leisure activities, such as playing a musical instrument, may be protective against brain aging and dementia in older adults (OA). Potential neuroprotective correlates underlying musical activity remain unclear.
OBJECTIVE OBJECTIVE
This cross-sectional study investigated the association between lifetime musical activity and resting-state functional connectivity (RSFC) in three higher-order brain networks: the Default Mode, Fronto-Parietal, and Salience networks.
METHODS METHODS
We assessed 130 cognitively unimpaired participants (≥ 60 years) from the baseline cohort of the DZNE-Longitudinal Cognitive Impairment and Dementia Study (DELCODE) study. Lifetime musical activity was operationalized by the self-reported participation in musical instrument playing across early, middle, and late life stages using the Lifetime of Experiences Questionnaire (LEQ). Participants who reported musical activity during all life stages (n = 65) were compared to controls who were matched on demographic and reserve characteristics (including education, intelligence, socioeconomic status, self-reported physical activity, age, and sex) and never played a musical instrument (n = 65) in local (seed-to-voxel) and global (within-network and between-network) RSFC patterns using pre-specified network seeds.
RESULTS RESULTS
Older participants with lifetime musical activity showed significantly higher local RSFC between the medial prefrontal cortex (Default Mode Network seed) and temporal as well as frontal regions, namely the right temporal pole and the right precentral gyrus extending into the superior frontal gyrus, compared to matched controls. There were no significant group differences in global RSFC within or between the three networks.
CONCLUSION CONCLUSIONS
We show that playing a musical instrument during life relates to higher RSFC of the medial prefrontal cortex with distant brain regions involved in higher-order cognitive and motor processes. Preserved or enhanced functional connectivity could potentially contribute to better brain health and resilience in OA with a history in musical activity.
TRIAL REGISTRATION BACKGROUND
German Clinical Trials Register (DRKS00007966, 04/05/2015).

Identifiants

pubmed: 38696395
doi: 10.1371/journal.pone.0299939
pii: PONE-D-23-20713
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e0299939

Informations de copyright

Copyright: © 2024 Liebscher et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Déclaration de conflit d'intérêts

O. Peters received fees for consultation from Abbvie, Biogen, Eisai, Griffols, MSD Roche, and Schwabe. J. Priller received fees for consultation, lectures, and patents from Neurimmune, Axon, Desitin, and Epomedics. J. Wiltfang is an advisory board member of Abbott, Biogen, Boehringer Ingelheim, Immunogenetics, Lilly, MSD Sharp & Dohme, and Roche Pharma and received honoraria for lectures from Actelion, Amgen, Beeijing Yibai Science and Technology Ltd., Janssen Cilag, Med Update GmbH, Pfizer, Roche Pharma and holds the following patents: PCT/EP 2011 001724 and PCT/EP 2015 052945. J. Wiltfang is supported by an Ilidio Pinho professorship, iBiMED (UIDB/04501/2020) at the University of Aveiro, Portugal. E. Düzel received fees for consultation from Roche, Biogen, RoxHealth and holds shares in neotiv. F. Jessen received fees for consultation from Eli Lilly, Novartis, Roche, BioGene, MSD, Piramal, Janssen, and Lundbeck. The remaining authors report no conflicts of interest. This does not alter our adherence to PLOS ONE policies on sharing data and materials.

Auteurs

Maxie Liebscher (M)

German Center for Neurodegenerative Diseases (DZNE), Dresden, Germany.

Andrea Dell'Orco (A)

German Center for Neurodegenerative Diseases (DZNE), Dresden, Germany.
Department of Neuroradiology, Charité -Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt- Universität zu Berlin, Berlin, Germany.

Johanna Doll-Lee (J)

Department of Neurology, Hannover Medical School, Hannover, Germany.

Katharina Buerger (K)

German Center for Neurodegenerative Diseases (DZNE), Munich, Germany.
Institute for Stroke and Dementia Research (ISD), University Hospital, LMU Munich, Munich, Germany.

Peter Dechent (P)

Department of Cognitive Neurology, MR-Research in Neurosciences, Georg-August-University Goettingen, Göttingen, Germany.

Michael Ewers (M)

German Center for Neurodegenerative Diseases (DZNE), Munich, Germany.

Klaus Fliessbach (K)

German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany.
Department of Neurodegenerative Disease and Geriatric Psychiatry/Psychiatry, University of Bonn Medical Center, Bonn, Germany.

Wenzel Glanz (W)

German Center for Neurodegenerative Diseases (DZNE), Magdeburg, Germany.

Stefan Hetzer (S)

Center for Advanced Neuroimaging, Charité -Universitätsmedizin Berlin, Berlin, Germany.

Daniel Janowitz (D)

Institute for Stroke and Dementia Research (ISD), University Hospital, LMU Munich, Munich, Germany.

Ingo Kilimann (I)

German Center for Neurodegenerative Diseases (DZNE), Rostock, Germany.
Department of Psychosomatic Medicine, Rostock University Medical Center, Rostock, Germany.

Christoph Laske (C)

German Center for Neurodegenerative Diseases (DZNE), Tübingen, Germany.
Section for Dementia Research, Hertie Institute for Clinical Brain Research and Department of Psychiatry and Psychotherapy, University of Tübingen, Tübingen, Germany.

Falk Lüsebrink (F)

German Center for Neurodegenerative Diseases (DZNE), Magdeburg, Germany.

Matthias Munk (M)

German Center for Neurodegenerative Diseases (DZNE), Tübingen, Germany.
Department of Psychiatry and Psychotherapy, University of Tübingen, Tübingen, Germany.

Robert Perneczky (R)

German Center for Neurodegenerative Diseases (DZNE), Munich, Germany.
Department of Psychiatry and Psychotherapy, University Hospital, LMU Munich, Munich, Germany.
Munich Cluster for Systems Neurology (SyNergy) Munich, Munich, Germany.
Ageing Epidemiology Research Unit (AGE), School of Public Health, Imperial College London, London, United Kingdom.

Oliver Peters (O)

German Center for Neurodegenerative Diseases (DZNE), Berlin, Germany.
Institute of Psychiatry and Psychotherapy, Charité -Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany.

Lukas Preis (L)

Institute of Psychiatry and Psychotherapy, Charité -Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany.

Josef Priller (J)

German Center for Neurodegenerative Diseases (DZNE), Berlin, Germany.
Department of Psychiatry and Psychotherapy, Charité -Universitätsmedizin Berlin, Berlin, Germany.
Department of Psychiatry and Psychotherapy, School of Medicine, Technical University of Munich, Munich, Germany.
University of Edinburgh and UK DRI, Edinburgh, United Kingdom.

Boris Rauchmann (B)

Department of Psychiatry and Psychotherapy, University Hospital, LMU Munich, Munich, Germany.
Sheffield Institute for Translational Neuroscience (SITraN), University of Sheffield, Sheffield, United Kingdom.
Department of Neuroradiology, University Hospital LMU, Munich, Germany.

Ayda Rostamzadeh (A)

Department of Psychiatry, University of Cologne, Medical Faculty, Cologne, Germany.

Nina Roy-Kluth (N)

German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany.

Klaus Scheffler (K)

Department for Biomedical Magnetic Resonance, University of Tübingen, Tübingen, Germany.

Anja Schneider (A)

German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany.
Department of Neurodegenerative Disease and Geriatric Psychiatry/Psychiatry, University of Bonn Medical Center, Bonn, Germany.

Björn H Schott (BH)

Department of Psychiatry and Psychotherapy, University Medical Center Goettingen, University of Goettingen, Goettingen, Germany.
German Center for Neurodegenerative Diseases (DZNE), Goettingen, Germany.

Annika Spottke (A)

German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany.
Department of Neurology, University of Bonn, Bonn, Germany.

Eike Spruth (E)

German Center for Neurodegenerative Diseases (DZNE), Berlin, Germany.
Department of Psychiatry and Psychotherapy, Charité -Universitätsmedizin Berlin, Berlin, Germany.

Stefan Teipel (S)

German Center for Neurodegenerative Diseases (DZNE), Rostock, Germany.
Department of Psychosomatic Medicine, Rostock University Medical Center, Rostock, Germany.

Jens Wiltfang (J)

Department of Psychiatry and Psychotherapy, University Medical Center Goettingen, University of Goettingen, Goettingen, Germany.
German Center for Neurodegenerative Diseases (DZNE), Goettingen, Germany.
Department of Medical Sciences, Neurosciences and Signaling Group, Institute of Biomedicine (iBiMED), University of Aveiro, Aveiro, Portugal.

Frank Jessen (F)

Department of Psychiatry, University of Cologne, Medical Faculty, Cologne, Germany.
Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases (CECAD), University of Cologne, Cologne, Germany.
German Center for Neurodegenerative Diseases (DZNE), Cologne, Germany.

Emrah Düzel (E)

German Center for Neurodegenerative Diseases (DZNE), Magdeburg, Germany.
Institute of Cognitive Neurology and Dementia Research (IKND), Otto-von-Guericke University, Magdeburg, Germany.

Michael Wagner (M)

German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany.
Department of Neurodegenerative Disease and Geriatric Psychiatry/Psychiatry, University of Bonn Medical Center, Bonn, Germany.

Sandra Röske (S)

German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany.

Miranka Wirth (M)

German Center for Neurodegenerative Diseases (DZNE), Dresden, Germany.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH