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Research Articles, Behavioral/Cognitive

Multimodal Imaging Brain Markers in Early Adolescence Are Linked with a Physically Active Lifestyle

Piergiorgio Salvan, Thomas Wassenaar, Catherine Wheatley, Nicholas Beale, Michiel Cottaar, Daniel Papp, Matteo Bastiani, Sean Fitzgibbon, Euguene Duff, Jesper Andersson, Anderson M. Winkler, Gwenaëlle Douaud, Thomas E. Nichols, Stephen Smith, Helen Dawes and Heidi Johansen-Berg
Journal of Neuroscience 12 January 2021, JN-RM-1260-20; DOI: https://doi.org/10.1523/JNEUROSCI.1260-20.2020
Piergiorgio Salvan
1Wellcome Centre for Integrative Neuroimaging, FMRIB Centre, Nuffield Department of Clinical Neurosciences, University of Oxford, John Radcliffe Hospital, Oxford, OX3 9DU, United Kingdom
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Thomas Wassenaar
1Wellcome Centre for Integrative Neuroimaging, FMRIB Centre, Nuffield Department of Clinical Neurosciences, University of Oxford, John Radcliffe Hospital, Oxford, OX3 9DU, United Kingdom
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Catherine Wheatley
1Wellcome Centre for Integrative Neuroimaging, FMRIB Centre, Nuffield Department of Clinical Neurosciences, University of Oxford, John Radcliffe Hospital, Oxford, OX3 9DU, United Kingdom
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Nicholas Beale
2Centre for Movement, Occupational and Rehabilitation Sciences, Oxford Brookes University, Oxford, OX3 0BP, United Kingdom
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Michiel Cottaar
1Wellcome Centre for Integrative Neuroimaging, FMRIB Centre, Nuffield Department of Clinical Neurosciences, University of Oxford, John Radcliffe Hospital, Oxford, OX3 9DU, United Kingdom
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Daniel Papp
1Wellcome Centre for Integrative Neuroimaging, FMRIB Centre, Nuffield Department of Clinical Neurosciences, University of Oxford, John Radcliffe Hospital, Oxford, OX3 9DU, United Kingdom
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Matteo Bastiani
1Wellcome Centre for Integrative Neuroimaging, FMRIB Centre, Nuffield Department of Clinical Neurosciences, University of Oxford, John Radcliffe Hospital, Oxford, OX3 9DU, United Kingdom
3Sir Peter Mansfield Imaging Centre, School of Medicine, University of Nottingham, Nottingham, NG7 2RD, United Kingdom
4National Institute for Health Research Biomedical Research Centre, University of Nottingham, Nottingham, NG7 2UH, United Kingdom
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Sean Fitzgibbon
1Wellcome Centre for Integrative Neuroimaging, FMRIB Centre, Nuffield Department of Clinical Neurosciences, University of Oxford, John Radcliffe Hospital, Oxford, OX3 9DU, United Kingdom
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Euguene Duff
1Wellcome Centre for Integrative Neuroimaging, FMRIB Centre, Nuffield Department of Clinical Neurosciences, University of Oxford, John Radcliffe Hospital, Oxford, OX3 9DU, United Kingdom
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Jesper Andersson
1Wellcome Centre for Integrative Neuroimaging, FMRIB Centre, Nuffield Department of Clinical Neurosciences, University of Oxford, John Radcliffe Hospital, Oxford, OX3 9DU, United Kingdom
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Anderson M. Winkler
5Emotion and Development Branch, National Institute of Mental Health, National Institutes of Health, Bethesda, MD 20892-9663, Maryland
6Department of Psychiatry, Yale University School of Medicine, New Haven, CT 06511, Connecticut
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Gwenaëlle Douaud
1Wellcome Centre for Integrative Neuroimaging, FMRIB Centre, Nuffield Department of Clinical Neurosciences, University of Oxford, John Radcliffe Hospital, Oxford, OX3 9DU, United Kingdom
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Thomas E. Nichols
1Wellcome Centre for Integrative Neuroimaging, FMRIB Centre, Nuffield Department of Clinical Neurosciences, University of Oxford, John Radcliffe Hospital, Oxford, OX3 9DU, United Kingdom
7Oxford Big Data Institute, Li Ka Shing Centre for Health Information and Discovery, Nuffield Department of Population Health, University of Oxford, Oxford, OX3 7LF, United Kingdom
8Department of Statistics, University of Warwick, Coventry, CV4 7AL, United Kingdom
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Stephen Smith
1Wellcome Centre for Integrative Neuroimaging, FMRIB Centre, Nuffield Department of Clinical Neurosciences, University of Oxford, John Radcliffe Hospital, Oxford, OX3 9DU, United Kingdom
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Helen Dawes
2Centre for Movement, Occupational and Rehabilitation Sciences, Oxford Brookes University, Oxford, OX3 0BP, United Kingdom
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Heidi Johansen-Berg
1Wellcome Centre for Integrative Neuroimaging, FMRIB Centre, Nuffield Department of Clinical Neurosciences, University of Oxford, John Radcliffe Hospital, Oxford, OX3 9DU, United Kingdom
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Abstract

The World Health Organization promotes physical exercise and a healthy lifestyle as means to improve youth development. However, relationships between physical lifestyle and human brain development are not fully understood. Here, we asked whether a human brain–physical latent mode of covariation underpins the relationship between physical activity, fitness, and physical health measures with multimodal neuroimaging markers. In 50 12-year old school pupils (26 females), we acquired multimodal whole-brain MRI, characterizing brain structure, microstructure, function, myelin content, and blood perfusion. We also acquired physical variables measuring objective fitness levels, 7 d physical activity, body mass index, heart rate, and blood pressure. Using canonical correlation analysis, we unravel a latent mode of brain–physical covariation, independent of demographics, school, or socioeconomic status. We show that MRI metrics with greater involvement in this mode also showed spatially extended patterns across the brain. Specifically, global patterns of greater gray matter perfusion, volume, cortical surface area, greater white matter extra-neurite density, and resting state networks activity covaried positively with measures reflecting a physically active phenotype (high fit, low sedentary individuals). Showing that a physically active lifestyle is linked with systems-level brain MRI metrics, these results suggest widespread associations relating to several biological processes. These results support the notion of close brain-body relationships and underline the importance of investigating modifiable lifestyle factors not only for physical health but also for brain health early in adolescence.

Significance Statement An active lifestyle is key for healthy development. In this work, we answer the following question: How do brain neuroimaging markers relate with young adolescents’ level of physical activity, fitness, and physical health? Combining advanced whole-brain multimodal MRI metrics with computational approaches, we show a robust relationship between physically active lifestyles and spatially extended, multimodal brain imaging-derived phenotypes. Suggesting a wider effect on brain neuroimaging metrics than previously thought, this work underlies the importance of studying physical lifestyle, as well as other brain–body relationships in an effort to foster brain health at this crucial stage in development.

Footnotes

  • Fit to Study was supported by the Education Endowment Foundation and Wellcome Trust Education and Neuroscience Program Grant 2681. H.J.-B. was supported by Wellcome Trust 110027/Z/15/Z and Oxford National Institute for Health Research Biomedical Research Center. G.D. was supported by the United Kingdom Medical Research Council MR/K006673/1. T.E.N. was supported by Wellcome Trust 100309/Z/12/Z. The Wellcome Center for Integrative Neuroimaging was supported by core funding from Wellcome Trust 203139/Z/16/Z. We thank all the Fit to Study investigators (https://www.fit-to-study.org/investigators) for contributions to the trial; Emma Eldridge, Emily Plester, Emily Curtis, Andy Meaney, Patrick Esser, Johnny Collett, Thomas Smejka, Jack Possee, Oliver Bushnell, Eneid Leika, and Cyrus Goodger for help with data collection; and all of the pupils, and their parents, who took part in, and fully engaged with, each aspect of this brain imaging substudy.

  • The authors declare no competing financial interests.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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Multimodal Imaging Brain Markers in Early Adolescence Are Linked with a Physically Active Lifestyle
Piergiorgio Salvan, Thomas Wassenaar, Catherine Wheatley, Nicholas Beale, Michiel Cottaar, Daniel Papp, Matteo Bastiani, Sean Fitzgibbon, Euguene Duff, Jesper Andersson, Anderson M. Winkler, Gwenaëlle Douaud, Thomas E. Nichols, Stephen Smith, Helen Dawes, Heidi Johansen-Berg
Journal of Neuroscience 12 January 2021, JN-RM-1260-20; DOI: 10.1523/JNEUROSCI.1260-20.2020

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Multimodal Imaging Brain Markers in Early Adolescence Are Linked with a Physically Active Lifestyle
Piergiorgio Salvan, Thomas Wassenaar, Catherine Wheatley, Nicholas Beale, Michiel Cottaar, Daniel Papp, Matteo Bastiani, Sean Fitzgibbon, Euguene Duff, Jesper Andersson, Anderson M. Winkler, Gwenaëlle Douaud, Thomas E. Nichols, Stephen Smith, Helen Dawes, Heidi Johansen-Berg
Journal of Neuroscience 12 January 2021, JN-RM-1260-20; DOI: 10.1523/JNEUROSCI.1260-20.2020
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