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Neural Scaffolding as the Foundation for Stable Performance of Aging Cerebellum

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Abstract

Although recently conceptualized as a neural node essential for a vast spectrum of associative and cognitive processes, the cerebellum has largely eluded attention in the research of aging, where it is marginalized mainly to structural analyses. In the current cross-sectional study of 67 healthy subjects of various ages (20 to 76 years), we sought to provide a comprehensive, multimodal account of age-related changes in the cerebellum during predictive motor timing, which was previously shown to engage this structure. We combined behavioral assessments of performance with functional MRI and voxel-based morphometry using an advanced method to avoid cerebellar deformation and registration imprecisions inherent to the standard processing at the whole-brain level. Higher age was surprisingly associated with stable behavioral performance during predictive motor timing, despite the massive decrease of infratentorial gray matter volume of a far higher extent than in the supratentorial region, affecting mainly the posterior cerebellar lobe. Nonetheless, this very area showed extensive hyperactivation directly correlated with age. The same region had decreased connectivity with the left caudate and increased connectivity with the left fusiform gyrus, the right pallidum, the hippocampus, and the lingual gyrus. Hence, we propose to extend the scaffolding theory of aging, previously limited mainly to the frontal cortices, to include also the cerebellum, which is likewise suffering from atrophy to a far greater extent than the rest of the brain and is similarly counteracting it by bilateral hyperactivation.

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Abbreviations

MRI:

Magnetic resonance imaging

fMRI:

Functional magnetic resonance imaging

VBM:

Voxel-based morphometry

BOLD:

Blood-oxygen-level dependent

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Acknowledgments

The authors are grateful to the patients and their families for their support of this research.

Funding

This work was supported by the EU H2020 Marie Skłodowska RISE project #691110 (MICROBRADAM).

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Authors and Affiliations

  1. Center for Magnetic Resonance Research (CMRR), University of Minnesota, Minneapolis, MN, USA

    Pavel Filip

  2. First Department of Neurology, Faculty of Medicine, University Hospital of St. Anne, Masaryk University, Brno, Czech Republic

    Pavel Filip & Martin Bareš

  3. Institut du Cerveau et de la Moelle épinière—ICM, Centre de NeuroImagerie de Recherche, Sorbonne Université UMR S1127, Inserm U1127, CNRS 7225, Paris, France

    Cécile Gallea & Stéphane Lehéricy

  4. Department of Psychiatry, Université de Montréal, Montréal, Québec, Canada

    Ovidiu Lungu

  5. Functional Neuroimaging Unit, Research Center of the Geriatric Institute affiliated with the Université de Montréal, Montréal, Québec, Canada

    Ovidiu Lungu

  6. Department of Neurology, School of Medicine, University of Minnesota, Minneapolis, MN, USA

    Martin Bareš

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  1. Pavel Filip
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  2. Cécile Gallea
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Correspondence to Pavel Filip.

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The study was approved by the Institutional Review Board of the University Hospital of St. Anne (Brno, Czech Republic) and by the Institutional Review Board of the University of Minnesota (Minneapolis, USA).

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There are no potential conflicts of interests regarding this paper and no financial or personal relationships that might bias this work.

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Filip, P., Gallea, C., Lehéricy, S. et al. Neural Scaffolding as the Foundation for Stable Performance of Aging Cerebellum. Cerebellum 18, 500–510 (2019). https://doi.org/10.1007/s12311-019-01015-7

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