Abstract

Age-related differences in bimanual motor performance have been extensively documented, but their underlying neural mechanisms remain less clear. Studies applying diffusion MRI in the aging population have revealed evidence for age-related white matter variations in the corpus callosum (CC) which are related to bimanual motor performance. However, the diffusion tensor model used in those studies is confounded by partial volume effects in voxels with complex fiber geometries which are present in up to 90% of white matter voxels, including the bilateral projections of the CC. A recently developed whole-brain analysis framework, known as fixel-based analysis (FBA), enables comprehensive statistical analyses of white matter quantitative measures in the presence of such complex fiber geometries. To investigate the contribution of age-related fiber-specific white matter variations to age-related differences in bimanual performance, a cross-sectional lifespan sample of healthy human adults (N ​= ​95; 20–75 years of age) performed a bimanual tracking task. Furthermore, diffusion MRI data were acquired and the FBA metrics associated with fiber density, cross-section, and combined fiber density and cross-section were estimated. Whole-brain FBA revealed significant negative associations between age and fiber density, cross-section, and combined metrics of multiple white matter tracts, including the bilateral projections of the CC, indicative of white matter micro- and macrostructural degradation with age. More importantly, mediation analyses demonstrated that age-related variations in the combined (fiber density and cross-section) metric of the genu, but not splenium, of the CC contributed to the observed age-related differences in bimanual coordination performance. These findings highlight the contribution of variations in interhemispheric communication between prefrontal (non-motor) cortices to age-related differences in motor performance.

Highlights

  • Bimanual coordination, which is the ability to move the two hands in an organized manner in space and time, is required for many fine and gross motor activities of daily living, such as driving a car, typing an email, and tying shoelaces

  • The overarching objective of this study was to examine whether agerelated variations in the white matter macro- and microstructural properties account for age-related differences in bimanual performance

  • Our results indicated that whereas motor task performance showed no significant correlations with fiber density and cross-section (FDC) of the white matter tract connecting the bilateral motor cortices, it was significantly associated with the FDC of the more anterior and posterior corpus callosum (CC) tracts

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Summary

Introduction

Bimanual coordination, which is the ability to move the two hands in an organized manner in space and time, is required for many fine and gross motor activities of daily living, such as driving a car, typing an email, and tying shoelaces (for reviews, see Maes et al, 2017; Swinnen, 2002; Swinnen and Wenderoth, 2004). Previous behavioral research has identified age-related declines in bimanual coordination performance, especially when the task at hand becomes more complex (for reviews, see Krehbiel et al, 2017; Maes et al, 2017). Such behavioral declines have adverse consequences in the context of functional independence and quality of life in aging. Besides musculoskeletal changes (Faulkner et al, 2007; Hairi et al, 2010), other important factors may underlie these age-related declines in bimanual performance, including alterations in the brain white matter (for a review, see Seidler et al, 2010). Similar to the clinical cases, these degenerative alterations in the properties of transcallosal white matter pathways may contribute to the bimanual performance deficits observed in aging

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