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Interindividual differences in gray and white matter properties are associated with early complex motor skill acquisition.

ABSTRACT: Brain circuits mediate but also constrain experience-induced plasticity and corresponding behavioral changes. Here we tested whether interindividual behavioral differences in learning a challenging new motor skill correlate with variations in brain anatomy. Young, healthy participants were scanned using structural magnetic resonance imaging (T1-weighted MPRAGE, n =?75 and/or diffusion-weighted MRI, n =?59) and practiced a complex whole-body balancing task on a seesaw-like platform. Using conjunction tests based on the nonparametric combination (NPC) methodology, we found that gray matter volume (GMV) in the right orbitrofrontal cortex was positively related to the subjects' initial level of proficiency and their ability to improve performance during practice. Similarly, we obtained a strong trend toward a positive correlation between baseline fractional anisotropy (FA) in commissural prefrontal fiber pathways and later motor learning. FA results were influenced more strongly by radial than axial diffusivity. However, we did not find unique anatomical correlates of initial performance and learning to rate. Our findings reveal structural predispositions for successful motor skill performance and acquisition in frontal brain structures and underlying frontal white matter tracts. Together with previous results, these findings support the view that structural constraints imposed by the brain determine subsequent behavioral success and underline the importance of structural brain network constitution before learning starts.

SUBMITTER: Lehmann N

PROVIDER: S-EPMC6865641 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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Interindividual differences in gray and white matter properties are associated with early complex motor skill acquisition.

Lehmann Nico N Tolentino-Castro J Walter JW Kaminski Elisabeth E Ragert Patrick P Villringer Arno A Taubert Marco M

Human brain mapping 20190701 15

Brain circuits mediate but also constrain experience-induced plasticity and corresponding behavioral changes. Here we tested whether interindividual behavioral differences in learning a challenging new motor skill correlate with variations in brain anatomy. Young, healthy participants were scanned using structural magnetic resonance imaging (T1-weighted MPRAGE, n = 75 and/or diffusion-weighted MRI, n = 59) and practiced a complex whole-body balancing task on a seesaw-like platform. Using conjunc ...[more]

PMID: 31264300

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Project description:OBJECTIVE:To quantify racial differences in brain structural characteristics in white and black octogenarians, and to examine whether these characteristics contribute to cognition. METHODS:Cross-sectional study of 283 adults 79-89 years old (59.4% white;42.0% women) with data on gray matter integrity via diffusion tensor imaging (mean diffusivity), gray matter atrophy (GMA), white matter hyperintensities (WMH), literacy, smoking, drinking, income, hypertension and diabetes. Participants were recruited from an ongoing epidemiological study of older adults living in the community with a range of chronic conditions, physical and cognitive function. Standardized betas (s?) of neuroimaging markers predicting Digit Symbol Substitution Test (DSST) and Modified Mini-Mental State Examination (3MS) scores were computed in multivariable regression models stratified by race. RESULTS:Compared to whites, blacks had lower DSST (p=0.001) and lower 3MS (p=0.006), but also lower mean diffusivity (i.e. higher gray matter microstructural integrity, p=0.032), independent of gender, income, literacy, body mass index, diabetes and drinking habits. Racial differences were not significant for WMH (p=0.062) or GMA (p=0.4). Among blacks, mean diffusivity and WMH were associated with DSST (s?=-.209, p=0.037 and -.211, p=.038, respectively) independent of each other and other covariates; among whites, mean diffusivity, but not WMH, was significantly associated with DSST and 3MS (s? =-.277, p=.002 and -.250, p=0.029, respectively). CONCLUSIONS:In this cohort of octogenarians living in the community, blacks appeared to have higher microstructural integrity of gray matter as compared to whites. This neuroimaging marker was related to higher cognition even in the presence of WMH and other cardiovascular conditions. If confirmed, these findings suggest microstructural gray matter integrity may be a target to improve cognition, especially among blacks who survive to very old age with a range of chronic cardiovascular conditions.

Project description:BackgroundAutism spectrum disorder (ASD) is a complex neurodevelopmental condition. Understanding the brain's microstructure and its relationship to clinical characteristics is important to advance our understanding of the neural supports underlying ASD. In the current work, we implemented Gray-Matter Based Spatial Statistics (GBSS) to examine and characterize cortical microstructure and assess differences between typically developing (TD) and autistic males.MethodsA multi-shell diffusion MRI (dMRI) protocol was acquired from 83 TD and 70 autistic males (5-to-21-years) and fit to the DTI and NODDI models. GBSS was performed for voxelwise analysis of cortical gray matter (GM). General linear models were used to investigate group differences, while age-by-group interactions assessed age-related differences between groups. Within the ASD group, relationships between cortical microstructure and measures of autistic symptoms were investigated.ResultsAll dMRI measures were significantly associated with age across the GM skeleton. Group differences and age-by-group interactions are reported. Group-wise increases in neurite density in autistic individuals were observed across frontal, temporal, and occipital regions of the right hemisphere. Significant age-by-group interactions of neurite density were observed within the middle frontal gyrus, precentral gyrus, and frontal pole. Negative relationships between neurite dispersion and the ADOS-2 Calibrated Severity Scores (CSS) were observed within the ASD group.DiscussionFindings demonstrate group and age-related differences between groups in neurite density in ASD across right-hemisphere brain regions supporting cognitive processes. Results provide evidence of altered neurodevelopmental processes affecting GM microstructure in autistic males with implications for the role of cortical microstructure in the level of autistic symptoms.ConclusionUsing dMRI and GBSS, our findings provide new insights into group and age-related differences of the GM microstructure in autistic males. Defining where and when these cortical GM differences arise will contribute to our understanding of brain-behavior relationships of ASD and may aid in the development and monitoring of targeted and individualized interventions.

Dataset Information

Interindividual differences in gray and white matter properties are associated with early complex motor skill acquisition.

Publications

Interindividual differences in gray and white matter properties are associated with early complex motor skill acquisition.

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