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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:The plasticity of the human nervous system allows us to acquire an open-ended repository of sensorimotor skills in adulthood, such as the mastery of tools, musical instruments or sports. How novel sensorimotor skills are learned from scratch is yet largely unknown. In particular, the so-called inverse mapping from goal states to motor states is underdetermined because a goal can often be achieved by many different movements (motor redundancy). How humans learn to resolve motor redundancy and by which principles they explore high-dimensional motor spaces has hardly been investigated. To study this question, we trained human participants in an unfamiliar and redundant visually-guided manual control task. We qualitatively compare the experimental results with simulation results from a population of artificial agents that learned the same task by Goal Babbling, which is an inverse-model learning approach for robotics. In Goal Babbling, goal-related feedback guides motor exploration and thereby enables robots to learn an inverse model directly from scratch, without having to learn a forward model first. In the human experiment, we tested whether different initial conditions (starting positions of the hand) influence the acquisition of motor synergies, which we identified by Principal Component Analysis in the motor space. The results show that the human participants' solutions are spatially biased towards the different starting positions in motor space and are marked by a gradual co-learning of synergies and task success, similar to the dynamics of motor learning by Goal Babbling. However, there are also differences between human learning and the Goal Babbling simulations, as humans tend to predominantly use Degrees of Freedom that do not have a large effect on the hand position, whereas in Goal Babbling, Degrees of Freedom with a large effect on hand position are used predominantly. We conclude that humans use goal-related feedback to constrain motor exploration and resolve motor redundancy when learning a new sensorimotor mapping, but in a manner that differs from the current implementation of Goal Babbling due to different constraints on motor exploration.

Project description:It is well established that brain structures and cognitive functions change across the life span. A long-standing hypothesis called "age differentiation" additionally posits that the relations between cognitive functions also change with age. To date, however, evidence for age-related differentiation is mixed, and no study has examined differentiation of the relationship between brain and cognition. Here we use multigroup structural equation models (SEMs) and SEM trees to study differences within and between brain and cognition across the adult life span (18-88 years) in a large (N > 646, closely matched across sexes), population-derived sample of healthy human adults from the Cambridge Centre for Ageing and Neuroscience (www.cam-can.org). After factor analyses of gray matter volume (from T1- and T2-weighted MRI) and white matter organization (fractional anisotropy from diffusion-weighted MRI), we found evidence for the differentiation of gray and white matter, such that the covariance between brain factors decreased with age. However, we found no evidence for age differentiation among fluid intelligence, language, and memory, suggesting a relatively stable covariance pattern among cognitive factors. Finally, we observed a specific pattern of age differentiation between brain and cognitive factors, such that a white matter factor, which loaded most strongly on the hippocampal cingulum, became less correlated with memory performance in later life. These patterns are compatible with the reorganization of cognitive functions in the face of neural decline, and/or with the emergence of specific subpopulations in old age.SIGNIFICANCE STATEMENT The theory of age differentiation posits age-related changes in the relationships among cognitive domains, either weakening (differentiation) or strengthening (dedifferentiation), but evidence for this hypothesis is mixed. Using age-varying covariance models in a large cross-sectional adult life span sample, we found age-related reductions in the covariance among both brain measures (neural differentiation), but no covariance change among cognitive factors of fluid intelligence, language, and memory. We also observed evidence of uncoupling (differentiation) between a white matter factor and cognitive factors in older age, most strongly for memory. Together, our findings support age-related differentiation as a complex, multifaceted pattern that differs for brain and cognition, and discuss several mechanisms that might explain the changing relationship between brain and cognition.

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

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

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