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Neural substrates of anticipatory motor adaptation for object lifting.

ABSTRACT: Anticipatory force control is a fundamental means by which humans stave off slipping, spilling, and tilting disasters while manipulating objects. This control must often be adapted due to changes in an object's dynamics (e.g. a lighter than expected mug of coffee) or its relation with involved effectors or digits (e.g. lift a mug with three vs. five digits). The neural processes guiding such anticipatory and adaptive control is understudied but presumably operates along multiple time scales, analogous to what has been identified with adaptation in other motor tasks, such as perturbations during reaching. Learning of anticipatory forces must be ultrafast to minimize tilting a visually symmetric object towards its concealed asymmetric center of mass (CoM), but slower when the CoM is explicitly and systematically switched from side to side. Studying the neural substrates of this latter slower learning process with rapid multiband brain imaging, in-scanner kinematics and Bayesian pattern component modelling, we show that CoM-specific pattern distances increase with repeated CoM switching exposures and improved learning. The cerebellum showed the most prominent effects, fitting with the idea that it forms a stored internal model that is used to build and update anticipatory control. CoM-specific pattern distances were present 24 h later, in line with the presence of consolidation effects.

SUBMITTER: Marneweck M

PROVIDER: S-EPMC7320154 | biostudies-literature | 2020 Jun

REPOSITORIES: biostudies-literature

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Neural substrates of anticipatory motor adaptation for object lifting.

Marneweck Michelle M Grafton Scott T ST

Scientific reports 20200626 1

Anticipatory force control is a fundamental means by which humans stave off slipping, spilling, and tilting disasters while manipulating objects. This control must often be adapted due to changes in an object's dynamics (e.g. a lighter than expected mug of coffee) or its relation with involved effectors or digits (e.g. lift a mug with three vs. five digits). The neural processes guiding such anticipatory and adaptive control is understudied but presumably operates along multiple time scales, ana ...[more]

PMID: 32591584

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Project description:Motor skill learning is critical in post-stroke motor recovery, but little is known about its underlying neural substrates. Recently, using a new visuomotor skill learning paradigm involving a speed/accuracy trade-off in healthy individuals we identified three subpopulations based on their behavioral trajectories: fitters (in whom improvement in speed or accuracy coincided with deterioration in the other parameter), shifters (in whom speed and/or accuracy improved without degradation of the other parameter), and non-learners. We aimed to identify the neural substrates underlying the first stages of motor skill learning in chronic hemiparetic stroke patients and to determine whether specific neural substrates were recruited in shifters versus fitters. During functional magnetic resonance imaging (fMRI), 23 patients learned the visuomotor skill with their paretic upper limb. In the whole-group analysis, correlation between activation and motor skill learning was restricted to the dorsal prefrontal cortex of the damaged hemisphere (DLPFCdamh: r = -0.82) and the dorsal premotor cortex (PMddamh: r = 0.70); the correlations was much lesser (-0.16 < r > 0.25) in the other regions of interest. In a subgroup analysis, significant activation was restricted to bilateral posterior parietal cortices of the fitters and did not correlate with motor skill learning. Conversely, in shifters significant activation occurred in the primary sensorimotor cortexdamh and supplementary motor areadamh and in bilateral PMd where activation changes correlated significantly with motor skill learning (r = 0.91). Finally, resting-state activity acquired before learning showed a higher functional connectivity in the salience network of shifters compared with fitters (qFDR < 0.05). These data suggest a neuroplastic compensatory reorganization of brain activity underlying the first stages of motor skill learning with the paretic upper limb in chronic hemiparetic stroke patients, with a key role of bilateral PMd.

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Neural substrates of anticipatory motor adaptation for object lifting.

Publications

Neural substrates of anticipatory motor adaptation for object lifting.

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