Neural substrates of anticipatory motor adaptation for object lifting

Michelle Marneweck,Scott T Grafton

doi:10.1038/s41598-020-67453-0

Michelle Marneweck, Scott T Grafton

Open Access

https://doi.org/10.1038/s41598-020-67453-0

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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.

Highlights

general linear models (GLMs)-derived beta weights were subsequently used in a Bayesian implementation of representational similarity analyses, i.e., variational representational similarity analyses, to assess the extent to which multivoxel spatial patterns in prespecified regions of interest (ROIs) were more sensitive to differences between pre- and the first post-switch trials in later than earlier blocks of sensorimotor learning
Using Bayesian variational representational similarity analyses (vRSA) of deconvolution-modelled fMRI data, multivoxel spatial patterns in prespecified ROIs were compared as subjects learned appropriate anticipatory force control to generate a torque away from a systematically, explicitly and repeatedly switching left- and right-sided center of mass (CoM)
In line with our hypotheses, CoM-specific pattern distances increased with repeated CoM switching exposures and improved learning in later than earlier blocks in one training session on day 1

Summary

Introduction

We test whether the ability to switch to the new appropriate pattern improves with repeated exposures If this were true, the pattern distance between the pre- and post-switch activity (reflecting the two CoMs) should increase over blocks of trials with multiple reversals. The pattern distance between the pre- and post-switch activity (reflecting the two CoMs) should increase over blocks of trials with multiple reversals We predicted these differences between earlier and later blocks to be apparent in cerebellum, given its role in storing internal models that are used to build and update predictive control, e.g.11,12. By using a rapid multiband imaging approach, we can test for these effects before lift onset, and examine anticipatory-related activity independent of motor execution and feedback processes We repeat these analyses on a subset of subjects returning 24 h later and test for behavioral retention, a measure of consolidation. Depending on whether learning is consolidated 24 h later, we have the opportunity to test if this is reflected in the corresponding CoM-specific fMRI pattern distances

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