Representational neural mapping of dexterous grasping before lifting in humans
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(Published version)
Date
2020
Authors
Marneweck, M.
Grafton, S.T.
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Journal article
Citation
Journal of Neuroscience, 2020; 40(13):2708-2716
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Michelle Marneweck and Scott T. Grafton
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Abstract
The ability of humans to reach and grasp objects in their environment have been the mainstay paradigm for characterizing the neural circuitry driving object-centric actions. While much is known about hand shaping, a persistent question is how the brain orchestrates and integrates the grasp with lift forces of the fingers in a coordinated manner. The objective of the current study was to investigate how the brain represents grasp configuration and lift force during a dexterous object-centric action in a large sample of male and female human subjects. BOLD activity was measured as subjects used a precision-grasp to lift an object with a center of mass (CoM) on the left or right with the goal of minimizing tilting the object. The extent to which grasp configuration and lift force varied between left and right CoM conditions was manipulated grasping the object collinearly (requiring a non-collinear force distribution) or non-collinearly (requiring more symmetrical forces). Bayesian variational representational similarity analyses on fMRI data assessed the evidence that a set of cortical and cerebellar regions were sensitive to grasp configuration or lift force differences between CoM conditions at differing timepoints during a grasp to lift action. In doing so, we reveal strong evidence that grasping and lift force are not represented by spatially separate functionally specialized regions, but by the same regions at differing timepoints. The coordinated grasp to lift effort is shown to be under dorsolateral (PMv and AIP) more than dorsomedial control, and under SPL7, somatosensory PSC, ventral LOC and cerebellar control. Signficance Statement: Clumsy disasters like spilling, dropping, and crushing during our daily interactions with objects are a rarity rather than the norm. These disasters are avoided in part as a result of our orchestrated anticipatory efforts to integrate and coordinate grasping and lifting of object interactions, all before the lift of an object even commences. How the brain orchestrates this integration process has been largely neglected by historical approaches independently and solely focusing on reaching and grasping and the neural principles that guide them. Here we test the extent to which grasping and lifting are represented in a spatially or temporally-distinct manner and identified strong evidence for the consecutive emergence of sensitivity to grasping, then lifting within the same region.
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Corrected by: Erratum: Marneweck and Grafton, “Representational Neural Mapping of Dexterous Grasping Before Lifting in Humans, in 41(2) 390; DOI: https://doi.org/10.1523/JNEUROSCI.2479-20.2020. An important detail was left out of the legend of Figure 2. The online version has been updated to include the following sentence: “All cortical regions (including those on the medial wall) are projected to the lateral surface.”
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