Representational Neural Mapping of Dexterous Grasping Before Lifting in Humans

Marneweck, Michelle; Grafton, Scott T.

doi:10.1523/jneurosci.2791-19.2020

Cited by 10 publications

(13 citation statements)

References 65 publications

(86 reference statements)

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“…Following preprocessing of structural and fMRI data, firstlevel deconvolution-based general linear models (GLMs) captured 800-ms time bins of cortical and subcortical activity for a total of 7.2 s starting 800 ms before lift onset for each pre-and post-switch trial at each of the 7 switching blocks. Given the average 4-6 s delay of the hemodynamic response, this method predominantly tracked activity relating to pre-lift anticipatory behavior, as was done previously 9,10 . GLM-derived beta weights were then subsequently used in a Bayesian implementation of representational similarity analyses, i.e., variational representational similarity analyses (vRSA), 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.…”

Section: Resultsmentioning

confidence: 99%

“…In the absence of salient visual cues, the behavioral paradigm we used requires subjects to use a sensorimotor memory of their previous experiences to enact anticipatory force control. Therefore, these pre-lift CoM-specific patterns are likely a neural corollary for the memory that allows anticipatory force control and consequent success in minimizing object tilting 9,10 .…”

Section: Discussionmentioning

confidence: 99%

“…As before, a conservative uninformed approach was adopted, selecting default hyperprior values from the spm_ reml_sc.m script (− 32, 256) because we had little evidence or prior beliefs as to how error might be represented. Further details of the vRSA implementation, its rationale over more traditional univariate and multivariate fMRI analyses, and why multiple comparisons are not needed can be found in 10 .…”

Section: Discussionmentioning

confidence: 99%

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Neural substrates of anticipatory motor adaptation for object lifting

Marneweck

Grafton

2020

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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. CoMspecific pattern distances were present 24 h later, in line with the presence of consolidation effects. Numerous behavioral and computational studies demonstrate that a wide variety of motor behaviors can be adapted to a constantly fluctuating environment and that this learning occurs on multiple time scales 1. For example, prism adaptation, force field adaptation and visuomotor rotation all can be described by a combination of fast and slow learning components. The same general idea of multiple time scales is likely to be operating when people manipulate objects. In this case, when an object's dynamics are mismatched with expectations, the lift forces of the digits adapt extremely rapidly to minimize roll or other aspects of movement error 2. For example, it takes only three trials to successfully lift a visually symmetrical inverted T-shaped object without tilting it towards its concealed asymmetric center of mass (CoM). This is accomplished by an anticipatory partitioning of digit lift forces at lift onset (i.e. more force by the digit closest to the CoM), which generates an appropriate torque counteracting the offset CoM 3. This improvement over just a few trials can be described as an ultrafast form of adaptation 4,5. When the object CoM is then switched from one side to the other (which alters the relation between the involved digits and the object), the movement errors re-emerge, suggesting that ultrafast adaptation is not immediately generalizable to different CoM offsets and appropriate lift forces must be re-acquired 6,7. Critically, this failure to generalize to a new CoM occurs despite a subject's explicit perceptual awareness of the switch (seeing the object being rotated) and an intact knowledge of the CoM (correctly point...

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Neural substrates of anticipatory motor adaptation for object lifting

Marneweck

Grafton

2020

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“…2018 ; Klein et al. 2019 ; Marneweck and Grafton 2020a , 2020b ). Thus, the ventral stream is involved in a hand-object interaction alongside frontoparietal regions in dorsolateral and dorsomedial streams that are more classically defined as subserving the reach and the grasp of a hand-object interaction, at least when objects have covert object properties.…”

Section: Introductionmentioning

confidence: 99%

“…Previously we established that there are differences of multivoxel patterns of activity in the above brain regions that emerge just prior to the successful lifting of T-shaped objects when we contrasted pattern distances for asymmetric left and right CoMs ( Marneweck et al. 2018 ; Marneweck and Grafton 2020a , 2020b ). Critically, the object’s visual shape did not allude to the covert CoM.…”

Section: Introductionmentioning

confidence: 99%

Overt and Covert Object Features Mediate Timing of Patterned Brain Activity during Motor Planning

Marneweck

Grafton

2020

Cerebral Cortex Communications

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Humans are seamless in their ability to efficiently and reliably generate fingertip forces to gracefully interact with objects. Such interactions rarely end in awkward outcomes like spilling, crushing or tilting given advanced motor planning. Here we combine multiband imaging with deconvolution- and Bayesian pattern component modelling of fMRI data and in-scanner kinematics, revealing compelling evidence that the human brain differentially represent preparatory information for skillful object interactions depending on the saliency of visual cues. Earlier patterned activity was particularly evident in ventral visual processing stream-, but also selectively in dorsal visual processing stream and cerebellum in conditions of heightened uncertainty when an object’s superficial shape was incompatible rather than compatible with a key underlying object feature.

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