Dataset Information

Hierarchical motor adaptations negotiate failures during force field learning.

ABSTRACT: Humans have the amazing ability to learn the dynamics of the body and environment to develop motor skills. Traditional motor studies using arm reaching paradigms have viewed this ability as the process of 'internal model adaptation'. However, the behaviors have not been fully explored in the case when reaches fail to attain the intended target. Here we examined human reaching under two force fields types; one that induces failures (i.e., target errors), and the other that does not. Our results show the presence of a distinct failure-driven adaptation process that enables quick task success after failures, and before completion of internal model adaptation, but that can result in persistent changes to the undisturbed trajectory. These behaviors can be explained by considering a hierarchical interaction between internal model adaptation and the failure-driven adaptation of reach direction. Our findings suggest that movement failure is negotiated using hierarchical motor adaptations by humans.

SUBMITTER: Ikegami T

PROVIDER: S-EPMC8084335 | biostudies-literature | 2021 Apr

REPOSITORIES: biostudies-literature

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Hierarchical motor adaptations negotiate failures during force field learning.

Ikegami Tsuyoshi T Ganesh Gowrishankar G Gibo Tricia L TL Yoshioka Toshinori T Osu Rieko R Kawato Mitsuo M

PLoS computational biology 20210419 4

Humans have the amazing ability to learn the dynamics of the body and environment to develop motor skills. Traditional motor studies using arm reaching paradigms have viewed this ability as the process of 'internal model adaptation'. However, the behaviors have not been fully explored in the case when reaches fail to attain the intended target. Here we examined human reaching under two force fields types; one that induces failures (i.e., target errors), and the other that does not. Our results s ...[more]

PMID: 33872304

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Project description:IntroductionAttention-Deficit/Hyperactivity Disorder (ADHD) is a neurodevelopmental disorder that exhibits unique neurological and behavioral characteristics. Those with ADHD often have noted impairments in motor performance and coordination, including during tasks that require force modulation. The present study provides insight into the role of altered neural processing and SMI in response to a motor learning paradigm requiring force modulation and proprioception, that previous literature has suggested to be altered in those with ADHD, which can also inform our understanding of the neurophysiology underlying sensorimotor integration (SMI) in the general population.MethodsAdults with ADHD (n = 15) and neurotypical controls (n = 15) performed a novel force-matching task, where participants used their right-thumb to match a trace template that varied from 2-12% of their Abductor Pollicis Brevis maximum voluntary contraction. This motor task was completed in pre, acquisition, and post blocks. Participants also completed a retention test 24 h later. Median nerve somatosensory-evoked potentials (SEPs) were collected pre and post motor acquisition. SEPs were stimulated at two frequencies, 2.47 Hz and 4.98 Hz, and 1,000 sweeps were recorded using 64-electrode electroencephalography (EEG) at 2,048 Hz. SEP amplitude changes were normalized to each participant's baseline values for that peak.ResultsBoth groups improved at post measures (ADHD: 0.85 ± 0.09; Controls: 0.85 ± 0.10), with improvements maintained at retention (ADHD: 0.82 ± 0.11; Controls: 0.82 ± 0.11). The ADHD group had a decreased N18 post-acquisition (0.87 ± 0.48), while the control N18 increased (1.91 ± 1.43). The N30 increased in both groups, with a small increase in the ADHD group (1.03 ± 0.21) and a more pronounced increase in controls (1.15 ± 0.27).DiscussionUnique neural differences between groups were found after the acquisition of a novel force-matching motor paradigm, particularly relating to the N18 peak. The N18 differences suggest that those with ADHD have reduced olivary-cerebellar-M1 inhibition when learning a novel motor task dependent on force-modulation, potentially due to difficulties integrating the afferent feedback necessary to perform the task. The results of this work provide evidence that young adults with ADHD have altered proprioceptive processing when learning a novel motor task when compared to neurotypical controls.

Dataset Information

Hierarchical motor adaptations negotiate failures during force field learning.

Publications

Hierarchical motor adaptations negotiate failures during force field learning.

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