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Sensorimotor integration and motor learning during a novel force-matching task in young adults with attention-deficit/hyperactivity disorder

INTRODUCTION: Attention-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. T...

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Autores principales: McCracken, Heather S., Murphy, Bernadette A., Ambalavanar, Ushani, Glazebrook, Cheryl M., Yielder, Paul C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9849696/
https://www.ncbi.nlm.nih.gov/pubmed/36684834
http://dx.doi.org/10.3389/fnhum.2022.1078925
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author McCracken, Heather S.
Murphy, Bernadette A.
Ambalavanar, Ushani
Glazebrook, Cheryl M.
Yielder, Paul C.
author_facet McCracken, Heather S.
Murphy, Bernadette A.
Ambalavanar, Ushani
Glazebrook, Cheryl M.
Yielder, Paul C.
author_sort McCracken, Heather S.
collection PubMed
description INTRODUCTION: Attention-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. METHODS: Adults 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. RESULTS: Both 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). DISCUSSION: Unique 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.
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spelling pubmed-98496962023-01-20 Sensorimotor integration and motor learning during a novel force-matching task in young adults with attention-deficit/hyperactivity disorder McCracken, Heather S. Murphy, Bernadette A. Ambalavanar, Ushani Glazebrook, Cheryl M. Yielder, Paul C. Front Hum Neurosci Human Neuroscience INTRODUCTION: Attention-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. METHODS: Adults 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. RESULTS: Both 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). DISCUSSION: Unique 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. Frontiers Media S.A. 2023-01-05 /pmc/articles/PMC9849696/ /pubmed/36684834 http://dx.doi.org/10.3389/fnhum.2022.1078925 Text en Copyright © 2023 McCracken, Murphy, Ambalavanar, Glazebrook and Yielder. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Human Neuroscience
McCracken, Heather S.
Murphy, Bernadette A.
Ambalavanar, Ushani
Glazebrook, Cheryl M.
Yielder, Paul C.
Sensorimotor integration and motor learning during a novel force-matching task in young adults with attention-deficit/hyperactivity disorder
title Sensorimotor integration and motor learning during a novel force-matching task in young adults with attention-deficit/hyperactivity disorder
title_full Sensorimotor integration and motor learning during a novel force-matching task in young adults with attention-deficit/hyperactivity disorder
title_fullStr Sensorimotor integration and motor learning during a novel force-matching task in young adults with attention-deficit/hyperactivity disorder
title_full_unstemmed Sensorimotor integration and motor learning during a novel force-matching task in young adults with attention-deficit/hyperactivity disorder
title_short Sensorimotor integration and motor learning during a novel force-matching task in young adults with attention-deficit/hyperactivity disorder
title_sort sensorimotor integration and motor learning during a novel force-matching task in young adults with attention-deficit/hyperactivity disorder
topic Human Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9849696/
https://www.ncbi.nlm.nih.gov/pubmed/36684834
http://dx.doi.org/10.3389/fnhum.2022.1078925
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