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The Myelin Content of the Human Precentral Hand Knob Reflects Interindividual Differences in Manual Motor Control at the Physiological and Behavioral Level

The primary motor cortex hand area (M1(HAND)) and adjacent dorsal premotor cortex (PMd) form the so-called motor hand knob in the precentral gyrus. M1(HAND) and PMd are critical for dexterous hand use and are densely interconnected via corticocortical axons, lacking a sharp demarcating border. In 24...

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Autores principales: Dubbioso, Raffaele, Madsen, Kristoffer Hougaard, Thielscher, Axel, Siebner, Hartwig Roman
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8026359/
https://www.ncbi.nlm.nih.gov/pubmed/33653698
http://dx.doi.org/10.1523/JNEUROSCI.0390-20.2021
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author Dubbioso, Raffaele
Madsen, Kristoffer Hougaard
Thielscher, Axel
Siebner, Hartwig Roman
author_facet Dubbioso, Raffaele
Madsen, Kristoffer Hougaard
Thielscher, Axel
Siebner, Hartwig Roman
author_sort Dubbioso, Raffaele
collection PubMed
description The primary motor cortex hand area (M1(HAND)) and adjacent dorsal premotor cortex (PMd) form the so-called motor hand knob in the precentral gyrus. M1(HAND) and PMd are critical for dexterous hand use and are densely interconnected via corticocortical axons, lacking a sharp demarcating border. In 24 young right-handed volunteers, we performed multimodal mapping to delineate the relationship between structure and function in the right motor hand knob. Quantitative structural magnetic resonance imaging (MRI) at 3 tesla yielded regional R1 maps as a proxy of cortical myelin content. Participants also underwent functional MRI (fMRI). We mapped task-related activation and temporal precision, while they performed a visuomotor synchronization task requiring visually cued abduction movements with the left index or little finger. We also performed sulcus-aligned transcranial magnetic stimulation of the motor hand knob to localize the optimal site (hotspot) for evoking a motor evoked potential (MEP) in two intrinsic hand muscles. Individual motor hotspot locations varied along the rostrocaudal axis. The more rostral the motor hotspot location in the precentral crown, the longer were corticomotor MEP latencies. “Hotspot rostrality” was associated with the regional myelin content in the precentral hand knob. Cortical myelin content also correlated positively with task-related activation of the precentral crown and temporal precision during the visuomotor synchronization task. Together, our results suggest a link among cortical myelination, the spatial cortical representation, and temporal precision of finger movements. We hypothesize that the myelination of cortical axons facilitates neuronal integration in PMd and M1(HAND) and, hereby, promotes the precise timing of movements. SIGNIFICANCE STATEMENT Here we used magnetic resonance imaging and transcranial magnetic stimulation of the precentral motor hand knob to test for a link among cortical myelin content, functional corticomotor representations, and manual motor control. A higher myelin content of the precentral motor hand knob was associated with more rostral corticomotor presentations, with stronger task-related activation and a higher precision of movement timing during a visuomotor synchronization task. We propose that a high precentral myelin content enables fast and precise neuronal integration in M1 (primary motor cortex) and dorsal premotor cortex, resulting in higher temporal precision during dexterous hand use. Our results identify the degree of myelination as an important structural feature of the neocortex that is tightly linked to the function and behavior supported by the cortical area.
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spelling pubmed-80263592021-04-08 The Myelin Content of the Human Precentral Hand Knob Reflects Interindividual Differences in Manual Motor Control at the Physiological and Behavioral Level Dubbioso, Raffaele Madsen, Kristoffer Hougaard Thielscher, Axel Siebner, Hartwig Roman J Neurosci Research Articles The primary motor cortex hand area (M1(HAND)) and adjacent dorsal premotor cortex (PMd) form the so-called motor hand knob in the precentral gyrus. M1(HAND) and PMd are critical for dexterous hand use and are densely interconnected via corticocortical axons, lacking a sharp demarcating border. In 24 young right-handed volunteers, we performed multimodal mapping to delineate the relationship between structure and function in the right motor hand knob. Quantitative structural magnetic resonance imaging (MRI) at 3 tesla yielded regional R1 maps as a proxy of cortical myelin content. Participants also underwent functional MRI (fMRI). We mapped task-related activation and temporal precision, while they performed a visuomotor synchronization task requiring visually cued abduction movements with the left index or little finger. We also performed sulcus-aligned transcranial magnetic stimulation of the motor hand knob to localize the optimal site (hotspot) for evoking a motor evoked potential (MEP) in two intrinsic hand muscles. Individual motor hotspot locations varied along the rostrocaudal axis. The more rostral the motor hotspot location in the precentral crown, the longer were corticomotor MEP latencies. “Hotspot rostrality” was associated with the regional myelin content in the precentral hand knob. Cortical myelin content also correlated positively with task-related activation of the precentral crown and temporal precision during the visuomotor synchronization task. Together, our results suggest a link among cortical myelination, the spatial cortical representation, and temporal precision of finger movements. We hypothesize that the myelination of cortical axons facilitates neuronal integration in PMd and M1(HAND) and, hereby, promotes the precise timing of movements. SIGNIFICANCE STATEMENT Here we used magnetic resonance imaging and transcranial magnetic stimulation of the precentral motor hand knob to test for a link among cortical myelin content, functional corticomotor representations, and manual motor control. A higher myelin content of the precentral motor hand knob was associated with more rostral corticomotor presentations, with stronger task-related activation and a higher precision of movement timing during a visuomotor synchronization task. We propose that a high precentral myelin content enables fast and precise neuronal integration in M1 (primary motor cortex) and dorsal premotor cortex, resulting in higher temporal precision during dexterous hand use. Our results identify the degree of myelination as an important structural feature of the neocortex that is tightly linked to the function and behavior supported by the cortical area. Society for Neuroscience 2021-04-07 /pmc/articles/PMC8026359/ /pubmed/33653698 http://dx.doi.org/10.1523/JNEUROSCI.0390-20.2021 Text en Copyright © 2021 Dubbioso et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Articles
Dubbioso, Raffaele
Madsen, Kristoffer Hougaard
Thielscher, Axel
Siebner, Hartwig Roman
The Myelin Content of the Human Precentral Hand Knob Reflects Interindividual Differences in Manual Motor Control at the Physiological and Behavioral Level
title The Myelin Content of the Human Precentral Hand Knob Reflects Interindividual Differences in Manual Motor Control at the Physiological and Behavioral Level
title_full The Myelin Content of the Human Precentral Hand Knob Reflects Interindividual Differences in Manual Motor Control at the Physiological and Behavioral Level
title_fullStr The Myelin Content of the Human Precentral Hand Knob Reflects Interindividual Differences in Manual Motor Control at the Physiological and Behavioral Level
title_full_unstemmed The Myelin Content of the Human Precentral Hand Knob Reflects Interindividual Differences in Manual Motor Control at the Physiological and Behavioral Level
title_short The Myelin Content of the Human Precentral Hand Knob Reflects Interindividual Differences in Manual Motor Control at the Physiological and Behavioral Level
title_sort myelin content of the human precentral hand knob reflects interindividual differences in manual motor control at the physiological and behavioral level
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8026359/
https://www.ncbi.nlm.nih.gov/pubmed/33653698
http://dx.doi.org/10.1523/JNEUROSCI.0390-20.2021
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