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Changes in cortical microstructure of the human brain resulting from long-term motor learning

Lehmann, N; Aye, N; Kaufmann, J; Heinze, HJ; Düzel, E; Ziegler, G; Taubert, M; (2023) Changes in cortical microstructure of the human brain resulting from long-term motor learning. Journal of Neuroscience , 43 (50) pp. 8637-8648. 10.1523/JNEUROSCI.0537-23.2023. Green open access

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Abstract

The mechanisms subserving motor skill acquisition and learning in the intact human brain are not fully understood. Previous studies in animals have demonstrated a causal relationship between motor learning and structural rearrangements of synaptic connections, raising the question of whether neurite-specific changes are also observable in humans. Here, we use advanced diffusion magnetic resonance imaging (MRI), sensitive to dendritic and axonal processes, to investigate neuroplasticity in response to long-term motor learning. We recruited healthy male and female human participants (age range 19–29) who learned a challenging dynamic balancing task over four consecutive weeks. Diffusion MRI signals were fitted using NODDI, a theory-driven biophysical model of diffusion, yielding measures of tissue volume, neurite density and the organizational complexity of neurites. While NODDI indices were unchanged and reliable during the control period, neurite orientation dispersion increased significantly during the learning period mainly in primary sensorimotor, prefrontal, premotor, supplementary and cingulate motor areas. Importantly, reorganization of cortical microstructure during the learning phase predicted concurrent behavioral changes, whereas there was no relationship between microstructural changes during the control phase and learning. Changes in neurite complexity were independent of alterations in tissue density, cortical thickness, and intracortical myelin. Our results are in line with the notion that structural modulation of neurites is a key mechanism supporting complex motor learning in humans.

Type: Article
Title: Changes in cortical microstructure of the human brain resulting from long-term motor learning
Location: United States
Open access status: An open access version is available from UCL Discovery
DOI: 10.1523/JNEUROSCI.0537-23.2023
Publisher version: http://dx.doi.org/10.1523/jneurosci.0537-23.2023
Language: English
Additional information: This version is the version of record. For information on re-use, please refer to the publisher’s terms and conditions.
Keywords: MRI, NODDI, brain microstructure, diffusion, motor learning, neuroplasticity, skill acquisition, Animals, Humans, Male, Female, Infant, Brain, Diffusion Magnetic Resonance Imaging, Magnetic Resonance Imaging, Neurites, Learning, White Matter
UCL classification: UCL
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences > Div of Psychology and Lang Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences > Div of Psychology and Lang Sciences > Institute of Cognitive Neuroscience
URI: https://discovery.ucl.ac.uk/id/eprint/10184944
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