Cited by 634Motor Control and AdaptationDeep Brain Stimulation and Movement DisordersMemory and Neural Mechanisms

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Distinct basal ganglia territories are engaged in early and advanced motor sequence learning

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Lehéricy, Stéphane, Benali, Habib, Van de Moortele, Pierre-François, Pélégrini-Issac, Mélanie, Waechter, Tobias, Ugurbil, Kamil, Doyon, Julien·2005·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.0502762102PMC PMC1194910

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Abstract

In this study, we used functional MRI (fMRI) at high field (3T) to track the time course of activation in the entire basal ganglia circuitry, as well as other motor-related structures, during the explicit learning of a sequence of finger movements over a month of training. Fourteen right-handed healthy volunteers had to practice 15 min daily a sequence of eight moves using the left hand. MRI sessions were performed on days 1, 14 and 28. In both putamen, activation decreased with practice in rostrodorsal (associative) regions. In contrast, there was a significant signal increase in more caudoventral (sensorimotor) regions of the putamen. Subsequent correlation analyses between signal variations and behavioral variables showed that the error rate (movement accuracy) was positively correlated with signal changes in areas activated during early learning, whereas reaction time (movement speed) was negatively correlated with signal changes in areas activated during advanced learning stages, including the sensorimotor putamen and globus pallidus. These results suggest the possibility that motor representations shift from the associative to the sensorimotor territories of the striato-pallidal complex during the explicit learning of motor sequences, suggesting that motor skills are stored in the sensorimotor territory of the basal ganglia that supports a speedy performance.

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Reviewer #1 (Public Review): Acquisition of auditory discrimination mediated by different processes through two distinct circuits linked to the lateral striatum
(2024) · eLife · doi:10.7554/elife.97326.1.sa1
eLife Assessment: Acquisition of auditory discrimination mediated by different processes through two distinct circuits linked to the lateral striatum
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Reviewer #2 (Public Review): Acquisition of auditory discrimination mediated by different processes through two distinct circuits linked to the lateral striatum
(2024) · eLife · doi:10.7554/elife.97326.1.sa0
Acquisition of auditory discrimination mediated by different processes through two distinct circuits linked to the lateral striatumPreprint
Setogawa, S., Okauchi, T., Hu, D., Wada, Y., Hikishima, K., Onoe, H., Nishizawa, K., Sakayori, N., Miyawaki, H., Kitanishi, T., et al. (2024) · eLife · doi:10.7554/elife.97326
Acquisition of auditory discrimination mediated by different processes through two distinct circuits linked to the lateral striatumPreprint
Setogawa, S., Okauchi, T., Hu, D., Wada, Y., Hikishima, K., Onoe, H., Nishizawa, K., Sakayori, N., Miyawaki, H., Kitanishi, T., et al. (2024) · eLife · doi:10.7554/elife.97326.1
Evidence for a sustained cerebrovascular response following motor practice
Patitucci, E., Censo, D. D., Chiarelli, A. M., Germuska, M. A., Tomassini, V., & Wise, R. G. (2024) · Imaging Neuroscience · doi:10.1162/imag_a_00282
Gradual consolidation of skilled sequential movements in primary motor cortex of non-human primatesPreprint
Ohbayashi, M., & Picard, N. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.10.06.616850

Authors: Lehéricy, S., Benali, H., Van de Moortele, P.-F., Pélégrini-Issac, M., Waechter, T., Ugurbil, K., & Doyon, J.
Affiliations: University of Minnesota (US)
Center for Magnetic Resonance Research/Department of Radiology, University of Minnesota, Minneapolis, MN 55455; Unité Mixte de Recherche-S 678, Institut National de la Santé et de la Recherche Médicale/University of Paris 6, Centre Hospitalier Universitaire Pitié-Salpêtrière, 75013 Paris, France; Brain Sciences Center, Veterans Affairs Medical Center, Minneapolis, MN 55417; and Department of Psychology, Functional Neuroimaging Unit, University of Montreal, Montreal, QC, Canada H3W 1W5
ORCID: Lehéricy, Stéphane
Benali, Habib
Doyon, Julien
Venue: Proceedings of the National Academy of Sciences
Publisher: National Academy of Sciences
Published: 2005-08-17
Volume: 102
Issue: 35
Pages: 12566-12571
ISSN: 0027-8424 (ISSN-L)
1091-6490
DOI: 10.1073/pnas.0502762102
PMC: PMC1194910
OpenAlex: W2017072258
Semantic Scholar: 76106906d8471ccfbde0bf91d6be8f4aade5ffb6
Cited by: 634
References: 49
Citations by year: 2026: 15 · 2025: 21 · 2024: 32 · 2023: 32 · 2022: 25 · 2021: 29 · 2020: 76 · 2019: 27 · 2018: 28 · 2017: 36 · 2016: 32 · 2015: 40 · 2014: 37 · 2013: 42 · 2012: 35
FWCI: 6.84
Type: journal article
Language: en
Open access: green
europepmc.org
Locations: Proceedings of the National Academy of Sciences (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute of Biomedical Imaging and Bioengineering (R01EB000331)
National Center for Research Resources (P41RR008079)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
Health Sciences › Medicine › Clinical Neurology › Deep Brain Stimulation and Movement Disorders
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords: basal ganglia, motor sequence learning, putamen, globus pallidus, finger movement, motor skill learning, practice effects, movement accuracy, reaction time, motor representations
MeSH terms: Adult, Basal Ganglia, Cerebellum, Female, Fingers, Humans, Learning, Magnetic Resonance Imaging, Male, Motor Cortex, Movement

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Distinct basal ganglia territories are engaged in early and advanced motor sequence learning

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