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Published online on August 17, 2005, 10.1073/pnas.0502762102
PNAS | August 30, 2005 | vol. 102 | no. 35 | 12566-12571


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

Stéphane Lehéricy *, {dagger}, Habib Benali {ddagger}, Pierre-François Van de Moortele *, Mélanie Pélégrini-Issac {ddagger}, Tobias Waechter §, Kamil Ugurbil *, and Julien Doyon {ddagger}, ¶

*Center for Magnetic Resonance Research/Department of Radiology, University of Minnesota, Minneapolis, MN 55455; {ddagger}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

Edited by Leslie G. Ungerleider, National Institutes of Health, Bethesda, MD, and approved July 11, 2005 (received for review April 4, 2005)

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.

functional MRI | human | subthalamic nucleus


Author contributions: S.L., H.B., K.U., and J.D. designed research; S.L. performed research; S.L., H.B., P.-F.V.d.M., M.P.-I., and T.W. analyzed data; and S.L., H.B., and J.D. wrote the paper.

This paper was submitted directly (Track II) to the PNAS office.

Abbreviations: DN, dentate nucleus; MC, Montreal Neurological Institute coordinate; SMA, supplementary motor area; SN, substantia nigra; STN, subthalamic nucleus; fMRI, functional MRI; EPI, echo-planar imaging; RM-ANOVA, repeated-measure ANOVA; U-sequence, untrained sequence; T-sequence, trained sequence.

Data deposition: The neuroimaging data have been deposited with the fMRI Data Center, www.fmridc.org (accession no. 2-2005-119 KH).

{dagger} To whom correspondence should be addressed at: Center for Magnetic Resonance Research, 2021 6th Street SE, Minneapolis, MN 55455. E-mail: lehericy{at}cmrr.umn.edu.

© 2005 by The National Academy of Sciences of the USA


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