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Distinct basal ganglia territories are engaged in early and advanced motor sequence learning
Open accessAbstract
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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“Several fMRI experiments subsequently reported a similar finding – that is, that activation in the associative striatum decreases with training [15–17].”
From Cortical and basal ganglia contributions to habit learning and automaticity (2010) · cites this paper as [15]
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“Several studies have reported that the associative striatum is active during initial skill acquisition and that its activity decreases with extended training.”
From Cortical and basal ganglia contributions to habit learning and automaticity (2010) · cites this paper as [15]
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“On the other hand, there is evidence that the response of the sensorimotor striatum to extended training may depend on the type of task that is used.”
From Cortical and basal ganglia contributions to habit learning and automaticity (2010) · cites this paper as [15]
In the citing paper
“In tasks that require subjects to learn a sequence of motor responses (e.g., button presses), a variety of fMRI studies have reported that sensorimotor striatal activation increases with extended training [15–17].”
From Cortical and basal ganglia contributions to habit learning and automaticity (2010) · cites this paper as [15]
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Cites
Parallel organization of functionally segregated circuits linking basal ganglia and cortex
Alexander, G. E., DeLong, M. R., & Strick, P. L. (1986) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.09.030186.002041 · Cited by 8,527
THE BASAL GANGLIA: FOCUSED SELECTION AND INHIBITION OF COMPETING MOTOR PROGRAMS
Mink, J. W. (1996) · Progress in Neurobiology · doi:10.1016/s0301-0082(96)00042-1 · Cited by 2,478
Basal ganglia and cerebellar loops: motor and cognitive circuits
Middleton, F. (2000) · Brain Research Reviews · doi:10.1016/s0165-0173(99)00040-5 · Cited by 1,940
Functional MRI evidence for adult motor cortex plasticity during motor skill learning
Kami, A., Meyer, G., Jezzard, P., Adams, M. M., Turner, R., & Ungerleider, L. G. (1995) · Nature · doi:10.1038/377155a0 · Cited by 1,883
Karni, A., Meyer, G., Rey-Hipolito, C., Jezzard, P., Adams, M. M., Turner, R., & Ungerleider, L. G. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.3.861 · Cited by 1,410
Relative reward preference in primate orbitofrontal cortex
Tremblay, L., & Schultz, W. (1999) · Nature · doi:10.1038/19525 · Cited by 1,314
Multiple reward signals in the brain
Schultz, W. (2000) · Nature Reviews Neuroscience · doi:10.1038/35044563 · Cited by 1,303
Motor sequence learning: a study with positron emission tomography
Jenkins, I., Brooks, D. J., Nixon, P., Frackowiak, R. S. J., & Passingham, R. E. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-06-03775.1994 · Cited by 1,201
Cocker, L. J. L. D., van Veluw, S. J., Fowkes, M. E., Luijten, P. R., Mali, W. P. T. M., & Hendrikse, J. (2013) · Cerebrovascular Diseases · doi:10.1159/000353668 · Cited by 1,163
Dopamine neurons report an error in the temporal prediction of reward during learning
Hollerman, J. R., & Schultz, W. (1998) · Nature Neuroscience · doi:10.1038/1124 · Cited by 1,161
Central mechanisms of motor skill learning
Hikosaka, O., Nakamura, K., Sakai, K., & Nakahara, H. (2002) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(02)00307-0 · Cited by 1,023
Neural Correlates of Motor Memory Consolidation
Shadmehr, R., & Holcomb, H. H. (1997) · Science · doi:10.1126/science.277.5327.821 · Cited by 1,022
Human cerebellar activity reflecting an acquired internal model of a new tool
Imamizu, H., Miyauchi, S., Tamada, T., Sasaki, Y., Takino, R., Pütz, B., Yoshioka, T., & Kawato, M. (2000) · Nature · doi:10.1038/35003194 · Cited by 1,000
Complementary roles of basal ganglia and cerebellum in learning and motor control
Doya, K. (2000) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00153-7 · Cited by 964
Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning
Doyon, J., Penhune, V. B., & Ungerleider, L. G. (2002) · Neuropsychologia · doi:10.1016/s0028-3932(02)00158-6 · Cited by 885
Self-citationBuilding neural representations of habits.
Jog, M. S., Kubota, Y., Connolly, C. I., Hillegaart, V., & Graybiel, A. M. (1999) · Science · doi:10.1126/science.286.5445.1745 · Cited by 834
Independent learning of internal models for kinematic and dynamic control of reaching
Krakauer, J. W., Ghilardi, M. F., & Ghez, C. P. (1999) · Nature Neuroscience · doi:10.1038/14826 · Cited by 797
Three-Dimensional MRI Atlas of the Human Cerebellum in Proportional Stereotaxic Space
Schmahmann, J. D., Doyon, J., McDonald, D., Holmes, C. J., Lavoie, K., Hurwitz, A. S., Kabani, N. J., Toga, A. W., Evans, A. C., & Petrides, M. (1999) · NeuroImage · doi:10.1006/nimg.1999.0459 · Cited by 782
Self-citationAnatomy of motor learning. I. Frontal cortex and attention to action
Jueptner, M., Stephan, K. M., Frith, C. D., Brooks, D. J., Frackowiak, R. S. J., & Passingham, R. E. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.77.3.1313 · Cited by 624
Functional anatomy of human procedural learning determined with regional cerebral blood flow and PET
Grafton, S., Mazziotta, J., Presty, S., Friston, K., Frackowiak, R., & Phelps, M. (1992) · The Journal of Neuroscience · doi:10.1523/jneurosci.12-07-02542.1992 · Cited by 607
Excitatory Cortical Inputs to Pallidal Neurons Via the Subthalamic Nucleus in the Monkey
Nambu, A., Tokuno, H., Hamada, I., Kita, H., Imanishi, M., Akazawa, T., Ikeuchi, Y., & Hasegawa, N. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.84.1.289 · Cited by 604
Building action repertoires: memory and learning functions of the basal ganglia
Graybiel, A. M. (1995) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(95)80100-6 · Cited by 572
Primate globus pallidus and subthalamic nucleus: functional organization
DeLong, M. R., Crutcher, M. D., & Georgopoulos, A. P. (1985) · Journal of Neurophysiology · doi:10.1152/jn.1985.53.2.530 · Cited by 556
Experience-dependent changes in cerebellar contributions to motor sequence learning
Doyon, J., Song, A. W., Karni, A., Lalonde, F. M., Adams, M. M., & Ungerleider, L. G. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.022615199 · Cited by 478
Self-citationAnatomy of Motor Learning. II. Subcortical Structures and Learning by Trial and Error
Jueptner, M., Frith, C., Brooks, D. J., Frackowiak, R. S. J., & Passingham, R. E. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.77.3.1325 · Cited by 466
Attention and stimulus characteristics determine the locus of motor-sequence encoding. A PET study
Hazeltine, E. (1997) · Brain · doi:10.1093/brain/120.1.123 · Cited by 459
Sequential Organization of Multiple Movements: Involvement of Cortical Motor Areas
Tanji, J. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.631 · Cited by 437
Aosaki, T., Graybiel, A. M., & Kimura, M. (1994) · Science · doi:10.1126/science.8023166 · Cited by 427
Speculations on the Functional Anatomy of Basal Ganglia Disorders
Penney, J. B., & Young, A. B. (1983) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.06.030183.000445 · Cited by 418
The Time Course of Changes during Motor Sequence Learning: A Whole-Brain fMRI Study
Toni, I., Krams, M., Turner, R., & Passingham, R. E. (1998) · NeuroImage · doi:10.1006/nimg.1998.0349 · Cited by 411
Differential roles of monkey striatum in learning of sequential hand movement
Miyachi, S., Hikosaka, O., Miyashita, K., Kárádi, Z., & Rand, M. K. (1997) · Experimental Brain Research · doi:10.1007/pl00005669 · Cited by 374
Changing Brain Networks for Visuomotor Control With Increased Movement Automaticity
Floyer-Lea, A., & Matthews, P. M. (2004) · Journal of Neurophysiology · doi:10.1152/jn.01092.2003 · Cited by 349
Mapping the network for planning: a correlational PET activation study with the Tower of London task
Dagher, A., Owen, A. M., Boecker, H., & Brooks, D. J. (1999) · Brain · doi:10.1093/brain/122.10.1973 · Cited by 345
Lehéricy, S. (2004) · Cerebral Cortex · doi:10.1093/cercor/bhh091 · Cited by 311
Self-citationHow self-initiated memorized movements become automatic: A functional MRI study
Wu, T., Kansaku, K., & Hallett, M. (2004) · Journal of Neurophysiology · doi:10.1152/jn.01052.2003 · Cited by 286
Functional anatomical correlates of controlled and automatic processing
Jansma, J. M., Ramsey, N. F., Slagter, H. A., & Kahn, R. S. (2001) · Journal of Cognitive Neuroscience · doi:10.1162/08989290152541403 · Cited by 281
Miyachi, S., Hikosaka, O., & Lu, X. (2002) · Experimental Brain Research · doi:10.1007/s00221-002-1213-7 · Cited by 262
Inase, M., Tokuno, H., Nambu, A., Akazawa, T., & Takada, M. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01531-0 · Cited by 227
Grafton, S. T., Woods, R. P., & Tyszka, M. (1994) · Human Brain Mapping · doi:10.1002/hbm.460010307 · Cited by 214
Frontal and Parietal Networks for Conditional Motor Learning: A Positron Emission Tomography Study
Deiber, M., Wise, S. P., Honda, M., Catalan, M.-J., Grafman, J. H., & Hallett, M. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.78.2.977 · Cited by 212
Learning arbitrary visuomotor associations: temporal dynamic of brain activity
Toni, I., Ramnani, N., Josephs, O., Ashburner, J., & Passingham, R. E. (2001) · NeuroImage · doi:10.1006/nimg.2001.0894 · Cited by 210
Presupplementary Motor Area Activation during Sequence Learning Reflects Visuo-Motor Association
Sakai, K., Hikosaka, O., Miyauchi, S., Sasaki, Y., Fujimaki, N., & Pütz, B. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-10-j0002.1999 · Cited by 170
Flament, D., Ellermann, J. M., Kim, S.-G., Uǧurbil, K., & Ebner, T. J. (1996) · Human Brain Mapping · doi:10.1002/hbm.460040302 · Cited by 140
Long-term adaptation to dynamics of reaching movements: a PET study
Nezafat, R., Shadmehr, R., & Holcomb, H. H. (2001) · Experimental Brain Research · doi:10.1007/s002210100787 · Cited by 140
THE ROLE OF THE SUBTHALAMIC NUCLEUS IN EXPERIMENTAL CHOREA
Mitchell, I., Jackson, A., Sambrook, M. A., & Crossman, A. R. (1989) · Brain · doi:10.1093/brain/112.6.1533 · Cited by 128
Effects of Local Inactivation of Monkey Medial Frontal Cortex in Learning of Sequential Procedures
Nakamura, K., Sakai, K., & Hikosaka, O. (1999) · Journal of Neurophysiology · doi:10.1152/jn.1999.82.2.1063 · Cited by 106
Long-term retention of motor skill in macaque monkeys and humans
Hikosaka, O., Rand, M., Nakamura, K., Miyachi, S., Kitaguchi, K., Sakai, K., Lü, X., & Shimo, Y. (2002) · Experimental Brain Research · doi:10.1007/s00221-002-1258-7 · Cited by 84
Glutamate‐Mediated Plasticity in Corticostriatal Networks
Kelley, A. E., Andrzejewski, M. E., Baldwin, A. E., Hernandez, P. J., & Pratt, W. E. (2003) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1300.061 · Cited by 77
Characteristics of a long-term procedural skill in the monkey
Rand, M. K., Hikosaka, O., Miyachi, S., Lu, X., & Miyashita, K. (1998) · Experimental Brain Research · doi:10.1007/s002210050284 · Cited by 72
Research works printed but not linked: 1
- Rand, M. K., Hikosaka, O., Miyachi, S., Lu, X. & Miyashita, K. (1998) Exp. Brain Res. 118, 293-297.9497137
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Haber, S. N., & Knutson, B. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.129 · Cited by 3,718
Balleine, B. W., & O'Doherty, J. P. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.131 · Cited by 1,775
Wood, W., & Rünger, D. (2016) · Annual Review of Psychology · doi:10.1146/annurev-psych-122414-033417 · Cited by 1,445
Neuroplasticity Subserving Motor Skill Learning
Dayan, E., & Cohen, L. G. (2011) · Neuron · doi:10.1016/j.neuron.2011.10.008 · Cited by 1,408
Goal-directed and habitual control in the basal ganglia: implications for Parkinson's disease
Redgrave, P., Rodriguez, M., Smith, Y., Rodriguez-Oroz, M. C., Lehericy, S., Bergman, H., Agid, Y., DeLong, M. R., & Obeso, J. A. (2010) · Nature reviews. Neuroscience · doi:10.1038/nrn2915 · Cited by 1,134
“During prolonged training on motor tasks (when performance would be expected to shift from being under goal-directed to being under habitual control), the activation pattern gradually shifts from rostromedial (associative) to caudolateral (sensorimotor) regions of the striatu”
Self-citation
Metadata
- 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
- 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
- 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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