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Functional anatomy of human procedural learning determined with regional cerebral blood flow and PET
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The functional anatomy of motor skill acquisition was investigated in six normal human subjects who learned to perform a pursuit rotor task with their dominant right hand during serial positron emission tomography (PET) imaging of relative cerebral blood flow (relCBF). The effect of motor execution, rather than learning, was identified by a comparison of four motor performance scans with two control scans (eye movements only). Motor execution was associated with activation of a distributed network involving cortical, striatonigral, and cerebellar sites. Second, the effect of early motor learning was examined. Performance improved from 17% to 66% mean time on target across the four PET scans obtained during pursuit rotor performance. Across the same scans, significant longitudinal increases of relCBF were located in the left primary motor cortex, the left supplementary motor area, and the left pulvinar thalamus. The results demonstrate that changes of regional cerebral activity associated with early learning of skilled movements occur in sites that are a subset of a more widely distributed network that is active during motor execution.
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“The putamen is often implicated in procedural learning (Grafton et al., 1992; Miyachi et al., 1997, 2002; Jueptner and Weiller, 1998; Turner et al., 2003).”
From Neural Correlates of Long-Term Memory Enhancement Following Retrieval Practice (2021) · cites this paper as Grafton et al., 1992
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BackgroundResultInfluentialModulation of motor cortical outputs to the reading hand of braille readers
Pascual‐Leone, Á., Cammarota, Á., Wassermann, E. M., Brasil-Neto, J. P., Cohen, L. G., & Hallett, M. (1993) · Annals of Neurology · doi:10.1002/ana.410340108 · Cited by 291
How 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
“The premotor cortex is important in the temporal organization of sequential movements (Halsband et al. 1990, 1993), selection of movements (Deiber et al. 1991), and in the generation of motor sequences from memory that fit into a precise plan (Grafton et al. 1992; Shibasaki et al. 1993).”
BackgroundMartin, R. E., MacIntosh, B. J., Smith, R. C., Barr, A. M., Stevens, T. K., Gati, J. S., & Menon, R. S. (2004) · Journal of Neurophysiology · doi:10.1152/jn.01144.2003 · Cited by 271
Thach, W. T. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081504 · Cited by 276
The Brain That Plays Music and Is Changed by It
Pascual‐Leone, Á. (2001) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2001.tb05741.x · Cited by 279
Commentary and Opinion: II. Statistical Parametric Mapping: Ontology and Current Issues
Friston, K. J. (1995) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.1995.45 · Cited by 268
Functionally Specific Changes in Resting-State Sensorimotor Networks after Motor Learning
Vahdat, S., Darainy, M., Milner, T. E., & Ostry, D. J. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.2737-11.2011 · Cited by 271
“These regions include contralateral primary motor cortex (M1) (Grafton et al., 1992; Steele and Penhune, 2010), dorsal premotor cortex (PMd) (Shadmehr and Holcomb, 1997), supplementary motor area (SMA) (Padoa-Schioppa et al.”
Hund‐Georgiadis, M., & von Cramon, D. Y. (1999) · Experimental Brain Research · doi:10.1007/s002210050698 · Cited by 264
“Previous PET-studies have focused on the nature and the extent of brain reorganization in response to motor learning based on different task types (Seitz et al. 1990; Grafton et al. 1992; Friston et al. 1992; Jenkins et al. 1994; Schlaug et al. 1994).”
BackgroundResultBrain correlates of stuttering and syllable production: A PET performance-correlation analysis
Fox, P. T. (2000) · Brain · doi:10.1093/brain/123.10.1985 · Cited by 268
Hikosaka, O., Sakai, K., Miyauchi, S., Takino, R., Sasaki, Y., & Pütz, B. (1996) · Journal of Neurophysiology · doi:10.1152/jn.1996.76.1.617 · Cited by 262
Neuronal Activity in Medial Frontal Cortex During Learning of Sequential Procedures
Nakamura, K., Sakai, K., & Hikosaka, O. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.80.5.2671 · Cited by 261
“Functional imaging studies on human subjects also suggest that the SMA is a storage site of movement skill (Grafton et al. 1992, 1994, 1995; van Mier and Petersen 1996) or sequence (Jenkins et al. 1994; Seitz and Roland 1992).”
BackgroundDoyon, J., Owen, A. M., Petrides, M., Sziklas, V., & Evans, A. C. (1996) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1996.tb01249.x · Cited by 326
On climbing fiber signals and their consequence(s)
Simpson, J. I., WYLIE, D. R. W., & Zeeuw, C. I. D. (1996) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00081486 · Cited by 252
Serial reaction time learning and Parkinson's disease: Evidence for a procedural learning deficit
Jackson, G. M., Jackson, S. R., Harrison, J., Henderson, L., & Christopher Kennard, C. (1995) · Neuropsychologia · doi:10.1016/0028-3932(95)00010-z · Cited by 249
Changes in brain activation during the acquisition of a new bimanual coordination task
Debaere, F., Wenderoth, N., Sunaert, S. G., Hecke, P. V., & Swinnen, S. P. (2004) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2003.12.010 · Cited by 250
“... al., 1996; Honda et al., 1998; Jenkins, Brooks, Nixon, Frackowiak, & Passingham, 1994; Jueptner, Frith, Brooks, Frackowiak, & Passingham, 1997; Jueptner, Stephan, Frith, Brooks, & Frackowiak, 1997; Karni et al., 1995; Sakai et al., 1998, 1999; Seitz & Roland, 1992; Toni & Passingham, 1999; Toni, Krams, Turner, & P…”
BackgroundA PET investigation of implicit and explicit sequence learning
Rauch, S. L., Savage, C. R., Brown, H. D., Curran, T., Alpert, N. M., Kendrick, A., Fischman, A. J., & Kosslyn, S. M. (1995) · Human Brain Mapping · doi:10.1002/hbm.460030403 · Cited by 241
Cognitive and behavioral heterogeneity in Alzheimer's disease: seeking the neurobiological basis
Cummings, J. L. (2000) · Neurobiology of Aging · doi:10.1016/s0197-4580(00)00183-4 · Cited by 238
“[148] Grafton ST, Mazziotta JC, Presty S, Friston KJ, Frackowiak RSJ, Phelps ME.”
BackgroundNeurocognitive Contributions to Motor Skill Learning: The Role of Working Memory
Seidler, R. D., Bo, J., & Anguera, J. A. (2012) · Journal of Motor Behavior · doi:10.1080/00222895.2012.672348 · Cited by 233
“Early neuroscience experiments of human skill learning focused predominantly on motor cortical plasticity (Grafton et al., 1992; Karni et al., 1995).”
An fMRI study of the human cortical motor system response to increasing functional demands
Wexler, B. E., Fulbright, R. K., Lacadie, C., Skudlarski, P., Kelz, M. B., Constable, R. T., & Gore, J. C. (1997) · Magnetic Resonance Imaging · doi:10.1016/s0730-725x(96)00232-9 · Cited by 232
Zilles, K., Gottfried Schlaug, A., Matelli, M., Luppino, G., Schleicher, A., Qü, M., Dabringhaus, A., Seitz, R. J., & Roland, P. E. (1995) · PubMed · Cited by 232
Gabrieli, J. D. E., Corkin, S., Mickel, S. F., & Growdon, J. H. (1993) · Behavioral Neuroscience · doi:10.1037//0735-7044.107.6.899 · Cited by 234
“A recent positron emission tomography study is relevant because it examined which neural brain regions were activated, as measured by increased relative cerebral blood flow, when normal subjects performed rotary pursuit across a number of trials ( Grafton, Mazziotta, Presty, Friston, Frackowiak, & Phelps, 1992 ).”
BackgroundFrequency-Dependent Changes of Regional Cerebral Blood Flow during Finger Movements
Sadato, N., Ibañez, V., Deiber, M., Campbell, G., Leonardo, M., & Hallett, M. (1996) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-199601000-00003 · Cited by 230
Boecker, H., Dagher, A., Ceballos-Baumann, A., Passingham, R. E., Samuel, M., Friston, K. J., Poline, J.-B., Dettmers, C., Conrad, B., & Brooks, D. J. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.79.2.1070 · Cited by 225
“This difference between suggesting that the basal ganglia do not primarily mediate motor procedural learning (Grafton et al. 1992a; Jenkins etour findings and those of Shibasaki et al. may in part be attributed to variations in the task design (self-paced task, al.”
BackgroundThe neural basis of visual skill learning: an fMRI study of mirror reading
Poldrack, R. (1998) · Cerebral Cortex · doi:10.1093/cercor/8.1.1 · Cited by 224
“Learning-related increases in activity have been observed also in the supplementary motor area (Grafton et al., 1992, 1994, 1995; Hazeltine et al., 1997) and basal ganglia (Seitz et al., 1990; Seitz and Roland, 1992; Grafton et al., 1995; Hazeltine et al., 1997).”
BackgroundEffective connectivity of brain networks during self-initiated movement in Parkinson's disease
Wu, T., Wang, L. Y., Hallett, M., Chen, Y., Li, K., & Chan, P. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.11.074 · Cited by 223
“The parietal cortex plays a role in selecting and monitoring a motor sequence (Deiber et al., 1991; Grafton et al., 1992), and involves the temporal aspects of motor sequence to ensure that each movement occurs after successfully completing the preceding move and in predicting the time required to…”
BackgroundInfluentialReductions in neural activity underlie behavioral components of repetition priming
Wig, G. S., Grafton, S. T., Demos, K. E., & Kelley, W. M. (2005) · Nature Neuroscience · doi:10.1038/nn1515 · Cited by 223
Mier, H. I. V., Tempel, L. W., Perlmutter, J. S., Raichle, M. E., & Petersen, S. E. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.80.4.2177 · Cited by 222
Transcranial magnetic stimulation and neuroplasticity
Pascual‐Leone, Á., Tarazona, F., Keenan, J. P., Tormos, J. M., Hamilton, R. H., & Catalá, M. D. (1998) · Neuropsychologia · doi:10.1016/s0028-3932(98)00095-5 · Cited by 224
Metadata
- Authors
- Grafton, S., Mazziotta, J., Presty, S., Friston, K., Frackowiak, R., & Phelps, M.
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 1992-07-01
- Volume
- 12
- Issue
- 7
- Pages
- 2542-2548
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6575851
- OpenAlex
- W2124365503
- Cited by
- 607
- References
- 34
- Citations by year
- 2025: 3 · 2024: 8 · 2023: 2 · 2022: 7 · 2021: 5 · 2020: 5 · 2019: 7 · 2018: 6 · 2017: 11 · 2016: 7 · 2015: 16 · 2014: 16 · 2013: 10 · 2012: 12
- FWCI
- 16.19
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Funders
- U.S. Department of Energy (FC03-87ER60615)
- National Institutes of Health (5r01mh037916-10)
- National Institute of Mental Health (R01 MH 37916)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neurobiology of Language and Bilingualism
- Health Sciences › Medicine › Clinical Neurology › Deep Brain Stimulation and Movement Disorders
- Keywords
- procedural learning, motor skill learning, pursuit rotor task, relative cerebral blood flow, primary motor cortex, supplementary motor area, cerebellum, motor execution
- MeSH terms
- Adult, Brain, Brain Mapping, Cerebrovascular Circulation, Eye Movements, Female, Humans, Functional Laterality, Learning, Male, Motor Activity, Movement, Organ Specificity, Regional Blood Flow, Tomography, Emission-Computed
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