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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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The dynamic network subserving the three phases of cognitive procedural learning
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BackgroundCortical activity related to accuracy of letter recognition
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“…1995; Zanette et al., 1997), ischemic blockade of peripheral nerves (Brasil–Neto et al., 1992, 1993b; Ridding and Rothwell, 1995, 1997; Ziemann et al., 1998b, 1998c, 2001), light deprivation (Boroojerdi et al., 2000, 2001b), and learning (Grafton et al., 1992; Shadmehr and Brashers–Krug, 1997).”
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“Recent findings have shown that motor learning may be mediated by subcortical structures, such as the basal ganglia, which form a closed field not recordable from scalp sites (e.g., Grafton et al., 1992; Jenkins, Brooks, Nixon, Frackowiak, & Passingham, 1994).”
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“Previous imaging studies of procedural motor learning from our laboratory examined the pursuit rotor task (Grafton et al., 1992).”
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“Evidence of cerebellar involvement in procedural learning comes from a number of sources, including patients with focal lesions or atrophy of the cerebellum, functional imaging, and positron emission tomography (Flament, Ellermann, Kim, Ugurbil, & Ebner, 1996; Grafton et al., 1992; Jenkins, Brooks, Nixon, Frackowiak,…”
BackgroundInfluentialPosner, M. I., & Raichle, M. E. (1995) · Behavioral and Brain Sciences · doi:10.1017/s0140525x0003870x · Cited by 49
Lefebvre, S., Dricot, L., Gradkowski, W., Laloux, P., & Vandermeeren, Y. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.04.052 · Cited by 47
Task-Related Interaction between Basal Ganglia and Cortical Dopamine Release
Garraux, G., Peigneux, P., Carson, R. E., & Hallett, M. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.1595-07.2007 · Cited by 47
“This interpretation would be consistent with previous studies demonstrating a prominent role of pre-SMA in the early stages of motor skill learning (Grafton et al., 1992, 1994).”
ResultMaddox, W. T., Aparicio, P. L., Marchant, N. L., & Ivry, R. B. (2005) · Journal of Cognitive Neuroscience · doi:10.1162/0898929053747630 · Cited by 47
Altered Synaptic Plasticity in Tourette's Syndrome and Its Relationship to Motor Skill Learning
Brandt, V. C., Nießen, E., Ganos, C., Kahl, U., Bäumer, T., & Münchau, A. M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0098417 · Cited by 50
“While the execution of the rotary pursuit task engages a wide network of brain regions located in the cortex, the striatum and the cerebellum, motor learning is correlated with increased activity over time in contralateral M1, SMA and pulvinar of the thalamus [32], hence synaptic plasticity in M1 and motor learning in…”
BackgroundPredicting performance from functional imaging data: methods matter
Sidtis, J. J., Strother, S. C., & Rottenberg, D. A. (2003) · NeuroImage · doi:10.1016/s1053-8119(03)00349-5 · Cited by 46
“A number of studies have identified brain areas where activity is correlated with parametric experimental manipulation (e.g., Grafton et al., 1992; Price et al., 1992; Dettmers et al., 1995; Blinkenberg et al., 1996; Sadato et al., 1996; Price et al., 1996).”
BackgroundPaquet, F., Soucy, J., Stip, É., Lévesque, M., Elie, A., & Bédard, M. (2004) · Journal of Neuropsychiatry · doi:10.1176/jnp.16.1.47 · Cited by 46
Cortical Plasticity and Motor Activity Studied with Transcranial Magnetic Stimulation
Tyč, F., & Boyadjian, A. (2006) · Reviews in the Neurosciences · doi:10.1515/revneuro.2006.17.5.469 · Cited by 48
Tracy, J. I., Faro, S., Mohammed, F., Pinus, A. B., Christensen, H. L., & Burkland, D. (2001) · Cognitive Brain Research · doi:10.1016/s0926-6410(00)00045-8 · Cited by 45
Reiss, J. P., Campbell, D. W., Leslie, W. D., Paulus, M. P., Ryner, L. N., Polimeni, J. O., Foot, B. J., & Sareen, J. (2006) · Schizophrenia Research · doi:10.1016/j.schres.2006.04.027 · Cited by 45
“Other motor-associated areas have been correlated with IL including primary motor cortex, premotor cortex, supplementary motor area and the cerebellum (Grafton et al., 1992, 1995; Jueptner et al., 1997).”
BackgroundMotor learning of hands with auditory cue in patients with Parkinson’s disease
Chuma, T., Reza, F., Ikoma, K., & Mano, Y. (2005) · Journal of Neural Transmission · doi:10.1007/s00702-005-0314-4 · Cited by 44
“Imaging studies using positron emission tomography (PET) have provided evidence that the motor cortex is more active during the process of motor learning (Grafton et al., 1992; Kawashima et al., 1994; Honda et al., 1998).”
BackgroundMcGregor, H. E., & Gribble, P. L. (2017) · Journal of Neurophysiology · doi:10.1152/jn.00275.2017 · Cited by 44
Cluster analysis of activity‐time series in motor learning
Balslev, D., Nielsen, F. Å., Frutiger, S. A., Sidtis, J. J., Christiansen, T. B., Svarer, C., Strother, S. C., Rottenberg, D. A., Hansen, L. K., Paulson, O. B., et al. (2002) · Human Brain Mapping · doi:10.1002/hbm.10015 · Cited by 44
“, 1995] or learning effects as described previously for the motor cortex [Grafton et al., 1992; Hazeltine et al., 1997].”
BackgroundActivation of NMDA receptors in brain endothelial cells increases transcellular permeability
Kim, K., Jeon, M. T., Kim, E. S., Lee, C. H., & Kim, D.-G. (2022) · Fluids and Barriers of the CNS · doi:10.1186/s12987-022-00364-6 · Cited by 46
“These phenomena have been documented by positron emission tomography studies using [18F]-fluoro-2-deoxy-d-glucose and by blood oxygen measurements using functional magnetic resonance imaging [8, 9]; thus, providing Open Access Fluids and Barriers of the CNS”
MethodDecrease in cortical activation during learning of a multi-joint discrete motor task
Ikegami, T., & Taga, G. (2008) · Experimental Brain Research · doi:10.1007/s00221-008-1518-2 · Cited by 43
Mapping the Brain’s electric fields with Magnetoelectric nanoparticles
Guduru, R., Liang, P., Yousef, M., Horstmyer, J., & Khizroev, S. (2018) · Bioelectronic Medicine · doi:10.1186/s42234-018-0012-9 · Cited by 43
Anatomical Substrates of Visual and Auditory Miniature Second-language Learning
Newman‐Norlund, R., Frey, S. H., Petitto, L., & Grafton, S. T. (2006) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2006.18.12.1984 · Cited by 43
“…(Hikosaka et al., 2001; Toni, Krams, Turner, & Passigham, 1998; Hikosaka et al., 1996; Kettner, Marcario, & Clark-Phelps, 1996; Sadato, Campbell, Ibanez, Deiber, & Hallett, 1996; Gordon et al., 1995; Grafton, 1995; Grafton et al., 1992; Mushiake, Inase, & Tanji, 1991; Halsband & Freund, 1990).”
The effect of experimental pain on motor training performance and sensorimotor integration
Dancey, E., Murphy, B. A., Srbely, J. Z., & Yielder, P. C. (2014) · Experimental Brain Research · doi:10.1007/s00221-014-3966-1 · Cited by 42
Baeck, J.-S., Kim, Y., Seo, J., Ryeom, H., Lee, J., Choi, S., Woo, M., Kim, W., Kim, J. G., & Chang, Y. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.06.001 · Cited by 48
Plasticity and Reorganization of the Uninjured Brain
Bayona, N. A., Bitensky, J., & Teasell, R. W. (2005) · Topics in Stroke Rehabilitation · doi:10.1310/a422-g91u-q4hb-86xc · Cited by 43
Changes in motor cortex excitability following training of a novel goal-directed motor task
Gallasch, E., Christova, M., Krenn, M. J., Kossev, A. R., & Rafolt, D. (2008) · European Journal of Applied Physiology · doi:10.1007/s00421-008-0871-y · Cited by 42
“In humans, studies with positron emission tomography ( Grafton et al. 1992; Kawashima et al. 1994; Honda et al. 1998), functional magnetic resonance imaging (Karni et al. 1995), and TMS (Pascual-Leone 1995; Classen et al. 1998; Muellbacher et al. 2001) also showed enlarged post-exercise representations in M1 during ac…”
BackgroundKern, R. S., Green, M. F., & Wallace, C. J. (1997) · Cognitive Neuropsychiatry · doi:10.1080/135468097396405 · Cited by 42
The Effect of Switching between Sequential and Repetitive Movements on Cortical Activation
Jäncke, L., Himmelbach, M., Shah, N. J., & Zilles, K. (2000) · NeuroImage · doi:10.1006/nimg.2000.0626 · Cited by 41
“In previous uman motor studies using brain imaging techniques, recuneus activity was found when subjects performed ovements guided by an internal trajectorial map Deiber et al., 1991) or during visually guided finger ovements (Grafton et al., 1992b).”
BackgroundMethodThe dorsomedial frontal cortex: eye and forelimb fields
Tehovnik, E. J. (1995) · Behavioural Brain Research · doi:10.1016/0166-4328(94)00151-5 · Cited by 41
Exploring the effect of inducing long-term potentiation in the human motor cortex on motor learning
Rajji, T. K., Liu, S.-K., Frantseva, M. V., Mulsant, B. H., Thoma, J., Chen, R. E., Fitzgerald, P. B., & Daskalakis, Z. J. (2010) · Brain stimulation · doi:10.1016/j.brs.2010.09.007 · Cited by 40
Brain Activation during the Fist-Edge-Palm Test: A Functional MRI Study
Umetsu, A., Okuda, J., Fujii, T., Tsukiura, T., Nagasaka, T., Yanagawa, I., Sugiura, M., Inoue, K., Kawashima, R., Suzuki, K., et al. (2002) · NeuroImage · doi:10.1006/nimg.2002.1218 · Cited by 40
MARSH, R., Alexander, G. M., Packard, M. G., Hongtu Zhu, B., & PETERSON, B. (2005) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2004.12.012 · Cited by 43
Procedural Learning in Humans ☆
Knowlton, B. J., Siegel, A. L. M., & Moody, T. D. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.21085-7 · Cited by 45
Towards understanding language organisation in the brain using fMRI
Matthews, P. M., Adcock, J., Chen, Y., Fu, S., Devlin, J. T., Rushworth, M. F. S., Smith, S. M., Beckmann, C. F., & Iversen, S. D. (2003) · Human Brain Mapping · doi:10.1002/hbm.10099 · Cited by 41
“An alternative approach is to apply a “parametric” variation and to identify the areas in the brain where activity scales with a psychophysically relevant dimension [Grafton et al., 1992; Price et al., 1992].”
MethodSpecial issue on functional neuroimaging of memory
Cabeza, R. E. L., & Nyberg, L. H. (2002) · Neuropsychologia · doi:10.1016/s0028-3932(02)00156-2 · Cited by 40
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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