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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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“Various other tasks have been used to study the acquisition and control of sequential movement skills, such as the pursuit rotor task (e.g., Grafton et al., 1992), the tracing of cut-out mazes (e.g., Van Mier et al., 1998), the m × n task (Hikosaka et al., 1995), a sequential elbow flexion and…”
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“Examples are studies by Grafton et al. (1992) who demonstrated correlations between rCBF and the performance of a motor tracking task in the supplementary motor area and thalamus.”
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“Whereas motor regions can be particularly important for procedural memories (Grafton et al., 1992), there may be hippocampal contributions to these tasks in some situations (Schendan et al.”
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“…concerned in test–retestdependent changes in this study may be involved in different periods of learning (Doyon et al., 1997; Friston et al., 1991; Grafton et al., 1992; Imamizu et al., 2000; Jenkins et al., 1994; Jueptner et al., 1997; Pascual-Leone et al., 1995; Petersen et al., 1998; Seitz et…”
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Kawashima, R., Roland, P. E., & O'Sullivan, B. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-06-03462.1994 · Cited by 154
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“There is evidence in the limb motor plasticity literature that repetition of a learned motor behavior may indeed be associated with a return to or below baseline values as participants continue to practice the learned behavior, although there are also published data that are not fully in accord with this view (Grafton…”
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“This is corroborated by our ®ndings that rCBF did not change between tasks in the frontal eye ®elds involved in ocular [2] movement, or in the primary and supplementary motor cortex controlling simple ®nger movement [11,13,20,24,25].”
ResultBrain Correlates of Stuttering and Syllable Production
Ingham, R. J., Fox, P. T., Ingham, J. C., Xiong, J., Zamarripa, F., Hardies, L. J., & Lancaster, J. L. (2004) · Journal of Speech Language and Hearing Research · doi:10.1044/1092-4388(2004/026 · Cited by 151
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“…that activity in the brain changes with learning, and that this change correlates with numerous measures of competency including time on task (Grafton et al., 1992, 1994, 2001; van Mier et al., 1998), tracking error (Miall et al., 2001; Diedrichsen et al., 2005; Miall and Jenkinson, 2005),…”
BackgroundInfluentialFrontal regions involved in learning of motor skill—A functional NIRS study
Hatakenaka, M., Miyai, I., Mihara, M., Sakoda, S., & Kubota, K. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.08.014 · Cited by 145
Theoretical and computational analysis of skill learning, repetition priming, and procedural memory.
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“A number of neuroimaging studies have indicated that skill learning is characterized by increases in the intensity or spatial extent of brain activation (e.g., Grafton, Hazeltine, & Ivry, 1995; Grafton et al., 1992; Hazeltine, Grafton, & Ivry, 1997; Karni et al., 1995).”
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“Cerebral Cortex Apr/May 1999, V 9 N 3 271 entations of cortical area 4 (Nudo et al., 1996; also see Grafton et al., 1992; Pascual-Leone et al., 1994; Schlaug et al., 1994; Karni et al., 1995).”
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The Remediation of Problem-Solving Skills in Schizophrenia
Medalia, A. A., Revheim, N., & Casey, M. (2001) · Schizophrenia Bulletin · doi:10.1093/oxfordjournals.schbul.a006872 · Cited by 143
“Initial research has used neuroimaging of normal control subjects to examine changes in cortical activation associated with procedural learning (Grafton et al. 1992) and with WCST training (Berman et al. 1995).”
MethodFunctional connectivity during Stroop task performance
Harrison, B. J., Shaw, M. E., Yücel, M., Purcell, R., Brewer, W. J., Strother, S. C., Egan, G. F., Olver, J. S., Nathan, P. J., & Pantelis, C. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2004.08.033 · Cited by 142
“The cerebellum has been previously implicated in studies of practice effects and automaticity in cognitive performance (Burnod, 1991; Grafton et al., 1992; Seitz et al., 1990) and typically shows decreased activity between unpracticed and practiced trials (e.”
BackgroundBrunner, P., Ritaccio, A. L., Lynch, T. M., Emrich, J. F., Wilson, J. A., Williams, J. C., Aarnoutse, E. J., Ramsey, N. F., Leuthardt, E. C., Bischof, H., et al. (2009) · Epilepsy & Behavior · doi:10.1016/j.yebeh.2009.04.001 · Cited by 141
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“As these areas correspond mainly to hand control (Grafton et al. 1992; Yousry et al. 1997; Indovina and Sanes 2001), we calculated the correlation between”
BackgroundMethodInfluentialMovement Science: Implicit and Explicit Processes during Acquisition of Functional Skills
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“A previous PET study showed that the back side of the bilateral parietal blood flow will increase according with the information complexity [57], and while the subjects were adopting this information, the bilateral parietal blood flow will decline.”
BackgroundImages of the Mind: Studies with Modern Imaging Techniques
Raichle, M. E. (1994) · Annual Review of Psychology · doi:10.1146/annurev.ps.45.020194.002001 · Cited by 134
Modulation of Neural Activity during Observational Learning of Actions and Their Sequential Orders
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“However, previous studies also demonstrate increased pulvinar activity during motor skill acquisition (Grafton et al., 1992) and when reaches must be directed to remembered target locations (Lacquaniti et al., 1997).”
BackgroundRémy, P., Zilbovicius, M., Leroy‐Willig, A., Syrota, A., & Samson, Y. (1994) · Annals of Neurology · doi:10.1002/ana.410360107 · Cited by 131
Explicit and implicit learning of event sequences: Evidence from event-related brain potentials.
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“This view is consistent with recent positron emission tomography data indicating that procedural learning of a motor skill involves modifications in the same brain areas as those that mediate the execution of the skill (Grafton et al., 1992) and that sequence learning is impaired in patients with degenerative changes…”
BackgroundResultInfluentialReview of functional near-infrared spectroscopy in neurorehabilitation
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“The PR task does not require precise control of finger movements, but it requires motor control of proximal parts of the upper extremity including the shoulder and elbow as well as postural control for sitting.(23) In both healthy subjects and those with stroke, the PR task performance improved with repetitions, altho…”
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“That is, practicing sensory or motor tasks is typically associated with increased activation in primary sensory or motor cortex (e.g., Grafton et al., 1992; Karni et al., 1995).”
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Functional MRI of motor sequence acquisition: effects of learning stage and performance
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“The within-session eVects of movement repetition in previous studies do not provide consistent results for the accompanying neural activation, showing either decreases (Karni et al. 1995, 1998) or increases ( Grafton et al. 1992; Iacoboni et al. 1996; Shadmehr and Holcomb 1997).”
ResultMovement-related potentials associated with movement preparation and motor imagery
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“, in press, for review), with activity of the supplementary motor area increasing as novel tasks become well-learnt with practice (Grafton et al. 1992).”
BackgroundThe role of the supplementary motor area in the control of voluntary movement
Cunnington, R., Bradshaw, J. L., & Iansek, R. (1996) · Human Movement Science · doi:10.1016/0167-9457(96)00018-8 · Cited by 121
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“In the last ten years, a substantial number of neuroimaging studies have shown that the brain regions activated during the acquisition of a motor skill vary with practice (Doyon et al. 1996; Friston et al. 1992; Grafton et al. 1992; Inoue et al. 2000; Karni et al. 1995; Krakauer et al. 2004).”
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Human Cortical Networks for New and Familiar Sequences of Saccades
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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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