How does long-term training and the development of motor skills modify the activity of the primary motor cortex (M1)? To address this issue, we trained monkeys for ∼1–6 years to perform visually guided and internally generated sequences of reaching movements. Then, we used [14C]2-deoxyglucose (2DG) uptake and single-neuron recording to measure metabolic and neuron activity in M1. After extended practice, we observed a profound reduction of metabolic activity in M1 for the performance of internally generated compared to visually guided tasks. In contrast, measures of neuron firing displayed little difference during the two tasks. These findings suggest that the development of skill through extended practice results in a reduction in the synaptic activity required to produce internally generated, but not visually guided, sequences of movements. Thus, practice leading to skilled performance results in more efficient generation of neuronal activity in M1.
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Adams, J.A. Historical review and appraisal of research on the learning, retention, and transfer of human motor skills. Psychol. Bull. 101, 41–74 (1987).
Proctor, R.W. & Dutta, A. Skill acquisition and human performance (Sage Publications, 1995).
Dayan, E. & Cohen, L.G. Neuroplasticity subserving motor skill learning. Neuron 72, 443–454 (2011).
Amunts, K. et al. Motor cortex and hand motor skills: Structural compliance in the human brain. Hum. Brain Mapp. 5, 206–215 (1997).
Gaser, C. & Schlaug, G. Brain structures differ between musicians and non-musicians. J. Neurosci. 23, 9240–9245 (2003).
Elbert, T., Pantev, C., Wienbruch, C., Rockstroh, B. & Taub, E. Increased cortical representation of the fingers of the left hand in string players. Science 270, 305–307 (1995).
Schwenkreis, P. et al. Assessment of sensorimotor cortical representation asymmetries and motor skills in violin players. Eur. J. Neurosci. 26, 3291–3302 (2007).
Hund-Georgiadis, M. & von Cramon, D.Y. Motor-learning-related changes in piano players and non-musicians revealed by functional magnetic-resonance signals. Exp. Brain Res. 125, 417–425 (1999).
Krings, T. et al. Cortical activation patterns during complex motor tasks in piano players and control subjects. A functional magnetic resonance imaging study. Neurosci. Lett. 278, 189–193 (2000).
Jäncke, L., Shah, N.J. & Peters, M. Cortical activations in primary and secondary motor areas for complex bimanual movements in professional pianists. Brain Res. Cogn. Brain Res. 10, 177–183 (2000).
Haslinger, B. et al. Reduced recruitment of motor association areas during bimanual coordination in concert pianists. Hum. Brain Mapp. 22, 206–215 (2004).
Meister, I. et al. Effects of long-term practice and task complexity in musicians and nonmusicians performing simple and complex motor tasks: implications for cortical motor organization. Hum. Brain Mapp. 25, 345–352 (2005).
Floyer-Lea, A. & Matthews, P.M. Changing brain networks for visuomotor control with increased movement automaticity. J. Neurophysiol. 92, 2405–2412 (2004).
Landau, S.M. & D'Esposito, M. Sequence learning in pianists and nonpianists: An fMRI study of motor expertise. Cogn. Affect. Behav. Neurosci. 6, 246–259 (2006).
Xiong, J. et al. Long-term motor training induced changes in regional cerebral blood flow in both task and resting states. Neuroimage 45, 75–82 (2009).
Li, C.-S., Padoa-Schioppa, C. & Bizzi, E. Neuronal correlates of motor performance and motor learning in the primary motor cortex of monkeys adapting to an external force field. Neuron 30, 593–607 (2001).
Paz, R., Boraud, T., Natan, C., Bergman, H. & Vaadia, E. Preparatory activity in motor cortex reflects learning of local visuomotor skills. Nat. Neurosci. 6, 882–890 (2003).
Ben-Shaul, Y. et al. Neuronal activity in motor cortical areas reflects the sequential context of movement. J. Neurophysiol. 91, 1748–1762 (2004).
Lu, X. & Ashe, J. Anticipatory activity in primary motor cortex codes memorized movement sequences. Neuron 45, 967–973 (2005).
Matsuzaka, Y.M., Picard, N. & Strick, P.L. Skill representation in the primary motor cortex after long-term practice. J. Neurophysiol. 97, 1819–1832 (2007).
Sokoloff, L. et al. The [14C]deoxyglucose method for the measurement of local cerebral glucose utilization: theory, procedure, and normal values in the conscious and anesthetized albino rat. J. Neurochem. 28, 897–916 (1977).
Picard, N. & Strick, P.L. Activation of the supplementary motor area (SMA) during performance of visually guided movements. Cereb. Cortex 13, 977–986 (2003).
Sokoloff, L. Sites and mechanisms of function-related changes in energy metabolism in the nervous system. Dev. Neurosci. 15, 194–206 (1993).
Smith, A.J. et al. Cerebral energetics and spiking frequency: the neurophysiological basis of fMRI. Proc. Natl. Acad. Sci. USA 99, 10765–10770 (2002).
Kim, D.-S. et al. Spatial relationship between neuronal activity and BOLD functional MRI. Neuroimage 21, 876–885 (2004).
Logothetis, N.K. What we can do and what we cannot do with fMRI. Nature 453, 869–878 (2008).
Matsunami, K. & Kawashima, T. Radioactive 2-DG incorporation patterns in the mesial frontal cortex of task-performing monkeys. Neurosci. Res. 23, 365–375 (1995).
Savaki, H.E. & Dalezios, Y. 14C-deoxyglucose mapping of the monkey brain during reaching to visual targets. Prog. Neurobiol. 58, 473–540 (1999).
Gregoriou, G.G., Luppino, G., Matelli, M. & Savaki, H.E. Frontal cortical areas of the monkey brain engaged in reaching behavior: a 14C-deoxyglucose imaging study. Neuroimage 27, 442–464 (2005).
Mushiake, H. & Strick, P.L. Preferential activity of dentate neurons during limb movements guided by vision. J. Neurophysiol. 70, 2660–2664 (1993).
Johnson, P.B., Ferraina, S., Bianchi, L. & Caminiti, R. Cortical networks for visual reaching: Physiological and anatomical organization of frontal and parietal lobe arm regions. Cereb. Cortex 6, 102–119 (1996).
Crammond, D.J. & Kalaska, J.F. Prior information in motor and premotor cortex: Activity during the delay period and effect on pre-movement activity. J. Neurophysiol. 84, 986–1005 (2000).
Hanakawa, T., Dimyan, M.A. & Hallett, M. Motor planning, imagery, and execution in the distributed motor network: a time-course study with functional MRI. Cereb. Cortex 18, 2775–2788 (2008).
Poldrack, R.A. Imaging brain plasticity: conceptual and methodological issues—A theoretical perspective. Neuroimage 12, 1–13 (2000).
Grill-Spector, K., Henson, R. & Martin, A. Repetition and the brain: neural models of stimulus-specific effects. Trends Cogn. Sci. 10, 14–23 (2006).
Hamilton, A.F.C. & Grafton, S.T. Repetition suppression for performed hand gestures revealed by fMRI. Hum. Brain Mapp. 30, 2898–2906 (2009).
Mushiake, H., Inase, M. & Tanji, J. Neuronal activity in primate premotor, supplementary motor and precentral motor cortex during visually guided and internally determined sequential movements. J. Neurophysiol. 66, 705–718 (1991).
Swain, R.A. et al. Prolonged exercise induces angiogenesis and increases cerebral blood volume in primary motor cortex of the rat. Neuroscience 117, 1037–1046 (2003).
Jueptner, M. & Weiller, C. Does measurement of regional cerebral blood flow reflect synaptic activity?—Implications for PET and fMRI. Neuroimage 2, 148–156 (1995).
Magistretti, P.J. Neuron-glia metabolic coupling and plasticity. J. Exp. Biol. 209, 2304–2311 (2006).
Karni, A. et al. Functional evidence for adult motor cortex plasticity during motor skill learning. Nature 377, 155–158 (1995).
Hluštik, P., Solodkin, A., Noll, D.C. & Small, S.L. Cortical plasticity during three-week motor skill learning. J. Clin. Neurophysiol. 21, 180–191 (2004).
Kelly, A.M.C. & Garavan, H. Human functional neuroimaging of brain changes associated with practice. Cereb. Cortex 15, 1089–1102 (2005).
Juliano, S.A. & Whitsel, B.L. A combined 2-deoxyglucose and neurophysiological study of primate somatosensory cortex. J. Comp. Neurol. 263, 514–525 (1987).
Devor, A. et al. Stimulus-induced changes in blood flow and 2-deoxyglucose uptake dissociate in ipsilateral somatosensory cortex. J. Neurosci. 28, 14347–14357 (2008).
Nudo, R.J. & Masterton, R.B. Stimulation induced [14C]2-deoxyglucose labeling of synaptic activity in the central nervous system. J. Comp. Neurol. 245, 553–565 (1986).
Rioult-Pedotti, M.-S., Friedman, D. & Donoghue, J.P. Learning-induced LTP in neocortex. Science 290, 533–536 (2000).
Adkins, D.L., Boychuk, J., Remple, M.S. & Kleim, J.A. Motor training induces experience-specific patterns of plasticity across motor cortex and spinal cord. J. Appl. Physiol. 101, 1776–1782 (2006).
Kilavik, B.E. et al. Long-term modifications in motor cortical dynamics induced by intensive practice. J. Neurosci. 29, 12653–12663 (2009).
Fu, M., Yu, X., Lu, J. & Zuo, Y. Repetitive motor learning induces coordinated formation of clustered dendritic spines in vivo. Nature 483, 92–95 (2012).
Rathelot, J.-A. & Strick, P.L. Subdivisions of primary motor cortex based on cortico-motoneuronal cells. Proc. Natl. Acad. Sci. USA 106, 918–923 (2009).
Shulman, R.G., Rothman, D.L. & Hyder, F. Stimulated changes in localized cerebral energy consumption under anesthesia. Proc. Natl. Acad. Sci. USA 96, 3245–3250 (1999).
Fu, Q.-G., Suarez, J.I. & Ebner, T.J. Neuronal specification of direction and distance during reaching movements in the superior precentral premotor area and primary motor cortex of monkeys. J. Neurophysiol. 70, 2097–2116 (1993).
Ashe, J. & Georgopoulos, A.P. Movement parameters and neural activity in motor cortex and area 5. Cereb. Cortex 4, 590–600 (1994).
Turner, R.S., Desmurget, M., Grethe, J., Crutcher, M.D. & Grafton, S.T. Motor subcircuits mediating the control of movement extent and speed. J. Neurophysiol. 90, 3958–3966 (2003).
Moran, D.W. & Schwartz, A.B. Motor cortical representation of speed and direction during reaching. J. Neurophysiol. 82, 2676–2692 (1999).
Stark, E., Drori, R., Asher, I., Ben-Shaul, Y. & Abeles, M. Distinct movement parameters are represented by different neurons in the motor cortex. Eur. J. Neurosci. 26, 1055–1066 (2007).
Wang, W., Chan, S.S., Heldman, D.A. & Moran, D.W. Motor cortical representation of position and velocity during reaching. J. Neurophysiol. 97, 4258–4270 (2007).
Orban, P. et al. Functional neuroanatomy associated with the expression of distinct movement kinematics in motor sequence learning. Neuroscience 179, 94–103 (2011).
This material is based on work supported in part by the Office of Research and Development, Medical Research Service, Department of Veterans Affairs, US National Institutes of Health grants R01 NS24328 (P.L.S.), P30 NS076405 (P.L.S.) and P01 NS044393 (P.L.S.). The contents do not represent the views of the Department of Veterans Affairs or the US Government. We are grateful to M. Page for the development of computer programs, and to M. O'Malley and K. McDonald for their expert technical assistance.
The authors declare no competing financial interests.
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Picard, N., Matsuzaka, Y. & Strick, P. Extended practice of a motor skill is associated with reduced metabolic activity in M1. Nat Neurosci 16, 1340–1347 (2013). https://doi.org/10.1038/nn.3477
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