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Extended practice of a motor skill is associated with reduced metabolic activity in M1

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Abstract

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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Figure 1: Activation during the Lick task.
Figure 2: Activation during the Track and Rem tasks.
Figure 3: Activation during the Random and Repeating tasks.
Figure 4: Comparison of activation measures in arm M1.
Figure 5: Single-neuron activity in a penetration through an area of high 2DG uptake (monkey N14).
Figure 6: Single-neuron activity in a penetration through an area of low 2DG uptake (monkey N14).
Figure 7: Relation between local average 2DG uptake and neuron activity.

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References

  1. 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).

    Article  Google Scholar 

  2. Proctor, R.W. & Dutta, A. Skill acquisition and human performance (Sage Publications, 1995).

  3. Dayan, E. & Cohen, L.G. Neuroplasticity subserving motor skill learning. Neuron 72, 443–454 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Amunts, K. et al. Motor cortex and hand motor skills: Structural compliance in the human brain. Hum. Brain Mapp. 5, 206–215 (1997).

    Article  CAS  PubMed  Google Scholar 

  5. Gaser, C. & Schlaug, G. Brain structures differ between musicians and non-musicians. J. Neurosci. 23, 9240–9245 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. 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).

    Article  CAS  PubMed  Google Scholar 

  7. Schwenkreis, P. et al. Assessment of sensorimotor cortical representation asymmetries and motor skills in violin players. Eur. J. Neurosci. 26, 3291–3302 (2007).

    Article  PubMed  Google Scholar 

  8. 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).

    Article  CAS  PubMed  Google Scholar 

  9. 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).

    Article  CAS  PubMed  Google Scholar 

  10. 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).

    Article  PubMed  Google Scholar 

  11. Haslinger, B. et al. Reduced recruitment of motor association areas during bimanual coordination in concert pianists. Hum. Brain Mapp. 22, 206–215 (2004).

    Article  PubMed  PubMed Central  Google Scholar 

  12. 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).

    Article  PubMed  PubMed Central  Google Scholar 

  13. Floyer-Lea, A. & Matthews, P.M. Changing brain networks for visuomotor control with increased movement automaticity. J. Neurophysiol. 92, 2405–2412 (2004).

    Article  CAS  PubMed  Google Scholar 

  14. 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).

    Article  PubMed  Google Scholar 

  15. 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).

    Article  PubMed  Google Scholar 

  16. 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).

    Article  CAS  PubMed  Google Scholar 

  17. 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).

    Article  CAS  PubMed  Google Scholar 

  18. Ben-Shaul, Y. et al. Neuronal activity in motor cortical areas reflects the sequential context of movement. J. Neurophysiol. 91, 1748–1762 (2004).

    Article  PubMed  Google Scholar 

  19. Lu, X. & Ashe, J. Anticipatory activity in primary motor cortex codes memorized movement sequences. Neuron 45, 967–973 (2005).

    Article  CAS  PubMed  Google Scholar 

  20. 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).

    Article  PubMed  Google Scholar 

  21. 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).

    Article  CAS  PubMed  Google Scholar 

  22. Picard, N. & Strick, P.L. Activation of the supplementary motor area (SMA) during performance of visually guided movements. Cereb. Cortex 13, 977–986 (2003).

    Article  PubMed  Google Scholar 

  23. Sokoloff, L. Sites and mechanisms of function-related changes in energy metabolism in the nervous system. Dev. Neurosci. 15, 194–206 (1993).

    Article  CAS  PubMed  Google Scholar 

  24. Smith, A.J. et al. Cerebral energetics and spiking frequency: the neurophysiological basis of fMRI. Proc. Natl. Acad. Sci. USA 99, 10765–10770 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Kim, D.-S. et al. Spatial relationship between neuronal activity and BOLD functional MRI. Neuroimage 21, 876–885 (2004).

    Article  PubMed  Google Scholar 

  26. Logothetis, N.K. What we can do and what we cannot do with fMRI. Nature 453, 869–878 (2008).

    Article  CAS  PubMed  Google Scholar 

  27. Matsunami, K. & Kawashima, T. Radioactive 2-DG incorporation patterns in the mesial frontal cortex of task-performing monkeys. Neurosci. Res. 23, 365–375 (1995).

    Article  CAS  PubMed  Google Scholar 

  28. Savaki, H.E. & Dalezios, Y. 14C-deoxyglucose mapping of the monkey brain during reaching to visual targets. Prog. Neurobiol. 58, 473–540 (1999).

    Article  CAS  PubMed  Google Scholar 

  29. 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).

    Article  CAS  PubMed  Google Scholar 

  30. Mushiake, H. & Strick, P.L. Preferential activity of dentate neurons during limb movements guided by vision. J. Neurophysiol. 70, 2660–2664 (1993).

    Article  CAS  PubMed  Google Scholar 

  31. 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).

    Article  CAS  PubMed  Google Scholar 

  32. 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).

    Article  CAS  PubMed  Google Scholar 

  33. 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).

    Article  PubMed  PubMed Central  Google Scholar 

  34. Poldrack, R.A. Imaging brain plasticity: conceptual and methodological issues—A theoretical perspective. Neuroimage 12, 1–13 (2000).

    Article  CAS  PubMed  Google Scholar 

  35. Grill-Spector, K., Henson, R. & Martin, A. Repetition and the brain: neural models of stimulus-specific effects. Trends Cogn. Sci. 10, 14–23 (2006).

    Article  PubMed  Google Scholar 

  36. Hamilton, A.F.C. & Grafton, S.T. Repetition suppression for performed hand gestures revealed by fMRI. Hum. Brain Mapp. 30, 2898–2906 (2009).

    Article  PubMed  Google Scholar 

  37. 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).

    Article  CAS  PubMed  Google Scholar 

  38. 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).

    Article  CAS  PubMed  Google Scholar 

  39. Jueptner, M. & Weiller, C. Does measurement of regional cerebral blood flow reflect synaptic activity?—Implications for PET and fMRI. Neuroimage 2, 148–156 (1995).

    Article  CAS  PubMed  Google Scholar 

  40. Magistretti, P.J. Neuron-glia metabolic coupling and plasticity. J. Exp. Biol. 209, 2304–2311 (2006).

    Article  CAS  PubMed  Google Scholar 

  41. Karni, A. et al. Functional evidence for adult motor cortex plasticity during motor skill learning. Nature 377, 155–158 (1995).

    Article  CAS  PubMed  Google Scholar 

  42. 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).

    Article  PubMed  Google Scholar 

  43. Kelly, A.M.C. & Garavan, H. Human functional neuroimaging of brain changes associated with practice. Cereb. Cortex 15, 1089–1102 (2005).

    Article  PubMed  Google Scholar 

  44. Juliano, S.A. & Whitsel, B.L. A combined 2-deoxyglucose and neurophysiological study of primate somatosensory cortex. J. Comp. Neurol. 263, 514–525 (1987).

    Article  CAS  PubMed  Google Scholar 

  45. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. 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).

    Article  CAS  PubMed  Google Scholar 

  47. Rioult-Pedotti, M.-S., Friedman, D. & Donoghue, J.P. Learning-induced LTP in neocortex. Science 290, 533–536 (2000).

    Article  CAS  PubMed  Google Scholar 

  48. 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).

    Article  PubMed  Google Scholar 

  49. Kilavik, B.E. et al. Long-term modifications in motor cortical dynamics induced by intensive practice. J. Neurosci. 29, 12653–12663 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. 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).

    Article  CAS  PubMed  Google Scholar 

  54. Ashe, J. & Georgopoulos, A.P. Movement parameters and neural activity in motor cortex and area 5. Cereb. Cortex 4, 590–600 (1994).

    Article  CAS  PubMed  Google Scholar 

  55. 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).

    Article  PubMed  Google Scholar 

  56. Moran, D.W. & Schwartz, A.B. Motor cortical representation of speed and direction during reaching. J. Neurophysiol. 82, 2676–2692 (1999).

    Article  CAS  PubMed  Google Scholar 

  57. 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).

    Article  PubMed  Google Scholar 

  58. 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).

    Article  PubMed  Google Scholar 

  59. Orban, P. et al. Functional neuroanatomy associated with the expression of distinct movement kinematics in motor sequence learning. Neuroscience 179, 94–103 (2011).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

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.

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N.P. conducted the 2DG experiments, Y.M. recorded single neuron activity, N.P. analyzed data, and N.P. and P.L.S. wrote the manuscript.

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Correspondence to Peter L Strick.

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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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