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Cortical Processing during Dynamic Motor Adaptation

  • Simon A. Overduin
  • Andrew G. Richardson
  • Emilio Bizzi
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 629)

Abstract

In this chapter we investigate the role of motor cortex in adapting movements to novel dynamic environments. We present results from two experiments in which monkey or human subjects learned to make two-dimensional reaching movements while holding a robotic manipulandum that applied a predictable pattern of forces (a curl field) to their hand. In the first study, we analyzed electrophysiological data recorded in motor cortex while monkeys adapted or readapted to the novel forces on each day of the experiment. In the second study, we perturbed the excitability of motor cortex using repetitive transcranial magnetic stimulation (rTMS) as human participants adapted to the forces. From the first experiment, we present qualitative evidence that a network of cortical areas including the supplementary motor area, premotor cortex, and primary motor cortex (M1) not only encodes kinematic and dynamic parameters of motor execution, but also registers changes in encoding that could provide a substrate for motor memory. Based on the second experiment, we qualify the role of M1 in motor memory, by showing that its disruption by rTMS does not interfere with the process of initial motor adaptation, but rather with offline improvement as measured at retest on the following day.

Keywords

Transcranial Magnetic Stimulation Prefer Direction Motor Learning Movement Onset Motor Memory 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Baraduc P, Lang N, Rothwell JC, Wolpert DM (2004) Consolidation of dynamic motor learning is not disrupted by rTMS of primary motor cortex. Curr Biol 14: 252–256.PubMedGoogle Scholar
  2. Chen H, Hua SE, Smith MA, Lenz FA, Shadmehr R (2006) Effects of human cerebellar thalamus disruption on adaptive control of reaching. Cereb Cortex 16: 1462–1473.PubMedCrossRefGoogle Scholar
  3. Chen R, Classen J, Gerloff C, Celnik P, Wassermann EM, Hallett M, Cohen LG (1997) Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 48: 1398–1403.PubMedGoogle Scholar
  4. Cheney PD, Fetz EE (1980) Functional classes of primate corticomotoneuronal cells and their relation to active force. J Neurophysiol 44: 773–791.PubMedGoogle Scholar
  5. Della-Maggiore V, Malfait N, Ostry DJ, Paus T (2004) Stimulation of the posterior parietal cortex interferes with arm trajectory adjustments during the learning of new dynamics. J Neurosci 24: 9971–9976.PubMedCrossRefGoogle Scholar
  6. Diedrichsen J, Hashambhoy Y, Rane T, Shadmehr R (2005) Neural correlates of reach errors. J Neurosci 25: 9919–9931.PubMedCrossRefGoogle Scholar
  7. Donchin O, Sawaki L, Madupu G, Cohen LG, Shadmehr R (2002) Mechanisms influencing acquisition and recall of motor memories. J Neurophysiol 88: 2114–2123.PubMedCrossRefGoogle Scholar
  8. Evarts EV (1968) Relation of pyramidal tract activity to force exerted during voluntary movement. J Neurophysiol 31: 14–27.PubMedGoogle Scholar
  9. Fayé IC (1983) An impedance controlled manipulandum for human movement studies. M.S. Thesis. Cambridge, MA: MIT Press.Google Scholar
  10. ∗Gandolfo F, Li CR, Benda BJ, Padoa-Schioppa C, Bizzi E (2000) Cortical correlates of learning in monkeys adapting to a new dynamical environment. Proc Natl Acad Sci USA 97: 2259–2263.PubMedCrossRefGoogle Scholar
  11. Gangitano M, Valero-Cabré A, Tormos JM, Mottaghy FM, Romero JR, Pascual-Leone A (2002) Modulation of input-output curves by low and high frequency repetitive transcranial magnetic stimulation of the motor cortex. Clin Neurophysiol 113: 1249–1257.PubMedCrossRefGoogle Scholar
  12. Humphrey DR, Schmidt EM, Thompson WD (1970) Predicting measures of motor performance from multiple cortical spike trains. Science 170: 758–762.PubMedCrossRefGoogle Scholar
  13. Kalaska JF, Cohen DA, Hyde ML, Prud’homme M (1989) A comparison of movement direction-related versus load direction-related activity in primate motor cortex, using a two-dimensional reaching task. J Neurosci 9: 2080–2102.PubMedGoogle Scholar
  14. Karniel A, Mussa-Ivaldi FA (2003) Sequence, time, or state representation: how does the motor control system adapt to variable environments? Biol Cybern 89: 10–21.PubMedGoogle Scholar
  15. Krebs HI, Brashers-Krug T, Rauch SL, Savage CR, Hogan N, Rubin RH, Fischman AJ, Alpert NM (1998) Robot-aided functional imaging: application to a motor learning study. Hum Brain Mapp 6: 59–72.PubMedCrossRefGoogle Scholar
  16. Lackner JR, DiZio P (1994) Rapid adaptation to Coriolis force perturbations of arm trajectory. J Neurophysiol 72: 299–313.PubMedGoogle Scholar
  17. Lee L, Siebner HR, Rowe JB, Rizzo V, Rothwell JC, Frackowiak RS, Friston KJ (2003) Acute remapping within the motor system induced by low-frequency repetitive transcranial magnetic stimulation. J Neurosci 23: 5308–5318.PubMedGoogle Scholar
  18. Li CR, Padoa-Schioppa C, Bizzi E (2001) 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.PubMedCrossRefGoogle Scholar
  19. Maschke M., Gomez CM, Ebner TJ, Konczak J (2004) Hereditary cerebellar ataxia progressively impairs force adaptation during goal-directed arm movements. J Neurophysiol 91: 230–238.PubMedCrossRefGoogle Scholar
  20. ∗Muellbacher W, Ziemann U, Wissel J, Dang N, Kofler M, Faccini S, Boroojerdi B, Poewe W, Hallett M (2002) Early consolidation in human primary motor cortex. Nature 415: 640–644.PubMedCrossRefGoogle Scholar
  21. Padoa-Schioppa C, Li CR, Bizzi E (2002) Neuronal correlates of kinematics-to-dynamics transformation in the supplementary motor area. Neuron 36: 751–765.PubMedCrossRefGoogle Scholar
  22. Padoa-Schioppa C, Li CR, Bizzi E (2004) Neuronal activity in the supplementary motor area of monkeys adapting to a new dynamical environment. J Neurophysiol 91: 449–473.PubMedCrossRefGoogle Scholar
  23. Pascual-Leone A, Grafman J, Hallett M (1994) Modulation of cortical motor output maps during development of implicit and explicit knowledge. Science 263: 1287–1289.PubMedCrossRefGoogle Scholar
  24. Paz R, Natan C, Boraud T, Bergman H, and Vaadia E (2005) Emerging patterns of neuronal responses in supplementary and primary motor areas during sensorimotor adaptation. J Neurosci 25: 10941–10951.PubMedCrossRefGoogle Scholar
  25. ∗Richardson AG, Overduin SA, Valero-Cabré A, Padoa-Schioppa C, Pascual-Leone A, Bizzi E, Press DZ (2006) Disruption of primary motor cortex prior to learning impairs memory of movement dynamics. J Neurosci 26: 12466–12470.PubMedCrossRefGoogle Scholar
  26. ∗Robertson EM, Pascual-Leone A, Miall RC (2004) Current concepts in procedural consolidation. Nat Rev Neurosci 5: 1–7.CrossRefGoogle Scholar
  27. Robertson EM, Press DZ, Pascual-Leone A (2005) Off-line learning and the primary motor cortex. J Neurosci 25: 6372–6378.PubMedCrossRefGoogle Scholar
  28. Robertson EM, Theoret H, Pascual-Leone A (2003) Studies in cognition: the problems solved and created by transcranial magnetic stimulation. J Cogn Neurosci 15: 948–960.PubMedCrossRefGoogle Scholar
  29. Romero JR, Anschel D, Sparing R, Gangitano M, Pascual-Leone A (2002) Subthreshold low frequency repetitive transcranial magnetic stimulation selectively decreases facilitation in the motor cortex. Clin Neurophysiol. 113: 101–107.PubMedCrossRefGoogle Scholar
  30. Sanes JN, Donoghue JP (2000) Plasticity and primary motor cortex. Annu Rev Neurosci 23: 393–415.PubMedCrossRefGoogle Scholar
  31. ∗Shadmehr R, Holcomb HH (1997) Neural correlates of motor memory consolidation. Science 277: 821–825.PubMedCrossRefGoogle Scholar
  32. Shadmehr R, Moussavi ZMK (2000) Spatial generalization from learning dynamics of reaching movements. J Neurosci 20: 7807–7815.PubMedGoogle Scholar
  33. ∗Shadmehr R, Mussa-Ivaldi FA (1994) Adaptive representation of dynamics during learning of a motor task. J Neurosci 14: 3208–3224.PubMedGoogle Scholar
  34. Smith MA, Shadmehr R (2005) Intact ability to learn internal models of arm dynamics in Huntington’s disease but not cerebellar degeneration. J Neurophysiol 93: 2809–2821.PubMedCrossRefGoogle Scholar
  35. Thach WT (1978) Correlation of neural discharge with pattern and force of muscular activity, joint position, and direction of intended next movement in motor cortex and cerebellum. J Neurophysiol 41:654–676.PubMedGoogle Scholar
  36. Thoroughman KA, Shadmehr R (1999) Electromyographic correlates of learning an internal model of reaching movements. J Neurosci 19: 8573–8588.PubMedGoogle Scholar
  37. Walker MP (2005) A refined model of sleep and the time course of memory formation. Behav Brain Sci 28: 51–104.PubMedGoogle Scholar
  38. Xiao J, Padoa-Schioppa C, Bizzi E (2006) Neuronal correlates of movement dynamics in the dorsal and ventral premotor area in the monkey. Exp Brain Res 168: 106–119.PubMedCrossRefGoogle Scholar
  39. The references marked with an asterisk (*) are specifically recommended for further introduction or background to the topic.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Simon A. Overduin
    • 1
  • Andrew G. Richardson
  • Emilio Bizzi
  1. 1.Department of Brain and Cognitive Sciences and McGovern Institute for Brain ResearchMassachusetts Institute of TechnologyCambridgeUSA

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