Abstract
In humans, learning to produce correct visually guided movements to adapt to new sensorimotor conditions requires the formation of an internal model that represents the new transformation between visual input and the required motor command. When the new environment requires adaptation to directional errors, learning generalizes poorly to untrained locations and directions, indicating that such learning is local. Here we replicated these behavioral findings in rhesus monkeys using a visuomotor rotation task and simultaneously recorded neuronal activity. Specific changes in activity were observed only in a subpopulation of cells in the motor cortex with directional properties corresponding to the locally learned rotation. These changes adhered to the dynamics of behavior during learning and persisted between learning and relearning of the same rotation. These findings suggest a neural mechanism for the locality of newly acquired sensorimotor tasks and provide electrophysiological evidence for their retention in working memory.
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References
Soechting, J.F. & Flanders, M. Sensorimotor representations for pointing to targets in three-dimensional space. J. Neurophysiol. 62, 582–594 (1989).
Kalaska, J.F., Scott, S.H., Cisek, P. & Sergio, L.E. Cortical control of reaching movements. Curr. Opin. Neurobiol. 7, 849–859 (1997).
Buneo, C.A., Jarvis, M.R., Batista, A.P. & Andersen, R.A. Direct visuomotor transformations for reaching. Nature 416, 632–636 (2002).
Shadmehr, R. & Mussa-Ivaldi, F.A. Adaptive representation of dynamics during learning of a motor task. J. Neurosci. 14, 3208–3224 (1994).
Kawato, M. Internal models for motor control and trajectory planning. Curr. Opin. Neurobiol. 9, 718–727 (1999).
Wolpert, D.M. & Ghahramani, Z. Computational principles of movement neuroscience. Nat. Neurosci. 3 (Suppl.), 1212–1217 (2000).
Gandolfo, F., Mussa-Ivaldi, F.A. & Bizzi, E. Motor learning by field approximation. Proc. Natl. Acad. Sci. USA 93, 3843–3846 (1996).
Pine, Z.M., Krakauer, J.W., Gordon, J. & Ghez, C. Learning of scaling factors and reference axes for reaching movements. Neuroreport 7, 2357–2361 (1996).
Ghahramani, Z., Wolpert, D.M. & Jordan, M.I. Generalization to local remappings of the visuomotor coordinate transformation. J. Neurosci. 16, 7085–7096 (1996).
Baraduc, P. & Wolpert, D.M. Adaptation to a visuomotor shift depends on the starting posture. J. Neurophysiol. 88, 973–981 (2002).
Shadmehr, R. & Moussavi, Z.M. Spatial generalization from learning dynamics of reaching movements. J. Neurosci. 20, 7807–7815 (2000).
Georgopoulos, A.P., Kalaska, J.F., Caminiti, R. & Massey, J.T. On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex. J. Neurosci. 2, 1527–1537 (1982).
Kakei, S., Hoffman, D.S. & Strick, P.L. Muscle and movement representations in the primary motor cortex. Science 285, 2136–2139 (1999).
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).
Gribble, P.L. & Scott, S.H. Overlap of internal models in motor cortex for mechanical loads during reaching. Nature 417, 938–941 (2002).
Padoa-Schioppa, C., Li, C.S.-R. & Bizzi, E. Neuronal correlates of kinematics-to-dynamics transformation in the supplementary motor area. Neuron 36, 751–765 (2002).
Wise, S.P., Moody, S.L., Blomstrom, K.J. & Mitz, A.R. Changes in motor cortical activity during visuomotor adaptation. Exp. Brain Res. 121, 285–299 (1998).
Sanes, J.N. & Donoghue, J.P. Plasticity and primary motor cortex. Annu. Rev. Neurosci. 23, 393–415 (2000).
Hess, G. & Donoghue, J.P. Long-term depression of horizontal connections in rat motor cortex. Eur. J. Neurosci. 8, 658–665 (1996).
Rioult, P.M., Friedman, D., Hess, G. & Donoghue, J.P. Strengthening of horizontal cortical connections following skill learning. Nat. Neurosci. 1, 230–234 (1998).
Karni, A. et al. Functional MRI evidence for adult motor cortex plasticity during motor skill learning. Nature 377, 155–158 (1995).
Jenkins, I.H., Brooks, D.J., Nixon, P.D., Frackowiak, R.S. & Passingham, R.E. Motor sequence learning: a study with positron emission tomography. J. Neurosci. 14, 3775–3790 (1994).
Muellbacher, W., Ziemann, U., Boroojerdi, B., Cohen, L. & Hallett, M. Role of the human motor cortex in rapid motor learning. Exp. Brain Res. 136, 431–438 (2001).
Shadmehr, R. & Holcomb, H.H. Neural correlates of motor memory consolidation. Science 277, 821–825 (1997).
Brashers-Krug, T., Shadmehr, R. & Bizzi, E. Consolidation in human motor memory. Nature 382, 252–255 (1996).
Muellbacher, W. et al. Early consolidation in human primary motor cortex. Nature 415, 640–644 (2002).
Krakauer, J.W., Ghilardi, M.F. & Ghez, C. Independent learning of internal models for kinematic and dynamic control of reaching. Nat. Neurosci. 2, 1026–1031 (1999).
Thoroughman, K.A. & Shadmehr, R. Electromyographic correlates of learning an internal model of reaching movements. J. Neurosci. 19, 8573–8588 (1999).
Nezafat, R., Shadmehr, R. & Holcomb, H.H. Long-term adaptation to dynamics of reaching movements: a PET study. Exp. Brain Res. 140, 66–76 (2001).
Osu, R. et al. Short- and long-term changes in joint co-contraction associated with motor learning as revealed from surface EMG. J. Neurophysiol. 88, 991–1004 (2002).
Nudo, R.J., Milliken, G.W., Jenkins, W.M. & Merzenich, M.M. Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys. J. Neurosci. 16, 785–807 (1996).
Plautz, E.J., Milliken, G.W. & Nudo, R.J. Effects of repetitive motor training on movement representations in adult squirrel monkeys: role of use versus learning. Neurobiol. Learn. Mem. 74, 27–55 (2000).
Poggio, T. & Girosi, F. Theory of networks for learning. Science 247, 978–982 (1990).
Schaal, S. & Atkeson, C.G. Constructive incremental learning from only local information. Neural Comput. 10, 2047–2084 (1998).
Pouget, A. & Snyder, L.H. Computational approaches to sensorimotor transformations. Nat. Neurosci. 3 (Suppl.), 1192–1198 (2000).
Thoroughman, K.A. & Shadmehr, R. Learning of action through adaptive combination of motor primitives. Nature 407, 742–747 (2000).
Kalaska, J.F., Cohen, D.A., Hyde, M.L. & Prud'homme, M. 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 (1989).
Mitz, A.R., Godschalk, M. & Wise, S.P. Learning-dependent neuronal activity in the premotor cortex: activity during the acquisition of conditional motor associations. J. Neurosci. 11, 1855–1872 (1991).
Yin, P.B. & Kitazawa, S. Long-lasting aftereffects of prism adaptation in the monkey. Exp. Brain Res. 141, 250–253 (2001).
Alexander, G.E. & Crutcher, M.D. Preparation for movement: neural representations of intended direction in three motor areas of the monkey. J. Neurophysiol. 64, 133–150 (1990).
Crammond, D.J. & Kalaska, J.F. Modulation of preparatory neuronal activity in dorsal premotor cortex due to stimulus-response compatibility. J. Neurophysiol. 71, 1281–1284 (1994).
Wise, S.P., Di Pellegrino, G. & Boussaoud, D. The premotor cortex and nonstandard sensorimotor mapping. Can. J. Physiol. Pharmacol. 74, 469–482 (1996).
Shen, L. & Alexander, G.E. Preferential representation of instructed target location versus limb trajectory in dorsal premotor area. J. Neurophysiol. 77, 1195–1212 (1997).
Kakei, S., Hoffman, D.S. & Strick, P.L. Direction of action is represented in the ventral premotor cortex. Nat. Neurosci. 4, 1020–1025 (2001).
Tong, C., Wolpert, D.M. & Flanagan, J.R. Kinematics and dynamics are not represented independently in motor working memory: evidence from an interference study. J. Neurosci. 22, 1108–1113 (2002).
Flanagan, J.R. et al. Composition and decomposition of internal models in motor learning under altered kinematic and dynamic environments. J. Neurosci. 19, RC34 (1999).
Acknowledgements
We thank S. Wise, S. Cardoso de Oliveira and R. Shadmehr for discussions and comments on earlier versions of this manuscript, and G. Goelman for the MRI. This study was partly supported by a Center of Excellence grant (8006/00) administrated by the Israeli Science Foundation (ISF) and by the German Federal Ministry of Education and Research (BMBF) within the framework of German-Israeli project cooperation (DIP). R.P. was supported by the Constantiner fellowship.
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Paz, R., Boraud, T., Natan, C. et al. Preparatory activity in motor cortex reflects learning of local visuomotor skills. Nat Neurosci 6, 882–890 (2003). https://doi.org/10.1038/nn1097
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DOI: https://doi.org/10.1038/nn1097
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