Abstract
When people learn to reach in a novel sensorimotor environment, there are changes in the muscle activity required to achieve task goals. Here, we assessed the time course of changes in muscle directional tuning during acquisition of a new mapping between visual information and isometric force production in the absence of feedback-based error corrections. We also measured the influence of visuomotor adaptation on corticospinal excitability, to test whether any changes in muscle directional tuning are associated with adaptations in the final output components of the sensorimotor control system. Nine right-handed subjects performed a ballistic, center-out isometric target acquisition task with the right wrist (16 targets spaced every 22.5° in the joint space). Surface electromyography was recorded from four major wrist muscles, and motor evoked potentials induced by transcranial magnetic stimulation were measured at baseline, after task execution in the absence of the rotation (A1), after adaptation to the rotation (B), and after a final block of trials without rotation (A2). Changes in the directional tuning of muscles closely matched the rotation of the directional error in force, indicating that the functional contribution of muscles remained consistent over the adaptation period. In contrast to previous motor learning studies, we found only minor changes in the amount of muscular activity and no increase in corticospinal excitability. These results suggest that increased muscle co-activation occurs only when the dynamics of the limb are perturbed and/or that online error corrections or altered force requirements are necessary to elicit a component of the adaptation in the final steps of the transformation between motor goal and muscle activation.
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References
Antal A, Nitsche MA, Kincses TZ, Kruse W, Hoffmann KP, Paulus W (2004) Facilitation of visuo-motor learning by transcranial direct current stimulation of the motor and extrastriate visual areas in humans. Eur J Neurosci 19:2888–2892
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
Buchanan TS, Rovai GP, Rymer WZ (1989) Strategies for muscle activation during isometric torque generation at the human elbow. J Neurophysiol 62:1201–1212
Cothros N, Köhler S, Dickie EW, Mirsattari SM, Gribble PL (2006) Proactive interference as a result of persisting neural representations of previously learned motor skills in primary motor cortex. J Cogn Neurosci 18:2167–2176
Darainy M, Ostry DJ (2008) Muscle cocontraction following dynamics learning. Exp Brain Res 190:153–163
de Rugy A (2010) Modulation of muscle synergies during sensorimotor adaptation: experiment and model. Hum Movement Sci. Accepted 31 Jan 2010 (in press)
de Rugy A, Hinder MR, Woolley DG, Carson RG (2009) The synergistic organization of muscle recruitment constrains visuomotor adaptation. J Neurophysiol 101:2263–2269
Flanders M (1991) Temporal patterns of muscle activation for arm movements in three-dimensional space. J Neurosci 11:2680–2693
Franklin DW, Osu R, Burdet E, Kawato M, Milner TE (2003) Adaptation to stable and unstable dynamics achieved by combined impedance control and inverse dynamics model. J Neurophysiol 90:3270–3282
Gandolfo F, Li C, Benda BJ, Schioppa CP, Bizzi E (2000) Cortical correlates of learning in monkeys adapting to a new dynamical environment. Proc Natl Acad Sci USA 97:2259–2263
Ghilardi MF, Gordon J, Ghez C (1995) Learning a visuomotor transformation in a local area of work space produces directional biases in other areas. J Neurophysiol 73:2535–2539
Hadipour-Niktarash A, Lee CK, Desmond JE, Shadmehr R (2007) Impairment of retention but not acquisition of a visuomotor skill through time-dependent disruption of primary motor cortex. J Neurosci 27:13413–13419
Haruno M, Wolpert DM (2005) Optimal control of redundant muscles in step-tracking wrist movements. J Neurophysiol 94:4244–4255
Hinder MR, Tresilian JR, Riek S, Carson RG (2008) The contribution of visual feedback to visuomotor adaptation: how much and when? Brain Res 1197:123–134
Hinder MR, Riek S, Tresilian JR, de Rugy A, Carson RG (2010) Real-time error detection but not error correction drives automatic visuomotor adaptation. Exp Brain Res 201:191–207
Hoffman DS, Strick PL (1999) Step-tracking movements of the wrist. IV. Muscle activity associated with movements in different directions. J Neurophysiol 81:319–333
Hunter T, Sacco P, Nitsche MA, Turner DL (2009) Modulation of internal model formation during force field-induced motor learning by anodal transcranial direct current stimulation of primary motor cortex. J Physiol 587:2949–2961
Jensen JL, Marstrand PC, Nielsen JB (2005) Motor skill training and strength training are associated with different plastic changes in the central nervous system. J Appl Physiol 99:1558–1568
Keppel G (1991) Design and analysis: a researcher’s handbook, 3rd edn. Prentice-Hall, Englewood Cliffs
Krakauer JW (2009) Motor learning and consolidation: the case of visuomotor rotation. Adv Exp Med Biol 629:405–421
Krakauer JW, Ghilardi MF, Ghez C (1999) Independent learning of internal models for kinematic and dynamic control of reaching. Nat Neurosci 2:1026–1031
Kudo K, Ohtsuki T (1998) Functional modification of agonist-antagonist electromyographic activity for rapid movement inhibition. Exp Brain Res 122:23–30
Lee M, Carroll TJ (2005) The amplitude of Mmax in human wrist flexors varies during different muscle contractions despite constant posture. J Neurosci Methods 149:95–100
Li CS, 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
Ljubisavljevic M (2006) Transcranial magnetic stimulation and the motor learning-associated cortical plasticity. Exp Brain Res 173:215–222
Muellbacher W, Ziemann U, Boroojerdi B, Cohen L, Hallett M (2001) Role of the human motor cortex in rapid motor learning. Exp Brain Res 136:431–438
Muellbacher W, Ziemann U, Wissel J, Dang N, Kofler M, Facchini S, Boroojerdi B, Poewe W, Hallett M (2002) Early consolidation in human primary motor cortex. Nature 415:640–644
Nitsche MA, Paulus W (2000) Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol 527(Pt 3):633–639
Osu R, Franklin DW, Kato H, Gomi H, Domen K, Yoshioka T, Kawato M (2002) Short- and long-term changes in joint co-contraction associated with motor learning as revealed from surface EMG. J Neurophysiol 88:991–1004
Pascual-Leone A, Nguyet D, Cohen LG, Brasil-Neto JP, Cammarota A, Hallett M (1995) Modulation of muscle responses evoked by transcranial magnetic stimulation during the acquisition of new fine motor skills. J Neurophysiol 74:1037–1045
Paz R, Vaadia E (2005) Specificity of sensorimotor learning and the neural code: neuronal representations in the primary motor cortex. J Physiol Paris 98:331–348
Paz R, Boraud T, Natan C, Bergman H, Vaadia E (2003) Preparatory activity in motor cortex reflects learning of local visuomotor skills. Nat Neurosci 6:882–890
Paz R, Natan C, Boraud T, Bergman H, Vaadia E (2005) Emerging patterns of neuronal responses in supplementary and primary motor areas during sensorimotor adaptation. J Neurosci 25:10941–10951
Reis J, Schambra HM, Cohen LG, Buch ER, Fritsch B, Zarahn E, Celnik PA, Krakauer JW (2009) Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation. Proc Natl Acad Sci USA 106:1590–1595
Riek S, Carson RG, Wright A (2000) A new technique for the selective recording of extensor carpi radialis longus and brevis EMG. J Electromyogr Kinesiol 10:249–253
Rioult-Pedotti MS, Friedman D, Hess G, Donoghue JP (1998) Strengthening of horizontal cortical connections following skill learning. Nat Neurosci 1:230–234
Sanes JN, Donoghue JP (2000) Plasticity and primary motor cortex. Annu Rev Neurosci 23:393–415
Teasdale N, Bard C, Fleury M, Young DE, Proteau L (1993) Determining movement onsets from temporal series. J Mot Behav 25:97–106
Thoroughman KA, Shadmehr R (1999) Electromyographic correlates of learning an internal model of reaching movements. J Neurosci 19:8573–8588
Tseng YW, Diedrichsen J, Krakauer JW, Shadmehr R, Bastian AJ (2007) Sensory prediction errors drive cerebellum-dependent adaptation of reaching. J Neurophysiol 98:54–62
Ziemann U, Ilic TV, Pauli C, Meintzschel F, Ruge D (2004) Learning modifies subsequent induction of long-term potentiation-like and long-term depression-like plasticity in human motor cortex. J Neurosci 24:1666–1672
Acknowledgments
We thank Daniel Dymond for his help with the experiment and David Lloyd for the figure of the apparatus. Grants This work was founded by The Australian Research Council (ARC-DP0770982).
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de Rugy, A., Carroll, T.J. Changes in muscle directional tuning parallel feedforward adaptation to a visuomotor rotation. Exp Brain Res 203, 701–709 (2010). https://doi.org/10.1007/s00221-010-2280-9
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DOI: https://doi.org/10.1007/s00221-010-2280-9