Impedance control is selectively tuned to multiple directions of movement

Journal of Neurophysiology

Volumn 106, Issue 5, 2011, Pages 2737-2748

  Kadiallah, Abdelhamid ^a   Liaw, Gary ^b   Kawato, Mitsuo ^c   Franklin, David W ^b,c,d   Burdet, Etienne ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b NATIONAL INSTITUTE OF INFORMATION AND COMMUNICATIONS TECHNOLOGY   (Japan)

^c ADVANCED TELECOMMUNICATIONS RESEARCH INSTITUTE INTERNATIONAL   (Japan)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Adaptation; Internal model; Stiffness; Unstable dynamics

Indexed keywords

ADAPTATION; ADULT; ARTICLE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; HUMAN; HUMAN EXPERIMENT; JOINT STIFFNESS; MALE; MECHANICAL IMPEDANCE; MOVEMENT (PHYSIOLOGY); MOVEMENT DIRECTION; MUSCLE STIFFNESS; NORMAL HUMAN; PHYSICAL RESISTANCE; PRIORITY JOURNAL; RIGIDITY; SIMULATION;

ADAPTATION, PHYSIOLOGICAL; ADULT; ARM; COMPUTER SIMULATION; ELBOW JOINT; HUMANS; LEARNING; MALE; MODELS, BIOLOGICAL; MOTOR SKILLS; MOVEMENT; MUSCLE CONTRACTION; MUSCLE, SKELETAL; PRACTICE (PSYCHOLOGY); PSYCHOMOTOR PERFORMANCE; SHOULDER JOINT; YOUNG ADULT;

EID: 80755181463     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00079.2011     Document Type: Article

References (78)

1. Akazawa K, Milner TE, Stein RB. Modulation of reflex EMG and stiffness in response to stretch of human finger muscle. J Neurophysiol 49: 16-27, 1983.
2. Asai Y, Tasaka Y, Nomura K, Nomura T, Casadio M, Morasso P. A model of postural control in quiet standing: robust compensation of delay-induced instability using intermittent activation of feedback control. PLos One 4: e6169, 2009.
3. Brashers-Krug T, Shadmehr R, Bizzi E. Consolidation in human motor memory. Nature 382: 252-255, 1996.
4. Burdet E, Osu R, Franklin DW, Milner TE, Kawato M. The central nervous system stabilizes unstable dynamics by learning optimal impedance. Nature 414: 446-449, 2001.
5. Burdet E, Osu R, Franklin DW, Yoshioka T, Milner TE, Kawato M. A method for measuring endpoint stiffness during multi-joint arm movements. J Biomech 33: 1705-1709, 2000.
6. Burdet E, Tee KP, Mareels I, Milner TE, Chew CM, Franklin DW, Osu R, Kawato M. Stability and motor adaptation in human arm movements. Biol Cybern 94: 20-32, 2006.
7. Caithness G, Osu R, Bays P, Chase H, Klassen J, Kawato M, Wolpert DM, Flanagan JR. Failure to consolidate the consolidation theory of learning for sensorimotor adaptation tasks. J Neurosci 24: 8662-8671, 2004.
8. Conditt MA, Gandolfo F, Mussa-Ivaldi FA. The motor system does not learn the dynamics of the arm by rote memorization of past experience. J Neurophysiol 78: 554-560, 1997.
9. Damm L, McIntyre J. Physiological basis of limb-impedance modulation during free and constrained movements. J Neurophysiol 100: 2577-2588, 2008.
10. Doemges F, Rack PM. Changes in the stretch reflex of the human first dorsal interosseous muscle during different tasks. J Physiol 447: 563-573, 1992a.
11. Doemges F, Rack PM. Task-dependent changes in the response of human wrist joints to mechanical disturbance. J Physiol 447: 575-585, 1992b.
12. Donchin O, Francis JT, Shadmehr R. Quantifying generalization from trial-by-trial behavior of adaptive systems that learn with basis functions: theory and experiments in human motor control. J Neurosci 23: 9032-9045, 2003.
13. Edman KA, Josephson RK. Determinants of force rise time during isometric contraction of frog muscle fibres. J Physiol 580: 1007-1019, 2007.
14. Flash T, Mussa-Ivaldi F. Human arm stiffness characteristics during the maintenance of posture. Exp Brain Res 82: 315-326, 1990.
15. Franklin DW, Burdet E, Osu R, Kawato M, Milner TE. Functional significance of stiffness in adaptation of multijoint arm movements to stable and unstable dynamics. Exp Brain Res 151: 145-157, 2003a.
16. Franklin DW, Burdet E, Tee KP, Osu R, Chew CM, Milner TE, Kawato M. CNS learns stable, accurate, and efficient movements using a simple algorithm. J Neurosci 28: 11165-11173, 2008.
17. Franklin DW, Liaw G, Milner TE, Osu R, Burdet E, Kawato M. Endpoint stiffness of the arm is directionally tuned to instability in the environment. J Neurosci 27: 7705-7716, 2007a.
18. Franklin DW, Milner TE. Adaptive control of stiffness to stabilize hand position with large loads. Exp Brain Res 152: 211-220, 2003.
19. Franklin DW, Osu R, Burdet E, Kawato M, Milner TE. Adaptation to stable and unstable dynamics achieved by combined impedance control and inverse dynamics model. J Neurophysiol 90: 3270-3282, 2003b.
20. Franklin DW, So U, Burdet E, Kawato M. Visual feedback is not necessary for the learning of novel dynamics. PLos One 2: e1336, 2007b.
21. Franklin DW, So U, Kawato M, Milner TE. Impedance control balances stability with metabolically costly muscle activation. J Neurophysiol 92: 3097-3105, 2004.
22. Gandolfo F, Mussa-Ivaldi FA, Bizzi E. Motor learning by field approximation. Proc Natl Acad Sci USA 93: 3843-3846, 1996.
23. Gomi H, Kawato. Equilibrium-point control hypothesis examined by measured arm stiffness during multijoint movement. Science 272: 117-120, 1996.
24. Gomi H, Kawato M. Human arm stiffness and equilibrium-point trajectory during multi-joint movement. Biol Cybern 76: 163-171, 1997.
25. Gomi H, Osu R. Task-dependent viscoelasticity of human multijoint arm and its spatial characteristics for interaction with environments. J Neurosci 18: 8965-8978, 1998.
26. Hamilton AF, Jones KE, Wolpert DM. The scaling of motor noise with muscle strength and motor unit number in humans. Exp Brain Res 157: 417-430, 2004.
27. Harris CM, Wolpert DM. Signal-dependent noise determines motor planning. Nature 394: 780-784, 1998.
28. Haruno M, Wolpert DM, Kawato M. Mosaic model for sensorimotor learning and control. Neural Comput 13: 2201-2220, 2001.
29. Hogan N. Adaptive control of mechanical impedance by coactivation of antagonist muscles. IEEE Trans Automat Contr AC-29: 681-690, 1984.
30. Hogan N. The mechanics of multi-joint posture and movement control. Biol Cybern 52: 315-331, 1985.
31. Howard IS, Ingram JN, Wolpert DM. Composition and decomposition in bimanual dynamic learning. J Neurosci 28: 10531-10540, 2008.
32. Howard IS, Ingram JN, Wolpert DM. Context-dependent partitioning of motor learning in bimanual movements. J Neurophysiol 104: 2082-2091, 2010.
33. Hwang EJ, Donchin O, Smith MA, Shadmehr R. A gain-field encoding of limb position and velocity in the internal model of arm dynamics. PLoS Biol 1: E25, 2003.
34. Ito T, Murano EZ, Gomi H. Fast force-generation dynamics of human articulatory muscles. J Appl Physiol 96: 2318-2324, 2004.
35. Kadiallah A. Generalisation in Human Motor Learning: Experimental and Modelling Studies. London: Imperial College, 2008.
36. Karniel A, Mussa-Ivaldi FA. Does the motor control system use multiple models and context switching to cope with a variable environment? Exp Brain Res 143: 520-524, 2002.
37. Krakauer JW, Ghilardi MF, Ghez C. Independent learning of internal models for kinematic and dynamic control of reaching. Nat Neurosci 2: 1026-1031, 1999.
38. Krutky MA, Ravichandran VJ, Trumbower RD, Perreault EJ. Interactions between limb and environmental mechanics influence stretch reflex sensitivity in the human arm. J Neurophysiol 103: 429-440, 2010.
39. Kurtzer IL, Pruszynski JA, Scott SH. Long-latency reflexes of the human arm reflect an internal model of limb dynamics. Curr Biol 18: 449-453, 2008.
40. Lametti DR, Houle G, Ostry DJ. Control of movement variability and the regulation of limb impedance. J Neurophysiol 98: 3516-3524, 2007.
41. Lewis GN, MacKinnon CD, Perreault EJ. The effect of task instruction on the excitability of spinal and supraspinal reflex pathways projecting to the biceps muscle. Exp Brain Res 174: 413-425, 2006.
42. Loram ID, Gollee H, Lakie M, Gawthrop PJ. Human control of an inverted pendulum: is continuous control necessary? Is intermittent control effective? Is intermittent control physiological? J Physiol 589: 307-324, 2011.
43. Loram ID, Lakie M, Gawthrop PJ. Visual control of stable and unstable loads: what is the feedback delay and extent of linear time-invariant control? J Physiol 587: 1343-1365, 2009.
44. Malfait N, Gribble PL, Ostry DJ. Generalization of motor learning based on multiple field exposures and local adaptation. J Neurophysiol 93: 3327-3338, 2005.
45. Malfait N, Shiller DM, Ostry DJ. Transfer of motor learning across arm configurations. J Neurosci 22: 9656-9660, 2002.
46. Mattar AA, Ostry DJ. Neural averaging in motor learning. J Neurophysiol 97: 220-228, 2007.
47. Matthews PBC. The human stretch reflex and the motor cortex. Trends Neurosci 14: 87-91, 1991.
48. McIntyre J, Mussa-Ivaldi FA, Bizzi E. The control of stable postures in the multijoint arm. Exp Brain Res 110: 248-264, 1996.
49. Milner TE. Adaptation to destabilizing dynamics by means of muscle cocontraction. Exp Brain Res 143: 406-416, 2002.
50. Milner TE, Franklin DW. Characterization of multijoint finger stiffness: dependence on finger posture and force direction. IEEE Trans Biomed Eng 45: 1363-1375, 1998.
51. Morasso P. 'Brute force' vs 'gentle taps' in the control of unstable loads. J Physiol 589: 459-460, 2011.
52. Murray WM, Buchanan TS, Delp SL. The isometric functional capacity of muscles that cross the elbow. J Biomech 33: 943-952, 2000.
53. Murray WM, Delp SL, Buchanan TS. Variation of muscle moment arms with elbow and forearm position. J Biomech 28: 513-525, 1995.
54. Mussa-Ivaldi FA, Hogan N, Bizzi E. Neural, mechanical, and geometric factors subserving arm posture in humans. J Neurosci 5: 2732-2743, 1985.
55. Nozaki D, Kurtzer I, Scott SH. Limited transfer of learning between unimanual and bimanual skills within the same limb. Nat Neurosci 9: 1364-1366, 2006.
56. Osu R, Burdet E, Franklin DW, Milner TE, Kawato M. Different mechanisms involved in adaptation to stable and unstable dynamics. J Neurophysiol 90: 3255-3269, 2003.
57. Osu R, Franklin DW, Kato H, Gomi H, Domen K, Yoshioka T, Kawato M. Short- and long-term changes in joint co-contraction associated with motor learning as revealed from surface EMG. J Neurophysiol 88: 991-1004, 2002.
58. Osu R, Hirai S, Yoshioka T, Kawato M. Random presentation enables subjects to adapt to two opposing forces on the hand. Nat Neurosci 7: 111-112, 2004.
59. Perreault EJ, Chen K, Trumbower RD, Lewis G. Interactions with compliant loads alter stretch reflex gains but not intermuscular coordination. J Neurophysiol 99: 2101-2113, 2008.
60. Perreault EJ, Kirsch RF, Crago PE. Effects of voluntary force generation on the elastic components of endpoint stiffness. Exp Brain Res 141: 312-323, 2001.
61. Perreault EJ, Kirsch RF, Crago PE. Multijoint dynamics and postural stability of the human arm. Exp Brain Res 157: 507-517, 2004.
62. Pruszynski JA, Kurtzer I, Scott SH. Rapid motor responses are appropriately tuned to the metrics of a visuospatial task. J Neurophysiol 100: 224-238, 2008.
63. Pruszynski JA, Kurtzer IL, Scott SH. The long-latency reflex is composed of at least two functionally independent processes. J Neurophysiol 18: 449-453, 2011.
64. Rancourt D, Hogan N. Stability in force-production tasks. J Mot Behav 33: 193-204, 2001.
65. Selen LP, Beek PJ, van Dieen JH. Can co-activation reduce kinematic variability? A simulation study. Biol Cybern 93: 373-381, 2005.
66. Selen LP, Franklin DW, Wolpert DM. Impedance control reduces instability that arises from motor noise. J Neurosci 29: 12606-12616, 2009.
67. Shadmehr R, Brashers-Krug T. Functional stages in the formation of human long-term motor memory. J Neurosci 17: 409-419, 1997.
68. Shadmehr R, Moussavi ZM. Spatial generalization from learning dynamics of reaching movements. J Neurosci 20: 7807-7815, 2000.
69. Shadmehr R, Mussa-Ivaldi FA. Adaptive representation of dynamics during learning of a motor task. J Neurosci 14: 3208-3224, 1994.
70. Takahashi CD, Scheidt RA, Reinkensmeyer DJ. Impedance control and internal model formation when reaching in a randomly varying dynamical environment. J Neurophysiol 86: 1047-1051, 2001.
71. Tee KP, Burdet E, Chew CM, Milner TE. A model of force and impedance in human arm movements. Biol Cybern 90: 368-375, 2004.
72. Thoroughman KA, Shadmehr R. Learning of action through adaptive combination of motor primitives. Nature 407: 742-747, 2000.
73. Thoroughman KA, Taylor JA. Rapid reshaping of human motor generalization. J Neurosci 25: 8948-8953, 2005.
74. Trumbower RD, Krutky MA, Yang BS, Perreault EJ. Use of self-selected postures to regulate multi-joint stiffness during unconstrained tasks. PLos One 4: e5411, 2009.
75. Tsuji T, Morasso PG, Goto K, Ito K. Human hand impedance characteristics during maintained posture. Biol Cybern 72: 475-485, 1995.
76. Wolpert DM, Kawato M. Multiple paired forward and inverse models for motor control. Neural Netw 11: 1317-1329, 1998.
77. Wong J, Wilson ET, Malfait N, Gribble PL. The influence of visual perturbations on the neural control of limb stiffness. J Neurophysiol 101: 246-257, 2009a.
78. Wong J, Wilson ET, Malfait N, Gribble PL. Limb stiffness is modulated with spatial accuracy requirements during movement in the absence of destabilizing forces. J Neurophysiol 101: 1542-1549, 2009b.