The training schedule affects the stability, not the magnitude, of the interlimb transfer of learned dynamics

Journal of Neurophysiology

Volumn 110, Issue 4, 2013, Pages 984-998

  Joiner, Wilsaan M ^a,b   Brayanov, Jordan B ^a   Smith, Maurice A ^a  

^a HARVARD UNIVERSITY   (United States)

^b George Mason University   (United States)

Author keywords

Interlimb generalization; Motor adaptation; Reaching arm movements; Training schedule

Indexed keywords

ADAPTATION; ARM MOVEMENT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DYNAMICS; HUMAN; IMPEDANCE; INTERLIMB TRANSFER; LEARNING; LIMB MOVEMENT; MEASUREMENT; MOTOR PERFORMANCE; NORMAL HUMAN; PRIORITY JOURNAL; RIGIDITY; TRAINING; VELOCITY;

EID: 84881634281     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.01072.2012     Document Type: Article

References (85)

1. Anguera JA, Russell CA, Noll DC, Seidler RD. Neural correlates associated with intermanual transfer of sensorimotor adaptation. Brain Res 1185: 136-151, 2007.
2. Baraduc P, Wolpert DM. Adaptation to a visuomotor shift depends on the starting posture. J Neurophysiol 88: 973-981, 2002.
3. Berniker M, Kording K. Estimating the sources of motor errors for adaptation and generalization. Nat Neurosci 11: 1454-1461, 2008.
4. Berniker M, Kording K. Estimating the relevance of world disturbances to explain savings, interference and long-term motor adaptation effects. PLoS Comput Biol 7: e1002210, 2011.
5. Bock O, Thomas M, Grigorova V. The effect of rest breaks on human sensorimotor adaptation. Exp Brain Res 163: 258-260, 2005.
6. Brayanov JB, Press DZ, Smith MA. Motor memory is encoded as a gain-field combination of intrinsic and extrinsic action representations. J Neurosci 32: 14951-14965, 2012.
7. Choe CS, Welch RB. Variables affecting the intermanual transfer and decay of prism adaptation. J Exp Psychol 102: 1076-1084, 1974.
8. Cisek P, Crammond DJ, Kalaska JF. Neural activity in primary motor and dorsal premotor cortex in reaching tasks with the contralateral versus ipsilateral arm. J Neurophysiol 89: 922-942, 2003.
9. Cohen MM. Continuous versus terminal visual feedback in prism aftereffects. Percept Mot Skills 24: 1295-1302, 1967.
10. Cohen MM. Visual feedback, distribution of practice, and intermanual transfer of prism aftereffects. Percept Mot Skills 37: 599-609, 1973.
11. Craske B. Adaptation to prisms: change in internally registered eye-position. Br J Psychol 58: 329-335, 1967.
12. Cressman EK, Henriques DY. Sensory recalibration of hand position following visuomotor adaptation. J Neurophysiol 102: 3505-3518, 2009.
13. Cressman EK, Henriques DY. Reach adaptation and proprioceptive recalibration following exposure to misaligned sensory input. J Neurophysiol 103: 1888-1895, 2010.
14. Cressman EK, Henriques DY. Visuomotor adaptation and proprioceptive recalibration. J Mot Behav 44: 435-444, 2012.
15. Criscimagna-Hemminger SE, Donchin O, Gazzaniga MS, Shadmehr R. Learned dynamics of reaching movements generalize from dominant to nondominant arm. J Neurophysiol 89: 168-176, 2003.
16. Darainy M, Mattar AA, Ostry DJ. Effects of human arm impedance on dynamics learning and generalization. J Neurophysiol 101: 3158-3168, 2009.
17. Diedrichsen J, Hashambhoy Y, Rane T, Shadmehr R. Neural correlates of reach errors. J Neurosci 25: 9919-9931, 2005.
18. 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.
19. Donchin O, Gribova A, Steinberg O, Bergman H, Vaadia E. Primary motor cortex is involved in bimanual coordination. Nature 395: 274-278, 1998.
20. 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.
21. Gandolfo F, Mussa-Ivaldi FA, Bizzi E. Motor learning by field approximation. Proc Natl Acad Sci USA 93: 3843-3846, 1996.
22. Ghez C, Scheidt R, Heijink H. Different learned coordinate frames for planning trajectories and final positions in reaching. J Neurophysiol 98: 3614-3626, 2007.
23. Gonzalez Castro LN, Monsen CB, Smith MA. The binding of learning to action in motor adaptation. PLoS Comput Biol 7: e1002052, 2011a.
24. Gonzalez Castro LN, Wu H, Smith M. Adaptation to dynamic environments displays local generalization for voluntary reaching movements. Conf Proc IEEE Eng Med Biol Soc 2011: 4050-4052, 2011b.
25. Goodbody SJ, Wolpert DM. Temporal and amplitude generalization in motor learning. J Neurophysiol 79: 1825-1838, 1998.
26. Hamilton CR. Intermanual transfer of adaptation to prisms. Am J Psychol 77: 457-462, 1964.
27. Harris CS. Adaptation to displaced vision: visual, motor, or proprioceptive change? Science 140: 812-813, 1963.
28. Huang VS, Shadmehr R. Persistence of motor memories reflects statistics of the learning event. J Neurophysiol 102: 931-940, 2009.
29. Joiner WM, Ajayi O, Sing GC, Smith MA. Linear hypergeneralization of learned dynamics across movement speeds reveals anisotropic, gain-encoding primitives for motor adaptation. J Neurophysiol 105: 45-59, 2011.
30. Joiner WM, Smith MA. Long-term retention explained by a model of short-term learning in the adaptive control of reaching. J Neurophysiol 100: 2948-2955, 2008.
31. Kagerer FA, Contreras-Vidal JL, Stelmach GE. Adaptation to gradual as compared with sudden visuo-motor distortions. Exp Brain Res 115: 557-561, 1997.
32. Kitazawa S, Kimura T, Uka T. Prism adaptation of reaching movements: specificity for the velocity of reaching. J Neurosci 17: 1481-1492, 1997.
33. Kluzik J, Diedrichsen J, Shadmehr R, Bastian AJ. Reach adaptation: what determines whether we learn an internal model of the tool or adapt the model of our arm? J Neurophysiol 100: 1455-1464, 2008.
34. Kojima Y, Iwamoto Y, Yoshida K. Memory of learning facilitates saccadic adaptation in the monkey. J Neurosci 24: 7531-7539, 2004.
35. Krakauer JW, Ghilardi MF, Ghez C. Independent learning of internal models for kinematic and dynamic control of reaching. Nat Neurosci 2: 1026-1031, 1999.
36. Krakauer JW, Pine ZM, Ghilardi MF, Ghez C. Learning of visuomotor transformations for vectorial planning of reaching trajectories. J Neurosci 20: 8916-8924, 2000.
37. Malfait N, Gribble PL, Ostry DJ. Generalization of motor learning based on multiple field exposures and local adaptation. J Neurophysiol 93: 3327-3338, 2005.
38. Malfait N, Ostry DJ. Is interlimb transfer of force-field adaptation a cognitive response to the sudden introduction of load? J Neurosci 24: 8084-8089, 2004.
39. Malfait N, Shiller DM, Ostry DJ. Transfer of motor learning across arm configurations. J Neurosci 22: 9656-9660, 2002.
40. Mattar AA, Ostry DJ. Generalization of dynamics learning across changes in movement amplitude. J Neurophysiol 104: 426-438, 2010.
41. Michel C, Pisella L, Prablanc C, Rode G, Rossetti Y. Enhancing visuomotor adaptation by reducing error signals: single-step (aware) versus multiplestep (unaware) exposure to wedge prisms. J Cogn Neurosci 19: 341-50, 2007.
42. Milner TE, Franklin DW. Impedance control and internal model use during the initial stage of adaptation to novel dynamics in humans. J Physiol 567: 651-664, 2005.
43. Nezafat R, Shadmehr R, Holcomb HH. Long-term adaptation to dynamics of reaching movements: a PET study. Exp Brain Res 140: 66-76, 2001.
44. Noto CT, Watanabe S, Fuchs AF. Characteristics of simian adaptation fields produced by behavioral changes in saccade size and direction. J Neurophysiol 81: 2798-2813, 1999.
45. Parlow SE, Kinsbourne M. Asymmetrical transfer of training between hands: implications for interhemispheric communication in normal brain. Brain Cogn 11: 98-113, 1989.
46. Rabe K, Livne O, Gizewski ER, Aurich V, Beck A, Timmann D, Donchin O. Adaptation to visuomotor rotation and force field perturbation is correlated to different brain areas in patients with cerebellar degeneration. J Neurophysiol 101: 1961-1971, 2009.
47. Raghavan P, Krakauer JW, Gordon AM. Impaired anticipatory control of fingertip forces in patients with a pure motor or sensorimotor lacunar syndrome. Brain 129: 1415-1425, 2006.
48. Redding GM, Wallace B. Strategic calibration and spatial alignment: a model from prism adaptation. J Mot Behav 34: 126-138, 2002.
49. Redding GM, Wallace B. Intermanual transfer of prism adaptation. J Mot Behav 40: 246-262, 2008.
50. Redding GM, Wallace B. Asymmetric visual prism adaptation and intermanual transfer. J Mot Behav 41: 83-94, 2009.
51. Redding GM, Wallace B. Prism adaptation in left-handers. Atten Percept Psychophys 73: 1871-1885, 2011.
52. Sainburg RL, Wang J. Interlimb transfer of visuomotor rotations: independence of direction and final position information. Exp Brain Res 145: 437-447, 2002.
53. Savion-Lemieux T, Penhune VB. The effects of practice and delay on motor skill learning and retention. Exp Brain Res 161: 423-431, 2005.
54. Scheidt RA, Dingwell JB, Mussa-Ivaldi FA. Learning to move amid uncertainty. J Neurophysiol 86: 971-985, 2001.
55. Scheidt RA, Ghez C. Separate adaptive mechanisms for controlling trajectory and final position in reaching. J Neurophysiol 98: 3600-3613, 2007.
56. Scheidt RA, Reinkensmeyer DJ, Conditt MA, Rymer WZ, Mussa-Ivaldi FA. Persistence of motor adaptation during constrained, multi-joint, arm movements. J Neurophysiol 84: 853-862, 2000.
57. Shadmehr R. Generalization as a behavioral window to the neural mechanisms of learning internal models. Hum Mov Sci 23: 543-568, 2004.
58. Shadmehr R, Mussa-Ivaldi FA. Adaptive representation of dynamics during learning of a motor task. J Neurosci 14: 3208-3224, 1994.
59. Simani MC, McGuire LM, Sabes PN. Visual-shift adaptation is composed of separable sensory and task-dependent effects. J Neurophysiol 98: 2827-2841, 2007.
60. Sing GC, Joiner WM, Nanayakkara T, Brayanov JB, Smith MA. Primitives for motor adaptation reflect correlated neural tuning to position and velocity. Neuron 64: 575-589, 2009.
61. Sing GC, Orozco SP, Smith MA. Limb motion dictates how motor learning arises from arbitrary environmental dynamics. J Neurophysiol 109: 2466-2482, 2013.
62. Sing GC, Smith MA. Reduction in learning rates associated with anterograde interference results from interactions between different timescales in motor adaptation. PLoS Comput Biol 6: e1000893, 2010.
63. Smith MA, Brandt J, Shadmehr R. Motor disorder in Huntington's disease begins as a dysfunction in error feedback control. Nature 403: 544-549, 2000.
64. Smith MA, Ghazizadeh A, Shadmehr R. Interacting adaptive processes with different timescales underlie short-term motor learning. PLoS Biol 4: 1035-1043, 2006.
65. Smith MA, Shadmehr R. Intact ability to learn internal models of arm dynamics in Huntington's disease but not cerebellar degeneration. J Neurophysiol 93: 2809-2821, 2005.
66. Steinberg O, Donchin O, Gribova A, Cardosa de Oliveira S, Bergman H, Vaadia E. Neuronal populations in primary motor cortex encode bimanual arm movements. Eur J Neurosci 15: 1371-1380, 2002.
67. 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.
68. Tanaka H, Sejnowski TJ, Krakauer JW. Adaptation to visuomotor rotation through interaction between posterior parietal and motor cortical areas. J Neurophysiol 102: 2921-2932, 2009.
69. Taub E, Goldberg LA. Prism adaptation: control of intermanual transfer by distribution of practice. Science 180: 755-757, 1973.
70. Taylor JA, Wojaczynski GJ, Ivry RB. Trial-by-trial analysis of intermanual transfer during visuomotor adaptation. J Neurophysiol 106: 3157-3172, 2011.
71. Tuan KM, Jones R. Adaptation to the prismatic effects of refractive lenses. Vision Res 37: 1851-1857, 1997.
72. Uhlarik JJ, Canon LK. Influence of concurrent and terminal exposure conditions on the nature of perceptual adaptation. J Exp Psychol 91: 233-239, 1971.
73. Wagner MJ, Smith MA. Shared internal models for feedforward and feedback control. J Neurosci 28: 10663-10673, 2008.
74. Wang J, Joshi M, Lei Y. The extent of interlimb transfer following adaptation to a novel visuomotor condition does not depend on awareness of the condition. J Neurophysiol 106: 259-264, 2011a
75. Wang J, Przybyla A, Wuebbenhorst K, Haaland KY, Sainburg RL. Aging reduces asymmetries in interlimb transfer of visuomotor adaptation. Exp Brain Res 210: 283-290, 2011b.
76. Wang J, Sainburg RL. Mechanisms underlying interlimb transfer of visuomotor rotations. Exp Brain Res 149: 520-526, 2003.
77. Wang J, Sainburg RL. Interlimb transfer of novel inertial dynamics is asymmetrical. J Neurophysiol 92: 349-360, 2004a.
78. Wang J, Sainburg RL. Limitations in interlimb transfer of visuomotor rotations. Exp Brain Res 155: 1-8, 2004b.
79. Wang J, Sainburg RL. The symmetry of interlimb transfer depends on workspace locations. Exp Brain Res 170: 464-471, 2006a.
80. Wang J, Sainburg RL. Interlimb transfer of visuomotor rotations depends on handedness. Exp Brain Res 175: 223-230, 2006b.
81. Wong AL, Shelhamer M. Saccade adaptation improves in response to a gradually introduced stimulus perturbation. Neurosci Lett 500: 207-211, 2011.
82. Wu HG, Smith MA. The generalization of visuomotor learning to untrained movements and movement sequences based on movement vector and goal location remapping. J Neurosci 33: 10772-10789, 2013.
83. Yin PB, Kitazawa S. Long-lasting aftereffects of prism adaptation in the monkey. Exp Brain Res 141: 250-253, 2001.
84. Yokoi A, Hirashima M, Nozaki D. Gain field encoding of the kinematics of both arms in the internal model enables flexible bimanual action. J Neurosci 31: 17058-17068, 2011.
85. Zarahn E, Weston GD, Liang J, Mazzoni P, Krakauer JW. Explaining savings for visuomotor adaptation: linear time-invariant state-space models are not sufficient. J Neurophysiol 100: 2537-2548, 2008.