Interactions between limb and environmental mechanics influence stretch reflex sensitivity in the human arm

Journal of Neurophysiology

Volumn 103, Issue 1, 2010, Pages 429-440

  Krutky, Matthew A ^a,c   Ravichandran, Vengateswaran J ^a,c   Trumbower, Randy D ^c   Perreault, Eric J ^a,b,c  

^a Northwestern University   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c REHABILITATION INSTITUTE OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARM; ARTICLE; ENVIRONMENT; FEMALE; HUMAN; HUMAN EXPERIMENT; LIMB; MALE; MECHANICAL STRESS; MYOTATIC REFLEX; NORMAL HUMAN; PRIORITY JOURNAL; REFLEX; RIGIDITY;

ADULT; ARM; ELASTICITY; ELECTROMYOGRAPHY; ENVIRONMENT; FEMALE; HUMANS; MALE; MOTOR ACTIVITY; MUSCLE, SKELETAL; REFLEX, STRETCH; ROBOTICS; STOCHASTIC PROCESSES; TIME FACTORS;

EID: 74049117026     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00679.2009     Document Type: Article

References (58)

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. Bendat JS, Piersol AG. Random Data: Analysis and Measurement Procedures. New York: Wiley-Interscience, 2000.
3. 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.
4. Capaday C, Forget R, Fraser R, Lamarre Y. Evidence for a contribution of the motor cortex to the long-latency stretch reflex of the human thumb. J Physiol 440: 243-255, 1991.
5. Cheung VC, d'Avella A, Tresch MC, Bizzi E. Central and sensory contributions to the activation and organization of muscle synergies during natural motor behaviors. J Neurosci 25: 6419-6434, 2005.
6. Colgate JE, Hogan N. Robust control of dynamically interacting systems. Int J Control 48: 65-88, 1988.
7. Crago PE, Houk JC, Hasan Z. Regulatory actions of human stretch reflex. J Neurophysiol 39: 925-935, 1976.
8. d'Avella A, Portone A, Fernandez L, Lacquaniti F. Control of fast-reaching movements by muscle synergy combinations. J Neurosci 26: 7791-7810, 2006.
9. Delagi EF, Iazzetti J, Perotto A, Morrison D. Anatomic Guide for the Electromyographer. Springfield, IL: Thomas, 1980.
10. Dietz V, Discher M, Trippel M. Task-dependent modulation of short- and long-latency electromyographic responses in upper limb muscles. Electroencephalogr Clin Neurophysiol 93: 49-56, 1994.
11. Doemges F, Rack PMH. Changes in the stretch reflex of the human first dorsal interosseous muscle during different tasks. J Physiol 447: 563-573, 1992a.
12. Doemges F, Rack PMH. Task-dependent changes in the response of human wrist joints to mechanical disturbance. J Physiol 447: 575-585, 1992b.
13. Evarts EV, Fromm C. The pyramidal tract neuron as summing point in a closed-loop control system in the monkey. In: Cerebral Motor Control in Man: Long Loop Mechanisms, edited by Desmedt JE. New York: Karger AG, 1978, vol. 4, p. 56-69.
14. 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, 2007.
15. Franklin DW, Milner TE. Adaptive control of stiffness to stabilize hand position with large loads. Exp Brain Res 152: 211-220, 2003.
16. 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, 2003.
17. Gielen CCAM, Ramaekers L, van Zuylen EJ. Long-latency stretch reflexes as co-ordinated functional responses in man. J Physiol 407: 275-292, 1988.
18. 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.
19. Hammond PH. The influence of prior instruction to the subject on an apparently involuntary neuro-muscular response. J Physiol 132:17-18P, 1956.
20. Hogan N. The mechanics of multi-joint posture and movement control. Biol Cybern 52: 315-331, 1985.
21. Kearney RE, Stein RB, Parameswaran L. Identification of intrinsic and reflex contributions to human ankle stiffness dynamics. IEEE Trans Biomed Eng 44: 493-504, 1997.
22. Kimura T, Haggard P, Gomi H. Transcranial magnetic stimulation over sensorimotor cortex disrupts anticipatory reflex gain modulation for skilled action. J Neurosci 26: 9272-9281, 2006.
23. 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.
24. Kurtzer IL, Pruszynski JA, Scott SH. Long-latency responses during reaching account for the mechanical interaction between the shoulder and elbow joints. J Neurophysiol 102: 3004-3015, 2009.
25. Lacquaniti F, Carrozzo M, Borghese NA. Time-varying mechanical behavior of multijointed arm in man. J Neurophysiol 69: 1443-1463, 1993.
26. Lacquaniti F, Soechting JF. EMG responses to load perturbations of the upper limb: effect of dynamic coupling between shoulder and elbow motion. Exp Brain Res 61: 482-496, 1986.
27. 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.
28. Lewis GN, Perreault EJ, Mackinnon CD. The influence of perturbation duration and velocity on the long-latency response to stretch in the biceps muscle. Exp Brain Res 163: 361-369, 2005.
29. MacKay WA, Murphy JT. Cerebellar modulation of reflex gain. Prog Neurobiol 13: 361-417, 1979.
30. MacKinnon CD, Verrier MC, Tatton WG. Motor cortical potentials precede long-latency EMG activity evoked by imposed displacements of the human wrist. Exp Brain Res 131: 477-490, 2000.
31. Maluf KS, Barry BK, Riley ZA, Enoka RM. Reflex responsiveness of a human hand muscle when controlling isometric force and joint position. Clin Neurophysiol 118: 2063-2071, 2007.
32. Matthews PB. Observations on the automatic compensation of reflex gain on varying the pre-existing level of motor discharge in man. J Physiol 374: 73-90, 1986.
33. Matthews PBC. The human stretch reflex and the motor cortex. Trends Neurosci 14: 87-91, 1991.
34. McIntyre J, Mussa-Ivaldi FA, Bizzi E. The control of stable arm postures in the multi-joint arm. Exp Brain Res 110: 248-264, 1996.
35. Milner TE, Franklin DW, Imamizu H, Kawato M. Central representation of dynamics when manipulating handheld objects. J Neurophysiol 95: 893-901, 2006.
36. Mussa-Ivaldi FA, Hogan N, Bizzi E. Neural, mechanical, and geometric factors subserving arm posture in humans. J Neurosci 5: 2732-2743, 1985.
37. Nichols TR, Houk JC. Improvement in linearity and regulation of stiffness that results from actions of stretch reflex. J Neurophysiol 39: 119-142, 1976.
38. 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.
39. Overduin SA, d'Avella A, Roh J, Bizzi E. Modulation of muscle synergy recruitment in primate grasping. J Neurosci 28: 880-892, 2008.
40. 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.
41. Perreault EJ, Kirsch RF, Acosta AM. Multiple-input, multiple-output system identification for the characterization of limb stiffness dynamics. Biol Cybern 80: 327-337, 1999.
42. 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.
43. Perreault EJ, Kirsch RF, Crago PE. Multijoint dynamics and postural stability of the human arm. Exp Brain Res 157: 507-517, 2004.
44. Press W, Flannery, BP, Teukolsky, SA, Vetterling, WT. Numerical Recipes. New York: Cambridge Univ. Press, 1986.
45. Prochazka A. Sensorimotor gain control: a basic strategy of motor systems? Prog Neurobiol 33: 281-307, 1989.
46. Pruszynski JA, Kurtzer I, Lillicrap TP, Scott SH. Temporal evolution of "automatic gain-scaling." J Neurophysiol 102: 992-1003, 2009.
47. Rancourt D, Hogan N. Stability in force-production tasks. J Mot Behav 33: 193-204, 2001.
48. Rohmert W. Ermittung von Erholung-spausen fur statische arbeit des menschen. Int Angew Physiol 18: 123-164, 1960.
49. Shadmehr R, Mussa-Ivaldi FA. Adaptive representation of dynamics during learning of a motor task. J Neurosci 14: 3208-3224, 1994.
50. Shemmell JBH, An JH, Perreault EJ. The differential role of motor cortex in stretch reflex modulation induced by changes in environmental mechanics and verbal instruction. J Neurosci 29: 13255-13263, 2009.
51. Sinkjaer T, Toft E, Andreassen S, Hornemann BC. Muscle stiffness in human ankle dorsiflexors: intrinsic and reflex components. J Neurophysiol 60: 1110-1121, 1988.
52. Smeets JB, Erkelens CJ. Dependence of autogenic and heterogenic stretch reflexes on pre-load activity in the human arm. J Physiol 440: 455-465, 1991.
53. Strick PL. The influence of motor preparation on the response of cerebellar neurons to limb displacements. J Neurosci 3: 2007-2020, 1983.
54. Torres-Oviedo G, Macpherson JM, Ting LH. Muscle synergy organization is robust across a variety of postural perturbations. J Neurophysiol 96: 1530-1546, 2006.
55. Tresch MC, Cheung VC, d'Avella A Matrix factorization algorithms for the identification of muscle synergies: evaluation on simulated and experimental data sets. J Neurophysiol 95: 2199-2212, 2006.
56. Trumbower RD, Krutky MA, Yang B-S, Perreault EJ. Use of self-selected postures to regulate multi-joint stiffness during unconstrained tasks. PLoS ONE 4: e5411, 2009.
57. Van der Linde RQ, Lammertse P, Frederiksen E, Ruiter B. The Haptic-Master, a new high-performance haptic interface. In: Proceedings Europtics. Edinburgh, UK, 2002, p. 1-5.
58. Zhang L-Q, Rymer WZ. Simultaneous and nonlinear identification of mechanical and reflex properties of human elbow joint muscles. IEEE Transn Biomed Eng 44: 1192-1209, 1997.