Central and sensory contributions to the activation and organization of muscle synergies during natural motor behaviors

Journal of Neuroscience

Volumn 25, Issue 27, 2005, Pages 6419-6434

  Cheung, Vincent C K ^a,b   D'Avella, Andrea ^c   Tresch, Matthew C ^d   Bizzi, Emilio ^b,e  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^d REHABILITATION INSTITUTE OF CHICAGO   (United States)

^e EUROPEAN BRAIN RESEARCH INSTITUTE   (Italy)

Author keywords

Afferent; Central pattern generators; Deafferentation; Feedback; Frog; Jumping; Locomotion; Non negative matrix factorization; Swimming

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; DEAFFERENTATION; ELECTROMYOGRAM; FEEDBACK SYSTEM; FROG; JUMPING; LEG MUSCLE; LOCOMOTION; MOTOR COORDINATION; NONHUMAN; PRIORITY JOURNAL; SENSORY SYSTEM; SWIMMING;

AFFERENT PATHWAYS; ANIMALS; ELECTRODES, IMPLANTED; ELECTROMYOGRAPHY; FEEDBACK; HINDLIMB; MODELS, NEUROLOGICAL; MOTOR ACTIVITY; MUSCULOSKELETAL EQUILIBRIUM; NERVE NET; PSYCHOMOTOR PERFORMANCE; RANA CATESBEIANA; RHIZOTOMY; SPINAL CORD; SPINAL NERVE ROOTS; SWIMMING;

EID: 21844435726     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4904-04.2005     Document Type: Article

References (63)

1. Bates DM, Watts DG (1988) Nonlinear regression analysis and its applications. New York: Wiley.
2. Bell AJ, Sejnowski TJ (1995) An information-maximisation approach to blind source separation and blind deconvolution. Neural Comput 7:1129-1159.
3. Bernstein N (1967) The co-ordination and regulation of movements. Oxford: Pergamon.
4. Bizzi E, Mussa-Ivaldi FA, Giszter S (1991) Computations underlying the execution of movement: a biological perspective. Science 253:287-291.
5. Brown TG (1911) The intrinsic factors in the act of progression in the mammal. Proc R Soc Lond B Biol Sci 84:308-319.
6. Browne MW (2000) Cross-validation methods. J Math Psychol 44:108-132.
7. Burke RE (1999) The use of state-dependent modulation of spinal reflexes as a tool to investigate the organization of spinal interneurons. Exp Brain Res 128:263-277.
8. Clarac F (1991) How do sensory and motor signals interact during locomotion? In: Motor control: concepts and issues (Humphrey DR, Freund H-J, eds), pp 199-221. New York: Wiley.
9. d'Avella A, Bizzi E (2005) Shared and specific muscle synergies in natural motor behaviors. Proc Natl Acad Sci USA 102:3076-3081.
10. d'Avella A, Saltiel P, Bizzi E (2003) Combinations of muscle synergies in the construction of a natural motor behavior. Nat Neurosci 6:300-308.
11. Delcomyn F (1980) Neural basis of rhythmic behavior in animals. Science 210:492-498.
12. Ecker A (1971) The anatomy of the frog (Haslam G, translator). Amsterdam: Asher.
13. Forssberg H (1979) Stumbling corrective reaction: a phase-dependent compensatory reaction during locomotion. J Neurophysiol 42:936-953.
14. Giuliani CA, Smith JL (1987) Stepping behaviors in chronic spinal cats with one hindlimb deafferented. J Neurosci 7:2537-2546.
15. Goldberger ME (1988) Partial and complete deafferentation of cat hindlimb: the contribution of behavioral substitution to recovery of motor function. Exp Brain Res 73:343-353.
16. Golub GH, Van Loan CF (1983) Matrix computations. Baltimore: Johns Hopkins UP.
17. González IC (2003) Linear control model of the spinal processing of descending neural signals. Masters degree thesis, Massachusetts Institute of Technology.
18. Gribble PL, Ostry DJ (1999) Compensation for interaction torques during single- and multijoint limb movement. J Neurophysiol 82:2310-2326.
19. Grillner S (1975) Locomotion in vertebrates: central mechanisms and reflex interaction. Physiol Rev 55:247-304.
20. Grillner S (1981) Control of locomotion in bipeds, tetrapods, and fish. In: Handbook of physiology, Sec 1 (Brooks VB, ed), pp 1179-1236. Bethesda, MD: American Physiological Society.
21. Grillner S (1985) Neurobiological bases of rhythmic motor acts in vertebrates. Science 228:143-149.
22. Grillner S, Zangger P (1984) The effect of dorsal root transection on the efferent motor pattern in the cat's hindlimb during locomotion. Acta Physiol Scand 120:393-405.
23. Hart CB, Giszter SF (2004) Modular premotor drives and unit bursts as primitives for frog motor behaviors. J Neurosci 24:5269-5282.
24. Hays WL (1994) Statistics. Belmont, CA: Wardsworth.
25. Hiebert GW, Pearson KG (1999) Contributions of sensory feedback to the generation of extensor activity during walking in the decerebrate cat. J Neurophysiol 81:758-770.
26. Hyvärinen A, Oja E (2000) Independent component analysis: algorithms and applications. Neural Netw 13:411-430.
27. Jing J, Cropper EC, Hurwitz I, Weiss KR (2004) The construction of movement with behavior-specific and behavior-independent modules. J Neurosci 24:6315-6325.
28. Kargo WJ, Giszter SF (2000a) Rapid correction of aimed movements by summation of force-field primitive. J Neurosci 20:409-426.
29. Kargo WJ, Giszter SF (2000b) Afferent roles in hindlimb wipe-reflex trajectories: free-limb kinematics and molor patterns. J Neurophysiol 83:1480-1501.
30. Kargo WJ, Rome LC (2002) Functional morphology of proximal hindlimb muscles in the frog Rana pipiens. J Exp Biol 205:1987-2004.
31. Koshland GF, Smith JL (1989) Mutable and immutable features of paw-shake responses after hindlimb deafferentation in the cat. J Neurophysiol 62:162-173.
32. Lee DD, Seung HS (1999) Learning the parts of objects by non-negative matrix factorization. Nature 401:788-791.
33. Lee DD, Seung HS (2001) Algorithms for non-negative matrix factorization. In: Advances in neural information processing systems, Vol 13 (Leen TK, Dietterich TG, Tresp V, ed), pp 556-562. Cambridge, MA: MIT.
34. Loeb GE (1993) The distal hindlimb musculature of the cat: interanimal variability of locomotor activity and cutaneous reflexes. Exp Brain Res 96:125-140.
35. Loeb EP, Giszter SF, Borghesani P, Bizzi E (1993) Effects of dorsal root cut on the forces evoked by spinal microstimulation in the spinalized frog. Somatosens Mot Res 10:81-95.
36. Mai MT, Lieber RL (1990) A model of semitendinosus muscle sarcomere length, knee and hip joint interaction in the frog hindlimb. J Biomech 23:271-279.
37. Marder E, Bucher D (2001) Central pattern generators and the control of rhythmic movements. Curr Biol 11:R986-R996.
38. McCrea DA (2001) Spinal circuitry of sensorimotor control of locomotion. J Physiol (Lond) 533.1:41-50.
39. Nauwelaerts S, Aerts P (2002) Two distinct gait types in swimming frogs. J Zool 258:183-188.
40. Olson JM, Marsh RL (1998) Activation patterns and length changes in hindlimb muscles of the bullfrog Rana catesbeiana during jumping. J Exp Biol 201:2763-2777.
41. Pearson KG (2000) Neural adaptation in the generation of rhythmic behavior. Annu Rev Physiol 62:723-753.
42. Pearson KG (2004) Generating the walking gait: role of sensory feedback. Prog Brain Res 143:123-129.
43. Pearson KG, Collins DF (1993) Reversal of the influence of group Ib afferents from plantaris on activity in medial gastrocnemius muscle during locomotor activity. J Neurophysiol 70:1009-1017.
44. Perret C, Cabelguen J-M (1980) Main characteristics of the hindlimb locomotor cycle in the decorticate cat with special reference to bifunctional muscles. Brain Res 187:333-352.
45. Pratt CA, Buford JA, Smith JL (1996) Adaptive control for backward quadrupedal walking. V. Mutable activation of bifunctional thigh muscles. J Neurophysiol 75:832-842.
46. Prochazka A (1996) Proprioceptive feedback and movement regulation. In: Handbook of physiology, Sec 12 (Rowell LB, Shepherd JT, eds), pp 89-127. New York: Oxford UP.
47. Raasch CC, Zajac FE (1999) Locomotor strategy for pedaling: muscle groups and biomechanical functions. J Neurophysiol 82:515-525.
48. Roberts TJ, Marsh RL (2003) Probing the limits to muscle-powered accelerations: lessons from jumping bullfrogs. J Exp Biol 206:2567-2580.
49. Rossignol S (1996) Neural control of stereotypic limb movements. In: Handbook of physiology, Sec 12 (Rowell LB, Shepherd JT, eds), pp 173-216. New York: Oxford UP.
50. Saltiel P, Wyler-Duda K, d'Avella A, Tresch MC, Bizzi E (2001) Muscle synergies encoded within the spinal cord: evidence from focal intraspinal NMDA iontophoresis in the frog. J Neurophysiol 85:605-619.
51. Schouenborg J (2002) Modular organisation and spinal somatosensory imprinting. Brain Res Brain Res Rev 40:80-91.
52. Smith JL, Hoy MG, Koshland GF, Phillips DM, Zernicke RF (1985) Intralimb coordination of the paw-shake response: a novel mixed synergy. J Neurophysiol 54:1271-1281.
53. Soffe SR (1993) Two distinct rhythmic motor patterns are driven by common premotor and motor neurons in a simple vertebrate spinal cord. J Neurosci 13:4456-4469.
54. Stein PSG (2005) Neuronal control of turtle hindlimb motor rhythms. J Comp Physiol [A] 191:213-229.
55. Stein PSG, Smith JL (1997) Neural and biomechanical control strategies for different forms of vertebrate hindlimb motor tasks. In: Neurons, networks, and motor behavior (Stein PSG, Grillner S, Selverston AI, Stuart DG, eds), pp 61-73. Cambridge, MA: MIT.
56. Székely G, Czéh G, Vörös G (1969) The activity pattern of limb muscles in freely moving normal and deafferented newts. Exp Brain Res 9:53-62.
57. Ting LH, Macpherson JM (2005) A limited set of muscle synergies for force control during a postural task. J Neurophysiol 93:609-613.
58. Ting LH, Kautz SA, Brown DA, Zajac FE (1999) Phase reversal of biomechanical functions and muscle activity in backward pedaling. J Neurophysiol 81:544-551.
59. Ting LH, Kautz SA, Brown DA, Zajac FE (2000) Contralateral movement and extensor force generation alter flexion phase muscle coordination in pedaling. J Neurophysiol 83:3351-3365.
60. Tresch MC, Saltiel P, Bizzi E (1999) The construction of movement by the spinal cord. Nat Neurosci 2:162-167.
61. Tresch MC, Saltiel P, d'Avella A, Bizzi E (2002) Coordination and localization in spinal motor system. Brain Res Brain Res Rev 40:66-79.
62. Whelan PJ (1996) Control of locomotion in the decerebrate cat. Prog Neurobiol 49:481-515.
63. Zernicke RF, Smith JL (1996) Biomechanical insights into neural control of movement. In: Handbook of physiology, Sec 12 (Rowell LB, Shepherd JT, eds), pp 293-330. New York: Oxford UP.