Motor primitives-new data and future questions

Current Opinion in Neurobiology

Volumn 33, Issue , 2015, Pages 156-165

  Giszter, Simon F ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BOOTSTRAPPING; ETHOLOGY; FORCE FIELD MOTOR ACTIVITY; HUMAN; KINEMATICS; MOTOR ACTIVITY; MOTOR COORDINATION; MOTOR PERFORMANCE; MUSCLE FUNCTION; MUSCLE STRENGTH; NERVE CELL PLASTICITY; NONHUMAN; PHYSICAL ACTIVITY; PRIORITY JOURNAL; REVIEW; SPINAL MUSCLE SYNERGY; TASK PERFORMANCE; TEMPORALIS MUSCLE; ANIMAL; BIOLOGICAL MODEL; BIOMECHANICS; BRAIN; INNERVATION; MOVEMENT (PHYSIOLOGY); PHYSIOLOGY; PSYCHOMOTOR PERFORMANCE; SKELETAL MUSCLE;

ANIMALS; BIOMECHANICAL PHENOMENA; BRAIN; HUMANS; MODELS, BIOLOGICAL; MOVEMENT; MUSCLE, SKELETAL; PSYCHOMOTOR PERFORMANCE;

EID: 84928119407     PISSN: 09594388     EISSN: 18736882     Source Type: Journal    
DOI: 10.1016/j.conb.2015.04.004     Document Type: Review

References (76)

1. Hogan N. An organizing principle for a class of voluntary movements. J Neurosci 1984, 4:2745-2754.
2. Flash T., Hogan N. The coordination of arm movements: an experimentally confirmed mathematical model. J Neurosci 1985, 5:1688-1703.
3. Hogan N., Sternad D. Dynamic primitives of motor behavior. Biol Cybern 2012, 106:727-739.
4. Sternad D., Marino H., Charles S.K., Duarte M., Dipietro L., Hogan N. Transitions between discrete and rhythmic primitives in a unimanual task. Front Comput Neurosci 2013, 7:90.
5. Hogan N., Sternad D. Dynamic primitives in the control of locomotion. Front Comput Neurosci 2013, 7:71.
6. Bizzi E., Mussa-Ivaldi F.A., Giszter S. Computations underlying the execution of movement: a biological perspective. Science 1991, 253:287-291.
7. Giszter S.F., Mussa-Ivaldi F.A., Bizzi E. Convergent force fields organized in the frog's spinal cord. J Neurosci 1993, 13:467-491.
8. Mussa-Ivaldi F.A., Giszter S.F., Bizzi E. Linear combinations of primitives in vertebrate motor control. Proc Natl Acad Sci U S A 1994, 91:7534-7538.
9. Kargo W.J., Giszter S.F. Rapid correction of aimed movements by summation of force-field primitives. Journal of Neuroscience 2000, 20:409-426.
10. Hart C.B., Giszter S.F. Modular premotor drives and unit bursts as primitives for frog motor behaviors. J Neurosci 2004, 24:5269-5282.
11. Saltiel P., Wyler-Duda K., D'Avella A., Tresch M.C., Bizzi E. Muscle synergies encoded within the spinal cord: evidence from focal intraspinal NMDA iontophoresis in the frog. J Neurophysiol 2001, 85:605-619.
12. Hart C.B., Giszter S.F. A neural basis for motor primitives in the spinal cord. J Neurosci 2010, 30:1322-1336.
13. Flash T., Hochner B. Motor primitives in vertebrates and invertebrates. Curr Opin Neurobiol 2005, 15:660-666.
14. Schaal S., Schweighofer N. Computational motor control in humans and robots. Curr Opin Neurobiol 2005, 15:675-682.
15. Ijspeert A.J., Nakanishi J., Hoffmann H., Pastor P., Schaal S. Dynamical movement primitives: learning attractor models for motor behaviors. Neural Comput 2013, 25:328-373.
16. Polyakov F., Stark E., Drori R., Abeles M., Flash T. Parabolic movement primitives and cortical states: merging optimality with geometric invariance. Biol Cybern 2009, 100:159-184.
17. Abeles M., Diesmann M., Flash T., Geisel T., Herrmann M., Teicher M. Compositionality in neural control: an interdisciplinary study of scribbling movements in primates. Front Comput Neurosci 2013, 7:103.
18. Sosnik R., Hauptmann B., Karni A., Flash T. When practice leads to co-articulation: the evolution of geometrically defined movement primitives. Exp Brain Res 2004, 156:422-438.
19. Rohrer B., Fasoli S., Krebs H.I., Volpe B., Frontera W.R., Stein J., Hogan N. Submovements grow larger, fewer, and more blended during stroke recovery. Motor Control 2004, 8:472-483.
20. Zelman I., Titon M., Yekutieli Y., Hanassy S., Hochner B., Flash T. Kinematic decomposition and classification of octopus arm movements. Front Comput Neurosci 2013, 7:60.
21. Kargo W.J., Giszter S.F. Individual premotor drive pulses, not time-varying synergies, are the units of adjustment for limb trajectories constructed in spinal cord,. J Neurosci 2008, 28:2409-2425.
22. Kargo W.J., Ramakrishnan A., Hart C.B., Rome L.C., Giszter S.F. A simple experimentally based model using proprioceptive regulation of motor primitives captures adjusted trajectory formation in spinal frogs. J Neurophysiol 2010, 103:573-590.
23. Berniker M., Jarc A., Bizzi E., Tresch M.C. Simplified and effective motor control based on muscle synergies to exploit musculoskeletal dynamics. Proc Natl Acad Sci U S A 2009, 106:7601-7606.
24. Kuppuswamy N., Harris C.M. Do muscle synergies reduce the dimensionality of behavior?. Front Comput Neurosci 2014, 8:63.
25. Lafreniere-Roula M., McCrea D.A. Deletions of rhythmic motoneuron activity during fictive locomotion and scratch provide clues to the organization of the mammalian central pattern generator. J Neurophysiol 2005, 94:1120-1132.
26. Rybak I.A., Shevtsova N.A., Lafreniere-Roula M., McCrea D.A. Modelling spinal circuitry involved in locomotor pattern generation: insights from deletions during fictive locomotion. J Physiol 2006, 577:617-639.
27. Kiehn O. Development and functional organization of spinal locomotor circuits. Curr Opin Neurobiol 2011, 21:100-109.
28. Drew T., Kalaska J., Krouchev N. Muscle synergies during locomotion in the cat: a model for motor cortex control. J Physiol 2008, 586:1239-1245.
29. Krouchev N., Drew T. Motor cortical regulation of sparse synergies provides a framework for the flexible control of precision walking. Front Comput Neurosci 2013, 7:83.
30. Overduin S.A., d'Avella A., Roh J., Bizzi E. Modulation of muscle synergy recruitment in primate grasping. J Neurosci 2008, 28:880-892.
31. Dominici N., Ivanenko Y.P., Cappellini G., d'Avella A., Mondi V., Cicchese M., Fabiano A., Silei T., Di Paolo A., Giannini C., et al. Locomotor primitives in newborn babies and their development. Science 2011, 334:997-999.
32. d'Avella A., Lacquaniti F. Control of reaching movements by muscle synergy combinations. Front Comput Neurosci 2013, 7:42.
33. Lacquaniti F., Ivanenko Y.P., d'Avella A., Zelik K.E., Zago M. Evolutionary and developmental modules. Front Comput Neurosci 2013, 7:61.
34. Torres-Oviedo G., Ting L.H. Muscle synergies characterizing human postural responses. J Neurophysiol 2007, 98:2144-2156.
35. Torres-Oviedo G., Ting L.H. Subject-specific muscle synergies in human balance control are consistent across different biomechanical contexts. J Neurophysiol 2010, 103:3084-3098.
36. Cheung V.C., Piron L., Agostini M., Silvoni S., Turolla A., Bizzi E. Stability of muscle synergies for voluntary actions after cortical stroke in humans. Proc Natl Acad Sci U S A 2009, 106:19563-19568.
37. Cheung V.C., Turolla A., Agostini M., Silvoni S., Bennis C., Kasi P., Paganoni S., Bonato P., Bizzi E. Muscle synergy patterns as physiological markers of motor cortical damage. Proc Natl Acad Sci U S A 2012, 109:14652-14656.
38. Steele K.M., Tresch M.C., Perreault E.J. The number and choice of muscles impact the results of muscle synergy analyses. Front Comput Neurosci 2013, 7:105.
39. Steele K.M., Tresch M.C., Perreault E.J. Consequences of biomechanically constrained tasks in the design and interpretation of synergy analyses. J Neurophysiol 2015, 10.1152/jn.00769.2013.
40. Straka H., Simmers J. Xenopus laevis: an ideal experimental model for studying the developmental dynamics of neural network assembly and sensory-motor computations. Dev Neurobiol 2012, 72:649-663.
41. Straka H., Fritzsch B., Glover J.C. Connecting ears to eye muscles: evolution of a 'simple' reflex arc. Brain Behav Evol 2014, 83:162-175.
42. Levine A.J., Hinckley C.A., Hilde K.L., Driscoll S.P., Poon T.H., Montgomery J.M., Pfaff S.L. Identification of a cellular node for motor control pathways. Nat Neurosci 2014, 17:586-593.
43. Talpalar A.E., Bouvier J., Borgius L., Fortin G., Pierani A., Kiehn O. Dual-mode operation of neuronal networks involved in left-right alternation. Nature 2013, 500:85-88.
44. Schouenborg J. Action-based sensory encoding in spinal sensorimotor circuits. Brain Res Rev 2008, 57:111-117.
45. Azim E., Jiang J., Alstermark B., Jessell T.M. Skilled reaching relies on a V2a propriospinal internal copy circuit. Nature 2014, 508:357-363.
46. Azim E., Alstermark B. Skilled forelimb movements and internal copy motor circuits. Curr Opin Neurobiol 2015, 33C:16-24.
47. Hagglund M., Dougherty K.J., Borgius L., Itohara S., Iwasato T., Kiehn O. Optogenetic dissection reveals multiple rhythmogenic modules underlying locomotion. Proc Natl Acad Sci USA 2013, 110:11589-11594.
48. Yakovenko S., Krouchev N., Drew T. Sequential activation of motor cortical neurons contributes to intralimb coordination during reaching in the cat by modulating muscle synergies. J Neurophysiol 2011, 105:388-409.
49. Wolpert D.M., Ghahramani Z., Jordan M.I. Perceptual distortion contributes to the curvature of human reaching movements. Exp Brain Res 1994, 98:153-156.
50. Maoz U., Flash T. Spatial constant equi-affine speed and motion perception. J Neurophysiol 2014, 111:336-349.
51. Mussa-Ivaldi F.A., Giszter S.F. Vector field approximation: a computational paradigm for motor control and learning. Biol Cybern 1992, 67:491-500.
52. Mussa-Ivaldi F.A. From basis functions to basis fields: vector field approximation from sparse data. Biol Cybern 1992, 67:479-489.
53. Colgate J.E., Hogan N. Robust-control of dynamically interacting systems. International Journal of Control 1988, 48:65-88.
54. Slotine J.J., Lohmiller W. Modularity, evolution, and the binding problem: a view from stability theory. Neural Netw 2001, 14:137-145.
55. McIntyre J., Slotine J.J. Does the brain make waves to improve stability?. Brain Res Bull 2008, 75:717-722.
56. McKay J.L., Ting L.H. Optimization of muscle activity for task-level goals predicts complex changes in limb forces across biomechanical contexts. PLoS Comput Biol 2012, 8:e1002465.
57. Collins J.J. The redundant nature of locomotor optimization laws. J Biomech 1995, 28:251-267.
58. Valero-Cuevas F.J. A mathematical approach to the mechanical capabilities of limbs and fingers. Adv Exp Med Biol 2009, 629:619-633.
59. Kutch J.J., Valero-Cuevas F.J. Challenges and new approaches to proving the existence of muscle synergies of neural origin. PLoS Comput Biol 2012, 8:e1002434.
60. Racz K., Brown D., Valero-Cuevas F.J. An involuntary stereotypical grasp tendency pervades voluntary dynamic multifinger manipulation. J Neurophysiol 2012, 108:2896-2911.
61. Racz K., Valero-Cuevas F.J. Spatio-temporal analysis reveals active control of both task-relevant and task-irrelevant variables. Front Comput Neurosci 2013, 7:155.
62. Clark D.J., Ting L.H., Zajac F.E., Neptune R.R., Kautz S.A. Merging of healthy motor modules predicts reduced locomotor performance and muscle coordination complexity post-stroke. J Neurophysiol 2010, 103:844-857.
63. Fox E.J., Tester N.J., Kautz S.A., Howland D.R., Clark D.J., Garvan C., Behrman A.L. Modular control of varied locomotor tasks in children with incomplete spinal cord injuries. J Neurophysiol 2013, 110:1415-1425.
64. Drew T., Marigold D.S. Taking the next step: cortical contributions to the control of locomotion. Curr Opin Neurobiol 2015, 33C:25-33.
65. Tremolizzo L., Susani E., Lunetta C., Corbo M., Ferrarese C., Appollonio I. Primitive reflexes in amyotrophic lateral sclerosis: prevalence and correlates. J Neurol 2014, 261:1196-1202.
66. Desmurget M., Richard N., Harquel S., Baraduc P., Szathmari A., Mottolese C., Sirigu A. Neural representations of ethologically relevant hand/mouth synergies in the human precentral gyrus. Proc Natl Acad Sci U S A 2014, 111:5718-5722.
67. Overduin S.A., d'Avella A., Carmena J.M., Bizzi E. Microstimulation activates a handful of muscle synergies. Neuron 2012, 76:1071-1077.
68. Overduin S.A., d'Avella A., Carmena J.M., Bizzi E. Muscle synergies evoked by microstimulation are preferentially encoded during behavior. Front Comput Neurosci 2014, 8:20.
69. Graziano M.S., Taylor C.S., Moore T. Complex movements evoked by microstimulation of precentral cortex. Neuron 2002, 34:841-851.
70. Takei T., Seki K. Spinal premotor interneurons mediate dynamic and static motor commands for precision grip in monkeys. J Neurosci 2013, 33:8850-8860.
71. Takei T., Seki K. Synaptic and functional linkages between spinal premotor interneurons and hand-muscle activity during precision grip. Front Comput Neurosci 2013, 7:40.
72. Martin J.H. The corticospinal system: from development to motor control. Neuroscientist 2005, 11:161-173.
73. Todorov E. Efficient computation of optimal actions. Proc Natl Acad Sci U S A 2009, 106:11478-11483.
74. Berger D.J., Gentner R., Edmunds T., Pai D.K., d'Avella A. Differences in adaptation rates after virtual surgeries provide direct evidence for modularity. J Neurosci 2013, 33:12384-12394.
75. Berger D.J., d'Avella A. Effective force control by muscle synergies. Front Comput Neurosci 2014, 8:46.
76. Muceli S., Falla D., Farina D. Reorganization of muscle synergies during multidirectional reaching in the horizontal plane with experimental muscle pain. J Neurophysiol 2014, 111:1615-1630.