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Applied Bionics and Biomechanics
Volume 2018, Article ID 3615368, 15 pages
https://doi.org/10.1155/2018/3615368
Review Article

A Systematic Review on Muscle Synergies: From Building Blocks of Motor Behavior to a Neurorehabilitation Tool

1Department of System Engineering, George W. Donaghey College of Engineering and Information Technology, University of Arkansas at Little Rock, Little Rock, AR 72204, USA
2Department of Engineering Technology, George W. Donaghey College of Engineering and Information Technology, University of Arkansas at Little Rock, Little Rock, AR 72204, USA
3School of Counseling, Human Performance and Rehabilitation, University of Arkansas at Little Rock, Little Rock, AR 72204, USA
4Department of Biochemistry and Molecular Biology, College of Medicine, University of Florida, Gainesville, FL 32610, USA

Correspondence should be addressed to Kamran Iqbal; ude.rlau@labqixk

Received 22 November 2017; Accepted 29 January 2018; Published 22 April 2018

Academic Editor: Panagiotis K. Artemiadis

Copyright © 2018 Rajat Emanuel Singh et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. N. Bernstein, The Co-Ordination and Regulation of Movements, Pergamon Press, Oxford, NY, USA, 1967.
  2. C. S. Sherrington, “Notes on the arrangement of some motor fibres in the lumbo-sacral plexus,” The Journal of Physiology, vol. 13, no. 6, pp. 621–772, 1892. View at Publisher · View at Google Scholar · View at Scopus
  3. W. J. W. Sharrard, “The segmental innervation of the lower limb muscles in man: Arris and Gale lecture delivered at the Royal College of Surgeons of England,” Annals of The Royal College of Surgeons, vol. 35, no. 2, pp. 106–122, 1964. View at Google Scholar
  4. D. Ferrier and G. F. Yeo, “The functional relations of the motor roots of the brachial and lumbo-sacral plexuses,” Proceedings of the Royal Society of London, vol. 32, no. 212-215, pp. 12–20, 1881. View at Publisher · View at Google Scholar
  5. S. A. Overduin, A. d’ Avella, J. M. Carmena, and E. Bizzi, “Microstimulation activates a handful of muscle synergies,” Neuron, vol. 76, no. 6, pp. 1071–1077, 2012. View at Publisher · View at Google Scholar · View at Scopus
  6. A. d’Avella, P. Saltiel, and E. Bizzi, “Combinations of muscle synergies in the construction of a natural motor behavior,” Nature Neuroscience, vol. 6, no. 3, pp. 300–308, 2003. View at Publisher · View at Google Scholar · View at Scopus
  7. A. d’Avella and E. Bizzi, “Shared and specific muscle synergies in natural motor behaviors,” Proceedings of the National Academy of Sciences, vol. 102, no. 8, pp. 3076–3081, 2005. View at Publisher · View at Google Scholar · View at Scopus
  8. M. M. Nazifi, H. U. Yoon, K. Beschorner, and P. Hur, “Shared and task-specific muscle synergies during normal walking and slipping,” Frontiers in Human Neuroscience, vol. 11, p. 40, 2017. View at Publisher · View at Google Scholar · View at Scopus
  9. B. Maton and S. Bouisset, “The distribution of activity among the muscles of a single group during isometric contraction,” European Journal of Applied Physiology and Occupational Physiology, vol. 37, no. 2, pp. 101–109, 1977. View at Publisher · View at Google Scholar · View at Scopus
  10. S. F. Giszter, F. A. Mussa-Ivaldi, and E. Bizzi, “Convergent force fields organized in the frog’s spinal cord,” Journal of Neuroscience, vol. 13, no. 2, pp. 467–491, 1993. View at Google Scholar
  11. E. Bizzi, F. Mussa-Ivaldi, and S. Giszter, “Computations underlying the execution of movement: a biological perspective,” Science, vol. 253, no. 5017, pp. 287–291, 1991. View at Publisher · View at Google Scholar
  12. S. A. Chvatal and L. H. Ting, “Voluntary and reactive recruitment of locomotor muscle synergies during perturbed walking,” The Journal of Neuroscience, vol. 32, no. 35, pp. 12237–12250, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. Y. P. Ivanenko, “Temporal components of the motor patterns expressed by the human spinal cord reflect foot kinematics,” Journal of Neurophysiology, vol. 90, no. 5, pp. 3555–3565, 2003. View at Publisher · View at Google Scholar · View at Scopus
  14. F. Mussa-Ivaldi, “Nonlinear force fields: a distributed system of control primitives for representing and learning movements,” in Proceedings 1997 IEEE international symposium on computational intelligence in robotics and automation CIRA97. 'Towards New Computational Principles for Robotics and Automation', Monterey, CA, USA, 1997. View at Publisher · View at Google Scholar
  15. S. H. Scott, L. E. Sergio, and J. F. Kalaska, “Reaching movements with similar hand paths but different arm orientations. II. Activity of individual cells in dorsal premotor cortex and parietal area 5,” Journal of Neurophysiology, vol. 78, no. 5, pp. 2413–2426, 1997. View at Publisher · View at Google Scholar
  16. F. A. Mussa-Ivaldi, “Motor primitives, force-fields and the equilibrium point theory,” From Basic Motor Control to Functional Recovery, N. Gantchev and G. N. Gantchev, Eds., Academic Publishing House, Sofia, Bulgaria, 1999. View at Google Scholar
  17. E. Bizzi and V. C. K. Cheung, “The neural origin of muscle synergies,” Frontiers in Computational Neuroscience, vol. 7, p. 51, 2013. View at Publisher · View at Google Scholar · View at Scopus
  18. F. Gandolfo, F. A. Mussa-Ivaldi, and E. Bizzi, “Motor learning by field approximation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 9, pp. 3843–3846, 1996. View at Publisher · View at Google Scholar · View at Scopus
  19. R. Shadmehr and F. A. Mussa-Ivaldi, “Adaptive representation of dynamics during learning of a motor task,” Journal of Neuroscience, vol. 14, no. 5, pp. 3208–3224, 1994. View at Google Scholar
  20. E. J. Huesler, M. A. Maier, and M. C. Hepp-Reymond, “EMG activation patterns during force production in precision grip. III. Synchronisation of single motor units,” Experimental Brain Research, vol. 134, no. 4, pp. 441–455, 2000. View at Publisher · View at Google Scholar · View at Scopus
  21. L. H. Ting and J. L. Mckay, “Neuromechanics of muscle synergies for posture and movement,” Current Opinion in Neurobiology, vol. 17, no. 6, pp. 622–628, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. R. A. Conwit, D. Stashuk, B. Tracy, M. Mchugh, W. F. Brown, and E. J. Metter, “The relationship of motor unit size, firing rate and force,” Clinical Neurophysiology, vol. 110, no. 7, pp. 1270–1275, 1999. View at Publisher · View at Google Scholar · View at Scopus
  23. J. L. McKay and L. H. Ting, “Functional muscle synergies constrain force production during postural tasks,” Journal of Biomechanics, vol. 41, no. 2, pp. 299–306, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. W. J. Kargo and S. F. Giszter, “Individual premotor drive pulses, not time-varying synergies, are the units of adjustment for limb trajectories constructed in spinal cord,” The Journal of Neuroscience, vol. 28, no. 10, pp. 2409–2425, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. C. B. Hart and S. F. Giszter, “Modular premotor drives and unit bursts as primitives for frog motor behaviors,” Journal of Neuroscience, vol. 24, no. 22, pp. 5269–5282, 2004. View at Publisher · View at Google Scholar · View at Scopus
  26. I. V. Grinyagin, “Kinematic and dynamic synergies of human precision-grip movements,” Journal of Neurophysiology, vol. 94, no. 4, pp. 2284–2294, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. T. Flash and B. Hochner, “Motor primitives in vertebrates and invertebrates,” Current Opinion in Neurobiology, vol. 15, no. 6, pp. 660–666, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. M. Tagliabue, A. L. Ciancio, T. Brochier, S. Eskiizmirliler, and M. A. Maier, “Differences between kinematic synergies and muscle synergies during two-digit grasping,” Frontiers in Human Neuroscience, vol. 9, p. 165, 2015. View at Publisher · View at Google Scholar · View at Scopus
  29. I. Wishaw, “Arm and hand movement: current knowledge and future perspective,” Frontiers in Neurology, vol. 6, 2015. View at Publisher · View at Google Scholar · View at Scopus
  30. F. A. Mussa-Ivaldi and S. A. Solla, “Neural primitives for motion control,” IEEE Journal of Oceanic Engineering, vol. 29, no. 3, pp. 640–650, 2004. View at Publisher · View at Google Scholar · View at Scopus
  31. F. Oscari, C. Finetto, S. A. Kautz, and G. Rosati, “Changes in muscle coordination patterns induced by exposure to a viscous force field,” Journal of Neuroengineering and Rehabilitation, vol. 13, no. 1, p. 58, 2016. View at Publisher · View at Google Scholar · View at Scopus
  32. P. Saltiel, K. Wyler-Duda, A. D'Avella, M. C. Tresch, and E. Bizzi, “Muscle synergies encoded within the spinal cord: evidence from focal intraspinal NMDA iontophoresis in the frog,” Journal of Neurophysiology, vol. 85, no. 2, pp. 605–619, 2001. View at Publisher · View at Google Scholar
  33. S. A. Overduin, A. d’ Avella, J. M. Carmena, and E. Bizzi, “Muscle synergies evoked by microstimulation are preferentially encoded during behavior,” Frontiers in Computational Neuroscience, vol. 8, p. 20, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. S. A. Overduin, A. d'Avella, J. Roh, J. M. Carmena, and E. Bizzi, “Representation of muscle synergies in the primate brain,” Journal of Neuroscience, vol. 35, no. 37, pp. 12615–12624, 2015. View at Publisher · View at Google Scholar · View at Scopus
  35. M. C. Tresch, P. Saltiel, and E. Bizzi, “The construction of movement by the spinal cord,” Nature Neuroscience, vol. 2, no. 2, pp. 162–167, 1999. View at Publisher · View at Google Scholar · View at Scopus
  36. A. P. Georgopoulos, R. E. Kettner, and A. B. Schwartz, “Primate motor cortex and free arm movements to visual targets in three-dimensional space. II. Coding of the direction of movement by a neuronal population,” Journal of Neuroscience, vol. 8, no. 8, pp. 2928–2937, 1988. View at Google Scholar
  37. F. A. Mussa-Ivaldi, S. F. Giszter, and E. Bizzi, “Linear combinations of primitives in vertebrate motor control,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 16, pp. 7534–7538, 1994. View at Publisher · View at Google Scholar · View at Scopus
  38. C. Ethier, L. Brizzi, W. G. Darling, and C. Capaday, “Linear summation of cat motor cortex outputs,” Journal of Neuroscience, vol. 26, no. 20, pp. 5574–5581, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. W. J. Kargo and S. F. Giszter, “Rapid correction of aimed movements by summation of force-field primitives,” Journal of Neuroscience, vol. 20, no. 1, pp. 409–426, 2000. View at Google Scholar
  40. M. A. Lemay, J. E. Calagan, N. Hogan, and E. Bizzi, “Modulation and vectorial summation of the spinalized frog’s hindlimb end-point force produced by intraspinal electrical stimulation of the cord,” IEEE Transactions on Neural Systems and Rehabilitation Engineering, vol. 9, no. 1, pp. 12–23, 2001. View at Publisher · View at Google Scholar · View at Scopus
  41. C. Capaday and C. van Vreeswijk, “Linear summation of outputs in a balanced network model of motor cortex,” Frontiers in Computational Neuroscience, vol. 9, p. 63, 2015. View at Publisher · View at Google Scholar · View at Scopus
  42. S. J. Day and M. Hulliger, “Experimental simulation of cat electromyogram: evidence for algebraic summation of motor-unit action-potential trains,” Journal of Neurophysiology, vol. 86, no. 5, pp. 2144–2158, 2001. View at Publisher · View at Google Scholar
  43. S. Hagio and M. Kouzaki, “Action direction of muscle synergies in three-dimensional force space,” Frontiers in Bioengineering and Biotechnology, vol. 3, 2015. View at Publisher · View at Google Scholar
  44. C. B. Hart and S. F. Giszter, “A neural basis for motor primitives in the spinal cord,” Journal of Neuroscience, vol. 30, no. 4, pp. 1322–1336, 2010. View at Publisher · View at Google Scholar · View at Scopus
  45. L. H. Ting, “A limited set of muscle synergies for force control during a postural task,” Journal of Neurophysiology, vol. 93, no. 1, pp. 609–613, 2005. View at Publisher · View at Google Scholar · View at Scopus
  46. J. P. Walter, A. L. Kinney, S. A. Banks et al., “Muscle synergies may improve optimization prediction of knee contact forces during walking,” Journal of Biomechanical Engineering, vol. 136, no. 2, pp. 021031–0210319, 2014. View at Publisher · View at Google Scholar · View at Scopus
  47. S. Aoi and T. Funato, “Neuromusculoskeletal models based on the muscle synergy hypothesis for the investigation of adaptive motor control in locomotion via sensory-motor coordination,” Neuroscience Research, vol. 104, pp. 88–95, 2016. View at Publisher · View at Google Scholar · View at Scopus
  48. V. Krishnamoorthy, M. L. Latash, J. P. Scholz, and V. M. Zatsiorsky, “Muscle synergies during shifts of the center of pressure by standing persons,” Experimental Brain Research, vol. 152, no. 3, pp. 281–292, 2003. View at Publisher · View at Google Scholar · View at Scopus
  49. J. Laczko and M. Latash, Progress in Motor Control Theories and Translations, Springer, Switzerland, 2016. View at Publisher · View at Google Scholar
  50. F. J. Valero-Cuevas, M. Venkadesan, and E. Todorov, “Structured variability of muscle activations supports the minimal intervention principle of motor control,” Journal of Neurophysiology, vol. 102, no. 1, pp. 59–68, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. V. C. K. Cheung, L. Piron, M. Agostini, S. Silvoni, A. Turolla, and E. Bizzi, “Stability of muscle synergies for voluntary actions after cortical stroke in humans,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 46, pp. 19563–19568, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. Y. Hashiguchi, K. Ohata, R. Kitatani et al., “Merging and fractionation of muscle synergy indicate the recovery process in patients with hemiplegia: the first study of patients after subacute stroke,” Neural Plasticity, vol. 2016, Article ID 5282957, 7 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  53. H. Hirai, F. Miyazaki, H. Naritomi et al., “On the origin of muscle synergies: invariant balance in the co-activation of agonist and antagonist muscle pairs,” Frontiers in Bioengineering and Biotechnology, vol. 3, p. 192, 2015. View at Publisher · View at Google Scholar
  54. H. Alkadhi, G. R. Crelier, S. H. Boendermaker, X. Golay, M. C. Hepp-Reymond, and S. S. Kollias, “Reproducibility of primary motor cortex somatotopy under controlled conditions,” American Journal of Neuroradiology, vol. 23, no. 9, pp. 1524–1532, 2002. View at Google Scholar
  55. J. Frère and F. Hug, “Between-subject variability of muscle synergies during a complex motor skill,” Frontiers in Computational Neuroscience, vol. 6, 2012. View at Publisher · View at Google Scholar · View at Scopus
  56. S. A. Overduin, A. D'avella, J. Roh, and E. Bizzi, “Modulation of muscle synergy recruitment in primate grasping,” Journal of Neuroscience, vol. 28, no. 4, pp. 880–892, 2008. View at Publisher · View at Google Scholar · View at Scopus
  57. J. Roh, W. Z. Rymer, and R. F. Beer, “Robustness of muscle synergies underlying three-dimensional force generation at the hand in healthy humans,” Journal of Neurophysiology, vol. 107, no. 8, pp. 2123–2142, 2012. View at Publisher · View at Google Scholar · View at Scopus
  58. G. Torres-Oviedo, J. M. Macpherson, and L. H. Ting, “Muscle synergy organization is robust across a variety of postural perturbations,” Journal of Neurophysiology, vol. 96, no. 3, pp. 1530–1546, 2006. View at Publisher · View at Google Scholar · View at Scopus
  59. G. Torres-Oviedo and L. H. Ting, “Subject-specific muscle synergies in human balance control are consistent across different biomechanical contexts,” Journal of Neurophysiology, vol. 103, no. 6, pp. 3084–3098, 2010. View at Publisher · View at Google Scholar · View at Scopus
  60. V. C. Cheung, “Central and sensory contributions to the activation and organization of muscle synergies during natural motor behaviors,” Journal of Neuroscience, vol. 25, no. 27, pp. 6419–6434, 2005. View at Publisher · View at Google Scholar · View at Scopus
  61. M. Berniker, A. Jarc, E. Bizzi, and M. C. Tresch, “Simplified and effective motor control based on muscle synergies to exploit musculoskeletal dynamics,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 18, pp. 7601–7606, 2009. View at Publisher · View at Google Scholar · View at Scopus
  62. W. J. Kargo, A. Ramakrishnan, C. B. Hart, L. C. Rome, and S. F. Giszter, “A simple experimentally based model using proprioceptive regulation of motor primitives captures adjusted trajectory formation in spinal frogs,” Journal of Neurophysiology, vol. 103, no. 1, pp. 573–590, 2010. View at Publisher · View at Google Scholar · View at Scopus
  63. N. Kuppuswamy and C. M. Harris, “Do muscle synergies reduce the dimensionality of behavior?” Frontiers in Computational Neuroscience, vol. 8, p. 63, 2014. View at Publisher · View at Google Scholar · View at Scopus
  64. J. J. Kutch and F. J. Valero-Cuevas, “Challenges and new approaches to proving the existence of muscle synergies of neural origin,” PLoS Computational Biology, vol. 8, no. 5, article e1002434, 2012. View at Publisher · View at Google Scholar · View at Scopus
  65. K. M. Bennett and R. N. Lemon, “The influence of single monkey cortico-motoneuronal cells at different levels of activity in target muscles,” The Journal of Physiology, vol. 477, no. 2, pp. 291–307, 1994. View at Publisher · View at Google Scholar · View at Scopus
  66. A. Cherian, H. L. Fernandes, and L. E. Miller, “Primary motor cortical discharge during force field adaptation reflects muscle-like dynamics,” Journal of Neurophysiology, vol. 110, no. 3, pp. 768–783, 2013. View at Publisher · View at Google Scholar · View at Scopus
  67. J. P. Donoghue, J. N. Sanes, N. G. Hatsopoulos, and G. Gaál, “Neural discharge and local field potential oscillations in primate motor cortex during voluntary movements,” Journal of Neurophysiology, vol. 79, no. 1, pp. 159–173, 1998. View at Publisher · View at Google Scholar
  68. K. W. Van Antwerp, T. J. Burkholder, and L. H. Ting, “Interjoint coupling effects on muscle contributions to endpoint force and acceleration in a musculoskeletal model of the cat hindlimb,” Journal of Biomechanics, vol. 40, no. 16, pp. 3570–3579, 2007. View at Publisher · View at Google Scholar · View at Scopus
  69. F. De Groote, I. Jonkers, and J. Duysens, “Task constraints and minimization of muscle effort result in a small number of muscle synergies during gait,” Frontiers in Computational Neuroscience, vol. 8, p. 115, 2014. View at Publisher · View at Google Scholar · View at Scopus
  70. Y. P. Ivanenko, R. E. Poppele, and F. Lacquaniti, “Five basic muscle activation patterns account for muscle activity during human locomotion,” The Journal of Physiology, vol. 556, no. 1, pp. 267–282, 2004. View at Publisher · View at Google Scholar · View at Scopus
  71. F. Hug, N. A. Turpin, S. Dorel, and A. Guével, “Smoothing of electromyographic signals can influence the number of extracted muscle synergies,” Clinical Neurophysiology, vol. 123, no. 9, pp. 1895-1896, 2012. View at Publisher · View at Google Scholar · View at Scopus
  72. E. J. Weiss and M. Flanders, “Muscular and postural synergies of the human hand,” Journal of Neurophysiology, vol. 92, no. 1, pp. 523–535, 2004. View at Publisher · View at Google Scholar · View at Scopus
  73. H. J. Chiel, L. H. Ting, O. Ekeberg, and M. J. Z. Hartmann, “The brain in its body: motor control and sensing in a biomechanical context,” Journal of Neuroscience, vol. 29, no. 41, pp. 12807–12814, 2009. View at Publisher · View at Google Scholar · View at Scopus
  74. A. J. Ijspeert, A. Crespi, D. Ryczko, and J. M. Cabelguen, “From swimming to walking with a salamander robot driven by a spinal cord model,” Science, vol. 315, no. 5817, pp. 1416–1420, 2007. View at Publisher · View at Google Scholar · View at Scopus
  75. F. Delcomyn, “Neural basis of rhythmic behavior in animals,” Science, vol. 210, no. 4469, pp. 492–498, 1980. View at Publisher · View at Google Scholar
  76. S. Grillner, “Neurobiological bases of rhythmic motor acts in vertebrates,” Science, vol. 228, no. 4696, pp. 143–149, 1985. View at Publisher · View at Google Scholar
  77. J. M. Inouye and F. J. Valero-Cuevas, “Muscle synergies heavily influence the neural control of arm endpoint stiffness and energy consumption,” PLoS Computational Biology, vol. 12, no. 2, article e1004737, 2016. View at Publisher · View at Google Scholar · View at Scopus
  78. A. Prochazka and P. Ellaway, “Sensory systems in the control of movement,” Comprehensive Physiology, vol. 2, pp. 2615–2627, 2012. View at Publisher · View at Google Scholar
  79. A. Prochazka and S. Yakovenko, “The neuromechanical tuning hypothesis,” Progress in Brain Research, vol. 165, pp. 255–265, 2007. View at Publisher · View at Google Scholar · View at Scopus
  80. T. G. Brown, “The intrinsic factors in the act of progression in the mammal,” Proceedings of the Royal Society B: Biological Sciences, vol. 84, no. 572, pp. 308–319, 1911. View at Publisher · View at Google Scholar
  81. S. Cash and R. Yuste, “Linear summation of excitatory inputs by CA1 pyramidal neurons,” Neuron, vol. 22, no. 2, pp. 383–394, 1999. View at Publisher · View at Google Scholar · View at Scopus
  82. J. A. Rathelot and P. L. Strick, “Subdivisions of primary motor cortex based on cortico-motoneuronal cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 3, pp. 918–923, 2009. View at Publisher · View at Google Scholar · View at Scopus
  83. A. J. Law, G. Rivlis, and M. H. Schieber, “Rapid acquisition of novel interface control by small ensembles of arbitrarily selected primary motor cortex neurons,” Journal of Neurophysiology, vol. 112, no. 6, pp. 1528–1548, 2014. View at Publisher · View at Google Scholar · View at Scopus
  84. K. Nazarpour, A. Barnard, and A. Jackson, “Flexible cortical control of task-specific muscle synergies,” Journal of Neuroscience, vol. 32, no. 36, pp. 12349–12360, 2012. View at Publisher · View at Google Scholar · View at Scopus
  85. S. Asavasopon, M. Rana, D. J. Kirages et al., “Cortical activation associated with muscle synergies of the human male pelvic floor,” The Journal of Neuroscience, vol. 34, no. 41, pp. 13811–13818, 2014. View at Publisher · View at Google Scholar · View at Scopus
  86. T. Drew, J. Kalaska, and N. Krouchev, “Muscle synergies during locomotion in the cat: a model for motor cortex control,” The Journal of Physiology, vol. 586, no. 5, pp. 1239–1245, 2008. View at Publisher · View at Google Scholar · View at Scopus
  87. M. Rana, M. S. Yani, S. Asavasopon, B. E. Fisher, and J. J. Kutch, “Brain connectivity associated with muscle synergies in humans,” Journal of Neuroscience, vol. 35, no. 44, pp. 14708–14716, 2015. View at Publisher · View at Google Scholar · View at Scopus
  88. T. Takei, J. Confais, S. Tomatsu, T. Oya, and K. Seki, “Neural basis for hand muscle synergies in the primate spinal cord,” Proceedings of the National Academy of Sciences of the United States of America, vol. 114, no. 32, pp. 8643–8648, 2017. View at Publisher · View at Google Scholar · View at Scopus
  89. T. Brochier, “Patterns of muscle activity underlying object-specific grasp by the macaque monkey,” Journal of Neurophysiology, vol. 92, no. 3, pp. 1770–1782, 2004. View at Publisher · View at Google Scholar · View at Scopus
  90. A. G. Rouse and M. H. Schieber, “Spatiotemporal distribution of location and object effects in primary motor cortex neurons during reach-to-grasp,” The Journal of Neuroscience, vol. 36, no. 41, pp. 10640–10653, 2016. View at Publisher · View at Google Scholar · View at Scopus
  91. E. Marder and D. Bucher, “Central pattern generators and the control of rhythmic movements,” Current Biology, vol. 11, no. 23, pp. R986–R996, 2001. View at Publisher · View at Google Scholar · View at Scopus
  92. K. Nishida, S. Hagio, B. Kibushi, T. Moritani, and M. Kouzaki, “Comparison of muscle synergies for running between different foot strike patterns,” PLoS One, vol. 12, no. 2, article e0171535, 2017. View at Publisher · View at Google Scholar · View at Scopus
  93. Y. P. Ivanenko, “Spinal cord maps of spatiotemporal alpha-motoneuron activation in humans walking at different speeds,” Journal of Neurophysiology, vol. 95, no. 2, pp. 602–618, 2006. View at Publisher · View at Google Scholar · View at Scopus
  94. M. C. Tresch, V. C. K. Cheung, and A. d’Avella, “Matrix factorization algorithms for the identification of muscle synergies: evaluation on simulated and experimental data sets,” Journal of Neurophysiology, vol. 95, no. 4, pp. 2199–2212, 2006. View at Publisher · View at Google Scholar · View at Scopus
  95. C. Alessandro, I. Delis, F. Nori, S. Panzeri, and B. Berret, “Muscle synergies in neuroscience and robotics: from input-space to task-space perspectives,” Frontiers in Computational Neuroscience, vol. 7, p. 43, 2013. View at Publisher · View at Google Scholar · View at Scopus
  96. A. d'Avella and F. Lacquaniti, “Control of reaching movements by muscle synergy combinations,” Frontiers in Computational Neuroscience, vol. 7, p. 42, 2013. View at Publisher · View at Google Scholar · View at Scopus
  97. C. B. Hart and S. F. Giszter, “Distinguishing synchronous and time-varying synergies using point process interval statistics: motor primitives in frog and rat,” Frontiers in Computational Neuroscience, vol. 7, p. 52, 2013. View at Publisher · View at Google Scholar
  98. M. Spüler, N. Irastorza-Landa, A. Sarasola-Sanz, and A. Ramos-Murguialday, “Extracting muscle synergy patterns from EMG data using autoencoders,” in Artificial neural networks and machine learning – ICANN 2016. Lecture Notes in Computer Science, vol. 9887, pp. 47–54. View at Publisher · View at Google Scholar · View at Scopus
  99. M. A. Maier and M. C. Hepp-Reymond, “EMG activation patterns during force production in precision grip. II. Muscular synergies in the spatial and temporal domain,” Experimental Brain Research, vol. 103, no. 1, pp. 123–136, 1995. View at Publisher · View at Google Scholar · View at Scopus
  100. K. M. Steele, M. C. Tresch, and E. J. Perreault, “Consequences of biomechanically constrained tasks in the design and interpretation of synergy analyses,” Journal of Neurophysiology, vol. 113, no. 7, pp. 2102–2113, 2015. View at Publisher · View at Google Scholar · View at Scopus
  101. T. Afzal, K. Iqbal, G. White, and A. B. Wright, “A method for locomotion mode identification using muscle synergies,” IEEE Transactions on Neural Systems and Rehabilitation Engineering, vol. 25, no. 6, pp. 608–617, 2017. View at Publisher · View at Google Scholar · View at Scopus
  102. G. Rasool, K. Iqbal, N. Bouaynaya, and G. White, “Real-time task discrimination for myoelectric control employing task-specific muscle synergies,” IEEE Transactions on Neural Systems and Rehabilitation Engineering, vol. 24, no. 1, pp. 98–108, 2016. View at Publisher · View at Google Scholar · View at Scopus
  103. I. Delis, B. Berret, T. Pozzo, and S. Panzeri, “Quantitative evaluation of muscle synergy models: a single-trial task decoding approach,” Frontiers in Computational Neuroscience, vol. 7, p. 8, 2013. View at Publisher · View at Google Scholar · View at Scopus
  104. J. J. Kutch, A. D. Kuo, A. M. Bloch, and W. Z. Rymer, “Endpoint force fluctuations reveal flexible rather than synergistic patterns of muscle cooperation,” Journal of Neurophysiology, vol. 100, no. 5, pp. 2455–2471, 2008. View at Publisher · View at Google Scholar · View at Scopus
  105. C. L. Banks, M. M. Pai, T. E. McGuirk, B. J. Fregly, and C. Patten, “Methodological choices in muscle synergy analysis impact differentiation of physiological characteristics following stroke,” Frontiers in Computational Neuroscience, vol. 11, p. 78, 2017. View at Publisher · View at Google Scholar · View at Scopus
  106. E. García-Cossio, D. Broetz, N. Birbaumer, and A. Ramos-Murguialday, “Cortex integrity relevance in muscle synergies in severe chronic stroke,” Frontiers in Human Neuroscience, vol. 8, p. 744, 2014. View at Publisher · View at Google Scholar · View at Scopus
  107. J. Roh, W. Z. Rymer, and R. F. Beer, “Evidence for altered upper extremity muscle synergies in chronic stroke survivors with mild and moderate impairment,” Frontiers in Human Neuroscience, vol. 9, p. 6, 2015. View at Publisher · View at Google Scholar · View at Scopus
  108. P. Tropea, V. Monaco, M. Coscia, F. Posteraro, and S. Micera, “Effects of early and intensive neuro-rehabilitative treatment on muscle synergies in acute post-stroke patients: a pilot study,” Journal of Neuroengineering and Rehabilitation, vol. 10, no. 1, p. 103, 2013. View at Publisher · View at Google Scholar · View at Scopus
  109. V. C. K. Cheung, A. Turolla, M. Agostini et al., “Muscle synergy patterns as physiological markers of motor cortical damage,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 36, pp. 14652–14656, 2012. View at Publisher · View at Google Scholar · View at Scopus
  110. D. J. Clark, L. H. Ting, F. E. Zajac, R. R. Neptune, and S. A. Kautz, “Merging of healthy motor modules predicts reduced locomotor performance and muscle coordination complexity post-stroke,” Journal of Neurophysiology, vol. 103, no. 2, pp. 844–857, 2010. View at Publisher · View at Google Scholar · View at Scopus
  111. I. Carpinella, J. Jonsdottir, T. Lencioni, T. Bowman, and M. Ferrarin, “Planar robotic rehabilitation of upper limb in post-stroke subjects: transfer of training effects to a non-trained 3D functional task,” Gait & Posture, vol. 49, Supplement 1, pp. S23–S24, 2016. View at Publisher · View at Google Scholar
  112. L. Dipietro, H. I. Krebs, S. E. Fasoli et al., “Changing motor synergies in chronic stroke,” Journal of Neurophysiology, vol. 98, no. 2, pp. 757–768, 2007. View at Publisher · View at Google Scholar · View at Scopus
  113. A. J. C. McMorland, K. D. Runnalls, and W. D. Byblow, “A neuroanatomical framework for upper limb synergies after stroke,” Frontiers in Human Neuroscience, vol. 9, p. 82, 2015. View at Publisher · View at Google Scholar · View at Scopus
  114. J. Godlove, T. Gulati, B. Dichter, E. Chang, and K. Ganguly, “Muscle synergies after stroke are correlated with perilesional high gamma,” Annals of Clinical and Translational Neurology, vol. 3, no. 12, pp. 956–961, 2016. View at Publisher · View at Google Scholar
  115. N. Manickaraj, L. M. Bisset, V. S. P. T. Devanaboyina, and J. J. Kavanagh, “Chronic pain alters spatiotemporal activation patterns of forearm muscle synergies during the development of grip force,” Journal of Neurophysiology, vol. 118, no. 4, pp. 2132–2141, 2017. View at Publisher · View at Google Scholar · View at Scopus
  116. S. Brunnstrom, Movement Therapy in Hemiplegia: A Neurophysiological Approach, Harper & Row, New York, New York, 1970.
  117. A. R. Fugl-Meyer, L. Jääskö, I. Leyman, S. Olsson, and S. Steglind, “The post-stroke hemiplegic patient. 1. a method for evaluation of physical performance,” Scandinavian Journal of Rehabilitation Medicine, vol. 7, no. 1, pp. 13–31, 1975. View at Google Scholar
  118. M. C. Cirstea and M. F. Levin, “Compensatory strategies for reaching in stroke,” Brain, vol. 123, no. 5, pp. 940–953, 2000. View at Publisher · View at Google Scholar
  119. M. G. Bowden, A. L. Behrman, R. R. Neptune, C. M. Gregory, and S. A. Kautz, “Locomotor rehabilitation of individuals with chronic stroke: difference between responders and nonresponders,” Archives of Physical Medicine and Rehabilitation, vol. 94, no. 5, pp. 856–862, 2013. View at Publisher · View at Google Scholar · View at Scopus
  120. T. A. Jones, “Motor compensation and its effects on neural reorganization after stroke,” Nature Reviews Neuroscience, vol. 18, no. 5, pp. 267–280, 2017. View at Publisher · View at Google Scholar · View at Scopus
  121. N. Hesam-Shariati, T. Trinh, A. G. Thompson-Butel, C. T. Shiner, and P. A. McNulty, “A longitudinal electromyography study of complex movements in poststroke therapy. 2: changes in coordinated muscle activation,” Frontiers in Neurology, vol. 8, p. 277, 2017. View at Publisher · View at Google Scholar · View at Scopus
  122. S. A. Chvatal, G. Torres-Oviedo, S. A. Safavynia, and L. H. Ting, “Common muscle synergies for control of center of mass and force in nonstepping and stepping postural behaviors,” Journal of Neurophysiology, vol. 106, no. 2, pp. 999–1015, 2011. View at Publisher · View at Google Scholar · View at Scopus
  123. N. Yang, Q. An, H. Yamakawa et al., “Clarification of muscle synergy structure during standing-up motion of healthy young, elderly and post-stroke patients,” in 2017 International Conference on Rehabilitation Robotics (ICORR), London, UK, 2017. View at Publisher · View at Google Scholar · View at Scopus
  124. N. Matsunaga, A. Imai, and K. Kaneoka, “Comparison of muscle synergies before and after 10 minutes of running,” Journal of Physical Therapy Science, vol. 29, no. 7, pp. 1242–1246, 2017. View at Publisher · View at Google Scholar · View at Scopus
  125. M. Kristiansen, A. Samani, P. Madeleine, and E. A. Hansen, “Effects of 5 weeks of bench press training on muscle synergies,” Journal of Strength and Conditioning Research, vol. 30, no. 7, pp. 1948–1959, 2016. View at Publisher · View at Google Scholar · View at Scopus
  126. S. Shaharudin, D. Zanotto, and S. Agrawal, “Muscle synergies of untrained subjects during 6 min maximal rowing on slides and fixed ergometer,” Journal of Sports Science & Medicine, vol. 13, no. 4, pp. 793–800, 2014. View at Google Scholar
  127. G. Grioli, M. Catalano, E. Silvestro, S. Tono, and A. Bicchi, “Adaptive synergies: an approach to the design of under-actuated robotic hands,” in 2012 IEEE/RSJ international conference on intelligent robots and systems (IROS), Vilamoura, Portugal, October 2012. View at Publisher · View at Google Scholar · View at Scopus
  128. G. Rasool, K. Iqbal, N. Bouaynaya, and G. White, “Neural drive estimation using the hypothesis of muscle synergies and the state-constrained Kalman filter,” in 2013 6th international IEEE/EMBS conference on neural engineering (NER), San Diego, CA, USA, 2013. View at Publisher · View at Google Scholar · View at Scopus
  129. M. G. Catalano, G. Grioli, E. Farnioli, A. Serio, C. Piazza, and A. Bicchi, “Adaptive synergies for the design and control of the Pisa/IIT SoftHand,” The International Journal of Robotics Research, vol. 33, no. 5, pp. 768–782, 2014. View at Publisher · View at Google Scholar · View at Scopus
  130. D. J. Berger and A. d'Avella, “Effective force control by muscle synergies,” Frontiers in Computational Neuroscience, vol. 8, 2014. View at Publisher · View at Google Scholar · View at Scopus
  131. M. C. Tresch and A. Jarc, “The case for and against muscle synergies,” Current Opinion in Neurobiology, vol. 19, no. 6, pp. 601–607, 2009. View at Publisher · View at Google Scholar · View at Scopus
  132. A. Bicchi, M. Gabiccini, and M. Santello, “Modelling natural and artificial hands with synergies,” Philosophical Transactions of the Royal Society B: Biological Sciences, vol. 366, no. 1581, pp. 3153–3161, 2011. View at Publisher · View at Google Scholar · View at Scopus
  133. A. J. Bastian, “Understanding sensorimotor adaptation and learning for rehabilitation,” Current Opinion in Neurology, vol. 21, no. 6, pp. 628–633, 2008. View at Publisher · View at Google Scholar · View at Scopus
  134. F. O. Barroso, D. Torricelli, E. Bravo-Esteban et al., “Muscle synergies in cycling after incomplete spinal cord injury: correlation with clinical measures of motor function and spasticity,” Frontiers in Human Neuroscience, vol. 9, p. 706, 2016. View at Publisher · View at Google Scholar · View at Scopus
  135. F. Lunardini, C. Casellato, M. Bertucco, T. D. Sanger, and A. Pedrocchi, “Children with and without dystonia share common muscle synergies while performing writing tasks,” Annals of Biomedical Engineering, vol. 45, no. 8, pp. 1949–1962, 2017. View at Publisher · View at Google Scholar · View at Scopus
  136. K. M. Steele, A. Rozumalski, and M. H. Schwartz, “Muscle synergies and complexity of neuromuscular control during gait in cerebral palsy,” Developmental Medicine & Child Neurology, vol. 57, no. 12, pp. 1176–1182, 2015. View at Publisher · View at Google Scholar · View at Scopus
  137. L. Tang, X. Chen, S. Cao, D. Wu, G. Zhao, and X. Zhang, “Assessment of upper limb motor dysfunction for children with cerebral palsy based on muscle synergy analysis,” Frontiers in Human Neuroscience, vol. 11, 2017. View at Publisher · View at Google Scholar · View at Scopus
  138. L. Tang, F. Li, S. Cao, X. Zhang, D. Wu, and X. Chen, “Muscle synergy analysis in children with cerebral palsy,” Journal of Neural Engineering, vol. 12, no. 4, article 046017, 2015. View at Publisher · View at Google Scholar · View at Scopus