Muscle activities in similar arms performing identical tasks reveal the neural basis of muscle synergies

Abstract

Are the muscle synergies extracted from multiple electromyographic signals an expression of neural information processing, or rather a by-product of mechanical and task constraints? To address this question, we asked 41 right-handed adults to perform a variety of motor tasks with their left and right arms. The analysis of the muscle activities resulted in the identification of synergies whose activation was different for the two sides. In particular, tasks involving the control of isometric forces resulted in larger differences. As the two arms essentially have identical biomechanical structure, we concluded that the differences observed in the activation of the respective synergies must be attributed to neural control.

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Data availability

The data sets analyzed during the current study are available from the corresponding author upon reasonable request.

References

  1. Adam A, De Luca CJ, Erim Z (1998) Hand dominance and motor unit firing behavior. J Neurophysiol 80:1373–1382

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  2. Alessandro C, Delis I, Nori F, Panzeri S, Berret B (2013) Muscle synergies in neuroscience and robotics: from input-space to task-space perspectives. Frontiers in computational neuroscience 7:43

    PubMed  PubMed Central  Article  Google Scholar 

  3. Annett M (1970) A classification of hand preference by association analysis. Br J Psychol 61:303–321

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  4. Annett M (2002) Handedness and brain asymmetry: the right shift theory. Psychology Press, Hove, East Sussex

    Google Scholar 

  5. Annett J, Annett M, Hudson P, Turner A (1979) The control of movement in the preferred and non-preferred hands. Q J Exp Psychol 31:641–652

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  6. Auerbach BM, Ruff CB (2006) Limb bone bilateral asymmetry: variability and commonality among modern humans. J Hum Evol 50:203–218

    PubMed  Article  PubMed Central  Google Scholar 

  7. Bagesteiro LB, Sainburg RL (2002) Handedness: dominant arm advantages in control of limb dynamics. J Neurophysiol 88:2408–2421

    PubMed  Article  PubMed Central  Google Scholar 

  8. Barroso FO, Torricelli D, Moreno JC, Taylor J, Gomez-Soriano J, Bravo-Esteban E, Piazza S, Santos C, Pons JL (2014) Shared muscle synergies in human walking and cycling. J Neurophysiol 112:1984–1998

    PubMed  Article  PubMed Central  Google Scholar 

  9. Batzianoulis I, El-Khoury S, Pirondini E, Coscia M, Micera S, Billard A (2017) EMG-based decoding of grasp gestures in reaching-to-grasping motions. Robot Auton Syst 91:59–70

    Article  Google Scholar 

  10. Berger DJ, d’Avella A (2014) Effective force control by muscle synergies. Front Comput Neurosci 8:46

    PubMed  PubMed Central  Article  Google Scholar 

  11. Bernstein N (1967) The co-ordination and regulation of movements. Pergamon Press, Oxford

    Google Scholar 

  12. Bizzi E, Cheung VC (2013) The neural origin of muscle synergies. Front Comput Neurosci 7:51

    PubMed  PubMed Central  Article  Google Scholar 

  13. Blank R, Miller V, von Voss H (2000) Human motor development and hand laterality: a kinematic analysis of drawing movements. Neurosci Lett 295:89–92

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  14. Boulinguez P, Nougier V, Velay JL (2001) Manual asymmetries in reaching movement control. I: study of right-handers. Cortex J Devot Study Nerv Syst Behav 37:101–122

    CAS  Article  Google Scholar 

  15. Cappellini G, Ivanenko YP, Poppele RE, Lacquaniti F (2006) Motor patterns in human walking and running. J Neurophysiol 95:3426–3437

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  16. Carson RG, Goodman D, Elliott D (1992) Asymmetries in the discrete and pseudocontinuous regulation of visually guided reaching. Brain Cogn 18:169–191

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  17. Carson RG, Chua R, Goodman D, Byblow WD, Elliott D (1995) The preparation of aiming movements. Brain Cogn 28:133–154

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  18. Casadio M, Sanguineti V, Morasso PG, Arrichiello V (2006) Braccio di Ferro: a new haptic workstation for neuromotor rehabilitation. Technol Health Care 14:123–142

    PubMed  Article  PubMed Central  Google Scholar 

  19. Casadio M, Sanguineti V, Solaro C, Morasso PG (2007) A haptic robot reveals the adaptation capability of individuals with multiple sclerosis. Int J Robot Res 26:1225–1233

    Article  Google Scholar 

  20. Casadio M, Sanguineti V, Morasso P, Solaro C (2008) Abnormal sensorimotor control, but intact force field adaptation, in multiple sclerosis subjects with no clinical disability. Mult Scler 14:330–342

    PubMed  Article  Google Scholar 

  21. Cheung VC, d’Avella A, Tresch MC, Bizzi E (2005) Central and sensory contributions to the activation and organization of muscle synergies during natural motor behaviors. J Neurosci 25:6419–6434

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  22. Cheung VC, d’Avella A, Bizzi E (2009a) Adjustments of motor pattern for load compensation via modulated activations of muscle synergies during natural behaviors. J Neurophysiol 101:1235–1257

    PubMed  Article  Google Scholar 

  23. Cheung VC, Piron L, Agostini M, Silvoni S, Turolla A, Bizzi E (2009b) Stability of muscle synergies for voluntary actions after cortical stroke in humans. Proc Natl Acad Sci USA 106:19563–19568

    CAS  PubMed  Article  Google Scholar 

  24. Cheung VC, Turolla A, Agostini M, Silvoni S, Bennis C, Kasi P, Paganoni S, Bonato P, Bizzi E (2012) Muscle synergy patterns as physiological markers of motor cortical damage. Proc Natl Acad Sci 109:14652–14656

    CAS  PubMed  Article  Google Scholar 

  25. Cipriani C, Antfolk C, Controzzi M, Lundborg G, Rosen B, Carrozza MC, Sebelius F (2011) Online myoelectric control of a dexterous hand prosthesis by transradial amputees. IEEE Trans Neural Syst Rehabilit Eng 19:260–270

    Article  Google Scholar 

  26. Corballis MC (1983) Human laterality. Academic Press, New York

    Google Scholar 

  27. Coscia M, Cheung VC, Tropea P, Koenig A, Monaco V, Bennis C, Micera S, Bonato P (2014) The effect of arm weight support on upper limb muscle synergies during reaching movements. J Neuroeng Rehabilit 11:22

    Article  Google Scholar 

  28. Coscia M, Monaco V, Martelloni C, Rossi B, Chisari C, Micera S (2015) Muscle synergies and spinal maps are sensitive to the asymmetry induced by a unilateral stroke. J Neuroeng Rehabilit 12:39

    Article  Google Scholar 

  29. Coscia M, Tropea P, Monaco V, Micera S (2018) Muscle synergies approach and perspective on application to robot-assisted rehabilitation. In: Rehabilitation Robotics, Elsevier, pp 319–331

  30. Danziger Z, Mussa-Ivaldi FA (2012) The influence of visual motion on motor learning. J Neurosci 32:9859–9869

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  31. 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

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  32. d’Avella A, Portone A, Fernandez L, Lacquaniti F (2006) Control of fast-reaching movements by muscle synergy combinations. J Neurosci 26:7791–7810

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  33. d’Avella A, Fernandez L, Portone A, Lacquaniti F (2008) Modulation of phasic and tonic muscle synergies with reaching direction and speed. J Neurophysiol 100:1433–1454

    PubMed  Article  PubMed Central  Google Scholar 

  34. d’Avella A, Portone A, Lacquaniti F (2011) Superposition and modulation of muscle synergies for reaching in response to a change in target location. J Neurophysiol 106:2796–2812

    PubMed  Article  PubMed Central  Google Scholar 

  35. Diederichsen LP, Norregaard J, Dyhre-Poulsen P, Winther A, Tufekovic G, Bandholm T, Rasmussen LR, Krogsgaard M (2007) The effect of handedness on electromyographic activity of human shoulder muscles during movement. J Electromyogr Kinesiol 17:410–419

    PubMed  Article  PubMed Central  Google Scholar 

  36. Dipietro L, Krebs HI, Fasoli SE, Volpe BT, Stein J, Bever C, Hogan N (2007) Changing motor synergies in chronic stroke. J Neurophysiol 98:757–768

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  37. Dominici N, Ivanenko YP, Cappellini G, d’Avella A, Mondì V, Cicchese M, Fabiano A, Silei T, Di Paolo A, Giannini C (2011) Locomotor primitives in newborn babies and their development. Science 334:997–999

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  38. Duthilleul N, Pirondini E, Coscia M, Micera S (2015) Effect of handedness on muscle synergies during upper limb planar movements. Conf Proc Ann Int Conf IEEE Eng Med Biol Soc IEEE Eng Med Biol Soc Ann Conf 2015:3452–3455

    CAS  Google Scholar 

  39. Elliott D, Roy EA, Goodman D, Carson RG, Chua R, Maraj BK (1993) Asymmetries in the preparation and control of manual aiming movements. Can J Exp Psychol Revue 47:570

    Article  Google Scholar 

  40. Farina D, Kallenberg LA, Merletti R, Hermens HJ (2003) Effect of side dominance on myoelectric manifestations of muscle fatigue in the human upper trapezius muscle. Eur J Appl Physiol 90:480–488

    PubMed  Article  PubMed Central  Google Scholar 

  41. Flanders M (1991) Temporal patterns of muscle activation for arm movements in three-dimensional space. J Neurosci 11:2680–2693

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  42. Freitas SM, Duarte M, Latash ML (2006) Two kinematic synergies in voluntary whole-body movements during standing. J Neurophysiol 95:636–645

    PubMed  Article  PubMed Central  Google Scholar 

  43. Frere J, Hug F (2012) Between-subject variability of muscle synergies during a complex motor skill. Front Comput Neurosci 6:99

    PubMed  PubMed Central  Article  Google Scholar 

  44. Friedli WG, Fuhr P, Wiget W (1987) Detection threshold for percutaneous electrical stimuli: asymmetry with respect to handedness. J Neurol Neurosurg Psychiatry 50:870–876

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  45. Fugl-Meyer A, Eriksson A, Sjöström M, Söderström G (1982) Is muscle structure influenced by genetical or functional factors? A study of three forearm muscles. Acta Physiol 114:277–281

    CAS  Article  Google Scholar 

  46. Giszter S, Patil V, Hart C (2007) Primitives, premotor drives, and pattern generation: a combined computational and neuroethological perspective. Prog Brain Res 165:323–346

    PubMed  Article  PubMed Central  Google Scholar 

  47. Goble DJ, Brown SH (2008) The biological and behavioral basis of upper limb asymmetries in sensorimotor performance. Neurosci Biobehav Rev 32:598–610

    PubMed  Article  PubMed Central  Google Scholar 

  48. Hart CB, Giszter SF (2010) A neural basis for motor primitives in the spinal cord. J Neurosci 30:1322–1336

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  49. Heath M, Roy EA (2000) The expression of manual asymmetries following extensive training of the nondominant hand: a kinematic perspective. Brain Cogn 43:252–257

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Hermens HJ, Freriks B, Disselhorst-Klug C, Rau G (2000) Development of recommendations for SEMG sensors and sensor placement procedures. J Electromyogr Kinesiol 10:361–374

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  51. Ison M, Artemiadis P (2014) The role of muscle synergies in myoelectric control: trends and challenges for simultaneous multifunction control. J Neural Eng 11:051001

    PubMed  Article  PubMed Central  Google Scholar 

  52. Ivanenko YP, Poppele RE, Lacquaniti F (2004) Five basic muscle activation patterns account for muscle activity during human locomotion. J Physiol 556:267–282

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  53. Kuiken TA, Lowery MM, Stoykov NS (2003) The effect of subcutaneous fat on myoelectric signal amplitude and cross-talk. Prosthet Orthot Int 27:48–54

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Kutch JJ, Valero-Cuevas FJ (2011) Muscle redundancy does not imply robustness to muscle dysfunction. J Biomech 44:1264–1270

    PubMed  PubMed Central  Article  Google Scholar 

  55. Kutch JJ, Valero-Cuevas FJ (2012) Challenges and new approaches to proving the existence of muscle synergies of neural origin. PLoS Comput Biol 8:e1002434

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  56. Latash ML, Anson JG (2006) Synergies in health and disease: relations to adaptive changes in motor coordination. Phys Ther 86:1151–1160

    PubMed  Article  PubMed Central  Google Scholar 

  57. Lee DD, Seung HS (2001) Algorithms for non-negative matrix factorization. In: Advances in neural information processing systems, pp 556–562

  58. Leib R, Rubin I, Nisky I (2018) Force feedback delay affects perception of stiffness but not action, and the effect depends on the hand used but not on the handedness. J Neurophysiol 120(2):781–794

    PubMed  Article  PubMed Central  Google Scholar 

  59. Levine AJ, Hinckley CA, Hilde KL, Driscoll SP, Poon TH, Montgomery JM, Pfaff SL (2014) Identification of a cellular node for motor control pathways. Nat Neurosci 17:586–593

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  60. Liu X, Mosier KM, Mussa-Ivaldi FA, Casadio M, Scheidt RA (2011) Reorganization of finger coordination patterns during adaptation to rotation and scaling of a newly learned sensorimotor transformation. J Neurophysiol 105:454–473

    PubMed  Article  Google Scholar 

  61. Muceli S, Jiang N, Farina D (2014) Extracting signals robust to electrode number and shift for online simultaneous and proportional myoelectric control by factorization algorithms. IEEE Trans Neural Syst Rehabilit Eng 22:623–633

    Article  Google Scholar 

  62. Mussa-Ivaldi FA, Bizzi E (2000) Motor learning through the combination of primitives. Philoso Trans R Soc B 355:1755–1769

    CAS  Article  Google Scholar 

  63. Neptune RR, Clark DJ, Kautz SA (2009) Modular control of human walking: a simulation study. J Biomech 42:1282–1287

    PubMed  PubMed Central  Article  Google Scholar 

  64. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113

    CAS  Article  Google Scholar 

  65. Osu R, Burdet E, Franklin DW, Milner TE, Kawato M (2003) Different mechanisms involved in adaptation to stable and unstable dynamics. J Neurophysiol 90:3255–3269

    PubMed  Article  Google Scholar 

  66. Overduin SA, d’Avella A, Carmena JM, Bizzi E (2012) Microstimulation activates a handful of muscle synergies. Neuron 76:1071–1077

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  67. Pellegrino L, Coscia M, Muller M, Solaro C, Casadio M (2018) Evaluating upper limb impairments in multiple sclerosis by exposure to different mechanical environments. Sci Rep 8:2110

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  68. Perotto A, Delagi EF (2005) Anatomical guide for the electromyographer: the limbs and trunk. Charles C Thomas Publisher

  69. Ranganathan R, Krishnan C (2012) Extracting synergies in gait: using EMG variability to evaluate control strategies. J Neurophysiol 108:1537–1544

    PubMed  PubMed Central  Article  Google Scholar 

  70. Roh J, Rymer WZ, Beer RF (2012) Robustness of muscle synergies underlying three-dimensional force generation at the hand in healthy humans. J Neurophysiol 107:2123–2142

    PubMed  PubMed Central  Article  Google Scholar 

  71. Roh J, Rymer WZ, Perreault EJ, Yoo SB, Beer RF (2013) Alterations in upper limb muscle synergy structure in chronic stroke survivors. J Neurophysiol 109:768–781

    PubMed  Article  PubMed Central  Google Scholar 

  72. Roy EA, Kalbfleisch L, Elliott D (1994) Kinematic analyses of manual asymmetries in visual aiming movements. Brain Cogn 24:289–295

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  73. Sainburg RL (2002) Evidence for a dynamic-dominance hypothesis of handedness. Exp Brain Res 142:241–258

    PubMed  Article  PubMed Central  Google Scholar 

  74. Sainburg RL (2005) Handedness: differential specializations for control of trajectory and position. Exerc Sport Sci Rev 33:206–213

    PubMed  Article  PubMed Central  Google Scholar 

  75. Sainburg RL, Schaefer SY (2004) Interlimb differences in control of movement extent. J Neurophysiol 92:1374–1383

    PubMed  PubMed Central  Article  Google Scholar 

  76. Santello M (2002) Kinematic synergies for the control of hand shape. Arch Ital Biol 140:221–228

    CAS  PubMed  PubMed Central  Google Scholar 

  77. Sathiamoorthy A, Sathiamoorthy SS (1990) Limb dominance and motor conduction velocity of median and ulnar nerves. Indian J Physiol Pharmacol 34:51–53

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Semmler JG, Nordstrom MA (1998) Hemispheric differences in motor cortex excitability during a simple index finger abduction task in humans. J Neurophysiol 79:1246–1254

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  79. Steele KM, Tresch MC, Perreault EJ (2015) Consequences of biomechanically constrained tasks in the design and interpretation of synergy analyses. J Neurophysiol 113:2102–2113

    PubMed  PubMed Central  Article  Google Scholar 

  80. Tan U (1989) Spinal motor lateralization assessed by recovery curve of H reflex from wrist flexors in right-, and left-handed normal subjects. Int J Neurosci 48:309–312

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  81. Teulings HL, Contreras-Vidal JL, Stelmach GE, Adler CH (1997) Parkinsonism reduces coordination of fingers, wrist, and arm in fine motor control. Exp Neurol 146:159–170

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  82. Ting LH, McKay JL (2007) Neuromechanics of muscle synergies for posture and movement. Curr Opin Neurobiol 17:622–628

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  83. Ting LH, Chiel HJ, Trumbower RD, Allen JL, McKay JL, Hackney ME, Kesar TM (2015) Neuromechanical principles underlying movement modularity and their implications for rehabilitation. Neuron 86:38–54

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  84. Torricelli D, Barroso F, Coscia M, Alessandro C, Lunardini F, Esteban EB, d’Avella A (2016) Muscle synergies in clinical practice: theoretical and practical implications. In: Emerging therapies in neurorehabilitation II. Springer, pp 251–272

  85. Tresch MC, Cheung VC, d’Avella A (2006) Matrix factorization algorithms for the identification of muscle synergies: evaluation on simulated and experimental data sets. J Neurophysiol 95:2199–2212

    PubMed  Article  PubMed Central  Google Scholar 

  86. Tropea P, Monaco V, Coscia M, Posteraro F, Micera S (2013) Effects of early and intensive neuro-rehabilitative treatment on muscle synergies in acute post-stroke patients: a pilot study. J Neuroeng Rehabilit 10:103

    Article  Google Scholar 

  87. van Doorn RR (2008) Manual asymmetries in the temporal and spatial control of aimed movements. Hum Mov Sci 27:551–576

    PubMed  Article  PubMed Central  Google Scholar 

  88. Volkmann J, Schnitzler A, Witte OW, Freund H (1998) Handedness and asymmetry of hand representation in human motor cortex. J Neurophysiol 79:2149–2154

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  89. Wang J, Sainburg RL (2007) The dominant and nondominant arms are specialized for stabilizing different features of task performance. Exp Brain Res 178:565–570

    PubMed  Article  PubMed Central  Google Scholar 

  90. Washabaugh EP, Krishnan C (2018) A wearable resistive robot facilitates locomotor adaptations during gait. Restor Neurol Neurosci 36:215–223

    PubMed  PubMed Central  Google Scholar 

  91. Woodworth RS (1899) Accuracy of voluntary movement. Psychol Rev 3:i

    Google Scholar 

  92. Yakovenko S, Krouchev N, Drew T (2011) Sequential activation of motor cortical neurons contributes to intralimb coordination during reaching in the cat by modulating muscle synergies. J Neurophysiol 105:388–409

    PubMed  Article  PubMed Central  Google Scholar 

  93. Zardoshti-Kermani M, Wheeler BC, Badie K, Hashemi RM (1995) EMG feature evaluation for movement control of upper extremity prostheses. IEEE Trans Rehabilit Eng 3:324–333

    Article  Google Scholar 

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Acknowledgements

The authors are grateful to all participants of the study for volunteering their time. We want to thank Giorgia Stranieri, Amel Chief and Maddalena Mugnosso for the help during the experimental sessions, Dr. Susanna Summa and Dr. Camilla Pierella for helpful suggestions, Prof. Ferdinando Mussa-Ivaldi for his advice and critical review of the manuscript, Prof. Niels Birbaumer for his further revision of the manuscript, and Brenda Klem for proofreading the manuscript.

Funding

This research was supported by Italian Multiple Sclerosis Foundation (FISM, 2013- Cod. 2013/R/5) and by Marie Curie Integration Grant FP7-PEOPLE- 2012-CIG- 334201 (REMAKE) Research projects of national interest (ModuLimb, PRIN-2015HFWRYY).

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All the authors conceived the study, designed the experimental protocol and developed the experimental setup. LP collected the data. All authors analyzed the results, contributed to the discussion of the results and to writing of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Maura Casadio.

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Communicated by Francesco Lacquaniti.

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Pellegrino, L., Coscia, M. & Casadio, M. Muscle activities in similar arms performing identical tasks reveal the neural basis of muscle synergies. Exp Brain Res 238, 121–138 (2020). https://doi.org/10.1007/s00221-019-05679-9

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Keywords

  • Upper limb
  • Robotic evaluation
  • Reaching
  • Electromyography