Multi-finger synergies and the muscular apparatus of the hand

Abstract

We explored whether the synergic control of the hand during multi-finger force production tasks depends on the hand muscles involved. Healthy subjects performed accurate force production tasks and targeted force pulses while pressing against loops positioned at the level of fingertips, middle phalanges, and proximal phalanges. This varied the involvement of the extrinsic and intrinsic finger flexors. The framework of the uncontrolled manifold (UCM) hypothesis was used to analyze the structure of inter-trial variance, motor equivalence, and anticipatory synergy adjustments prior to the force pulse in the spaces of finger forces and finger modes (hypothetical finger-specific control signals). Subjects showed larger maximal force magnitudes at the proximal site of force production. There were synergies stabilizing total force during steady-state phases across all three sites of force production; no differences were seen across the sites in indices of structure of variance, motor equivalence, or anticipatory synergy adjustments. Indices of variance, which did not affect the task (within the UCM), correlated with motor equivalent motion between the steady states prior to and after the force pulse; in contrast, variance affecting task performance did not correlate with non-motor equivalent motion. The observations are discussed within the framework of hierarchical control with referent coordinates for salient effectors at each level. The findings suggest that multi-finger synergies are defined at the level of abundant transformation between the low-dimensional hand level and higher dimensional finger level while being relatively immune to transformations between the finger level and muscle level. The results also support the scheme of control with two classes of neural variables that define referent coordinates and gains in back-coupling loops between hierarchical control levels.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Ambike S, Zatsiorsky VM, Latash ML (2015) Processes underlying unintentional finger force changes in the absence of visual feedback. Exp Brain Res 233:711–721

    Article  PubMed  Google Scholar 

  2. Ambike S, Mattos D, Zatsiorsky VM, Latash ML (2016) Synergies in the space of control variables within the equilibrium-point hypothesis. Neurosci 315:150–161

    CAS  Article  Google Scholar 

  3. An KN, Chao EY, Cooney WP, Linschield RL (1985) Forces in the normal and abnormal hand. J Orthop Res 3:202–211

    CAS  Article  PubMed  Google Scholar 

  4. Basmajian JV, De Luca CJ (1985) Muscles Alive, 5th edn. Williams and Wilkins, Baltimore

    Google Scholar 

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

    Google Scholar 

  6. Chao EY, Opgrande JD, Axmear FE (1976) Three dimensional force analysis of finger joints in selected isometric hand function. J Biomech 19:387–396

    Article  Google Scholar 

  7. Danion F, Schöner G, Latash ML, Li S, Scholz JP, Zatsiorsky VM (2003) A force mode hypothesis for finger interaction during multi-finger force production tasks. Biol Cybern 88:91–98

    Article  PubMed  Google Scholar 

  8. Darling WG, Cole KJ, Miller GF (1994) Coordination of index finger movements. J Biomech 27:479–491

    CAS  Article  PubMed  Google Scholar 

  9. Domkin D, Laczko J, Jaric S, Johansson H, Latash ML (2002) Structure of joint variability in bimanual pointing tasks. Exp Brain Res 143:11–23

    Article  PubMed  Google Scholar 

  10. Falaki A, Huang X, Lewis MM, Latash ML (2017) Motor equivalence and structure of variance: multi-muscle postural synergies in Parkinson’s disease. Exp Brain Res 235:2243–2258

    Article  PubMed  Google Scholar 

  11. Feldman AG (1966) Functional tuning of the nervous system with control of movement or maintenance of a steady posture. II. Controllable parameters of the muscle. Biophysics 11:565–578

    Google Scholar 

  12. Feldman AG (1980) Superposition of motor programs. I. Rhythmic forearm movements in man. Neurosci 5:81–90

    CAS  Article  Google Scholar 

  13. Feldman AG (1986) Once more on the equilibrium-point hypothesis (λ-model) for motor control. J Mot Behav 18:17–54

    CAS  Article  PubMed  Google Scholar 

  14. Feldman AG (2015) Referent control of action and perception: challenging conventional theories in behavioral science. Springer, NY

    Google Scholar 

  15. Friedman J, SKM V, Zatsiorsky VM, Latash ML (2009) The sources of two components of variance: An example of multifinger cyclic force production tasks at different frequencies. Exp Brain Res 196:263–277

    Article  PubMed  PubMed Central  Google Scholar 

  16. Furmanek M, Solnik S, Piscitelli D, Rasouli O, Falaki A, Latash ML (2018) Synergies and motor equivalence in voluntary sway tasks: the effects of visual and mechanical constraints. J Mot Behav (in press) https://doi.org/10.1080/00222895.2017.1367642

    Google Scholar 

  17. Gelfand IM, Latash ML (1998) On the problem of adequate language in movement science. Mot Control 2:306–313

    CAS  Article  Google Scholar 

  18. Hogan N, Sternad D (2007) On rhythmic and discrete movements: reflections, definitions and implications for motor control. Exp Brain Res 181:13–30

    Article  PubMed  Google Scholar 

  19. Hughlings Jackson J (1889) On the comparative stuy of disease of the nervous system. Brit Med J 355–362

  20. Johnston JA, Bobich LR, Santello M (2010) Coordination of intrinsic and extrinsic hand muscle activity as a function of wrist joint angle during two-digit grasping. Neurosci Lett 474:104–108

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. Kang N, Shinohara M, Zatsiorsky VM, Latash ML (2004) Learning multi-finger synergies: an uncontrolled manifold analysis. Exp Brain Res 157:336–350

    Article  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  23. Landsmeer JMF, Long C (1965) The mechanism of finger control, based on electromyograms and location analysis. Acta Anat 60:330–347

    CAS  Article  PubMed  Google Scholar 

  24. Latash ML (2008) Synergy. Oxford University Press, New York

    Google Scholar 

  25. Latash ML (2010) Motor synergies and the equilibrium-point hypothesis. Mot Control 14:294–322

    Article  Google Scholar 

  26. Latash ML (2012) The bliss (not the problem) of motor abundance (not redundancy). Exp Brain Res 217:1–5

    Article  PubMed  PubMed Central  Google Scholar 

  27. Latash ML (2016) Towards physics of neural processes and behavior. Neurosci Biobehav Rev 69:136–146

    Article  PubMed  PubMed Central  Google Scholar 

  28. Latash ML (2017) Biological movement and laws of physics. Mot Control 21:327–344

    Article  Google Scholar 

  29. Latash ML, Zatsiorsky VM (1993) Joint stiffness: myth or reality? Hum Move Sci 12:653–692

    Article  Google Scholar 

  30. Latash ML, Zatsiorsky VM (2016) Biomechanics and motor control: defining central concepts. Academic Press, New York, NY

    Google Scholar 

  31. Latash ML, Scholz JF, Danion F, Schöner G (2001) Structure of motor variability in marginally redundant multi-finger force production tasks. Exp Brain Res 141:153–165

    CAS  Article  PubMed  Google Scholar 

  32. Latash ML, Scholz JF, Danion F, Schöner G (2002) Finger coordination during discrete and oscillatory force production tasks. Exp Brain Res 146:412–432

    Google Scholar 

  33. Latash ML, Shim JK, Smilga AV, Zatsiorsky V (2005) A central back-coupling hypothesis on the organization of motor synergies: a physical metaphor and a neural model. Biol Cybern 92:186–191

    Article  PubMed  PubMed Central  Google Scholar 

  34. Latash ML, Scholz JP, Schöner G (2007) Toward a new theory of motor synergies. Mot Control 11:275–307

    Google Scholar 

  35. Leone FC, Nottingham RB, Nelson LS (1961) The folded normal distribution. Technometrics 3:543–550

    Article  Google Scholar 

  36. Li ZM, Latash ML, Zatsiorsky VM (1998) Force sharing among fingers as a model of the redundancy problem. Exp Brain Res 119:276–286

    CAS  Article  PubMed  Google Scholar 

  37. Li ZM, Zatsiorsky VM, Latash ML (2000) Contribution of the extrinsic and intrinsic hand muscles to the moments in finger joints. Clin Biomech 15:203–211

    CAS  Article  Google Scholar 

  38. Li S, Danion F, Latash ML, Li Z-M, Zatsiorsky VM (2001) Bilateral deficit and symmetry in finger force production during two-hand multi-finger tasks. Exp Brain Res 141:530–540

    CAS  Article  PubMed  Google Scholar 

  39. Li Z-M, Zatsiorsky VM, Latash ML, Bose NK (2002) Anatomically and experimentally based neural networks modelling force coordination in static multi-finger tasks. Neurocomputing 47:259–275

    CAS  Article  Google Scholar 

  40. Long C (1965) Intrinsic-extrinsic muscle control of the fingers. J Bone Joint Surg 50A:973–984

    Google Scholar 

  41. Martin V, Scholz JP, Schöner G (2009) Redundancy, self-motion, and motor control. Neural Comput 21:1371–1414

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  42. Mattos D, Latash ML, Park E, Kuhl J, Scholz JP (2011) Unpredictable elbow joint perturbation during reaching results in multijoint motor equivalence. J Neurophysiol 106:1424–1436

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  43. Olafsdottir H, Yoshida N, Zatsiorsky VM, Latash ML (2005) Anticipatory covariation of finger forces during self-paced and reaction time force production. Neurosci Lett 381:92–96

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  44. Rearick MP, Casares A, Santello M (2003) Task-dependent modulation of multi-digit force coordination patterns. J Neurophysiol 89:1317–1326

    Article  PubMed  Google Scholar 

  45. Reschechtko S, Latash ML (2017) Stability of hand force production: I. Hand level control variables and multi-finger synergies. J Neurophysiol 118:3152–3164

    Article  PubMed  Google Scholar 

  46. Schieber MH, Santello M (2004) Hand function: peripheral and central constraints on performance. J Appl Physiol 96:2293–2300

    Article  PubMed  Google Scholar 

  47. Scholz JP, Schöner G (1999) The uncontrolled manifold concept: identifying control variables for a functional task. Exp Brain Res 126:289–306

    CAS  Article  PubMed  Google Scholar 

  48. Scholz JP, Danion F, Latash ML, Schöner G (2002) Understanding finger coordination through analysis of the structure of force variability. Biol Cybern 86:29–39

    Article  PubMed  Google Scholar 

  49. Schöner G (1995) Recent developments and problems in human movement science and their conceptual implications. Ecol Psychol 8:291–314

    Article  Google Scholar 

  50. Shaklai S, Minouni-Blouch A, Levin M, Friedman J (2017) Development of finger force coordination in children. Exp Brain Res 235:3709–3720

    CAS  Article  PubMed  Google Scholar 

  51. Shim JK, Olafsdottir H, Zatsiorsky VM, Latash ML (2005) The emergence and disappearance of multi-digit synergies during force production tasks. Exp Brain Res 164:260–270

    Article  PubMed  PubMed Central  Google Scholar 

  52. Shinohara M, Latash ML, Zatsiorsky VM (2003) Age effects on force production by the intrinsic and extrinsic hand muscles and finger interaction during maximal contraction tasks. J Appl Physiol 95:1361–1369

    Article  PubMed  Google Scholar 

  53. Shinohara M, Scholz JP, Zatsiorsky VM, Latash ML (2004) Finger interaction during accurate multi-finger force production tasks in young and elderly persons. Exp Brain Res 156:282–292

    Article  PubMed  Google Scholar 

  54. Slobounov S, Chiang H, Johnston J, Ray W (2002) Modulated cortical control of individual fingers in experienced musicians: an EEG study. Electroencephalographic study. Clin Neurophysiol 113:2013–2024

    CAS  Article  PubMed  Google Scholar 

  55. Solnik S, Pazin N, Coelho CJ, Rosenbaum DA, Scholz JP, Zatsiorsky VM, Latash ML (2013) End-state comfort and joint configuration variance during reaching. Exp Brain Res 225(3):431–442

    Article  PubMed  PubMed Central  Google Scholar 

  56. Sternad D, Dean WJ (2003) Rhythmic and discrete elements in multi-joint coordination. Brain Res 989:152–171

    CAS  Article  PubMed  Google Scholar 

  57. Vaillancourt DE, Russell DM (2002) Temporal capacity of short-term visuomotor memory in continuous force production. Exp Brain Res 145:275–285

    Article  PubMed  Google Scholar 

  58. Winges SA, Santello M (2004) Common input to motor units of digit flexors during multi-digit grasping. J Neurophysiol 92:3210–3220

    Article  PubMed  Google Scholar 

  59. Wu Y-H, Latash ML (2014) The effects of practice on coordination. Exer Sport Sci Rev 42:37–42

    Article  Google Scholar 

  60. Xu J, Ejaz N, Hertler B, Branscheidt M, Widmer M, Faria AV, Harran MD, Cortes JC, Kim N, Celnik PA, Kitago T, Luft AR, Krakauer JW, Diedrichsen J (2017) Separable systems for recovery of finger strength and control after stroke. J Neurophysiol 118:1151–1163

    Article  PubMed  Google Scholar 

  61. Zatsiorsky VM, Latash ML (2008) Multi-finger prehension: an overview. J Mot Behav 40:446–476

    Article  PubMed  PubMed Central  Google Scholar 

  62. Zatsiorsky VM, Li Z-M, Latash ML (1998) Coordinated force production in multi-finger tasks: finger interaction and neural network modeling. Biol Cybern 79(2):139–150

    CAS  Article  PubMed  Google Scholar 

  63. Zatsiorsky VM, Li ZM, Latash ML (2000) Enslaving effects in multi-finger force production. Exp Brain Res 131:187–195

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgements

The study was in part supported by NIH grant NS095873.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Mark L. Latash.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Cuadra, C., Bartsch, A., Tiemann, P. et al. Multi-finger synergies and the muscular apparatus of the hand. Exp Brain Res 236, 1383–1393 (2018). https://doi.org/10.1007/s00221-018-5231-5

Download citation

Keywords

  • Hand
  • Finger
  • Synergy
  • Uncontrolled manifold
  • Referent coordinate
  • Motor equivalence
  • Anticipatory synergy adjustment