Advertisement

Experimental Brain Research

, Volume 236, Issue 6, pp 1545–1562 | Cite as

Stability of steady hand force production explored across spaces and methods of analysis

  • Paulo B. de Freitas
  • Sandra M. S. F. Freitas
  • Mechelle M. Lewis
  • Xuemei Huang
  • Mark L. Latash
Research Article
  • 152 Downloads

Abstract

We used the framework of the uncontrolled manifold (UCM) hypothesis and explored the reliability of several outcome variables across different spaces of analysis during a very simple four-finger accurate force production task. Fourteen healthy, young adults performed the accurate force production task with each hand on 3 days. Small spatial finger perturbations were generated by the “inverse piano” device three times per trial (lifting the fingers 1 cm/0.5 s and lowering them). The data were analyzed using the following main methods: (1) computation of indices of the structure of inter-trial variance and motor equivalence in the space of finger forces and finger modes, and (2) analysis of referent coordinates and apparent stiffness values for the hand. Maximal voluntary force and the index of enslaving (unintentional finger force production) showed good to excellent reliability. Strong synergies stabilizing total force were reflected in both structure of variance and motor equivalence indices. Variance within the UCM and the index of motor equivalent motion dropped over the trial duration and showed good to excellent reliability. Variance orthogonal to the UCM and the index of non-motor equivalent motion dropped over the 3 days and showed poor to moderate reliability. Referent coordinate and apparent stiffness indices co-varied strongly and both showed good reliability. In contrast, the computed index of force stabilization showed poor reliability. The findings are interpreted within the scheme of neural control with referent coordinates involving the hierarchy of two basic commands, the r-command and c-command. The data suggest natural drifts in the finger force space, particularly within the UCM. We interpret these drifts as reflections of a trade-off between stability and optimization of action. The implications of these findings for the UCM framework and future clinical applications are explored in the discussion. Indices of the structure of variance and motor equivalence show good reliability and can be recommended for applied studies.

Keywords

Hand Synergy Variance Motor equivalence Referent coordinate Reliability 

Notes

Acknowledgements

The study was in part supported by NIH Grants NS082151 and NS095873.

References

  1. Ambike S, Mattos D, Zatsiorsky VM, Latash ML (2016) Synergies in the space of control variables within the equilibrium-point hypothesis. Neurosci 315:150–161CrossRefGoogle Scholar
  2. Bernstein NA (1967) The co-ordination and regulation of movements. Pergamon Press, OxfordGoogle Scholar
  3. Cicchetti DV (1994) Guidelines, criteria, and rules of thumb for evaluating normed and standardized assessment instruments in psychology. Psychol Assess 6:284–290CrossRefGoogle Scholar
  4. Corcos DM, Agarwal GC, Flaherty BP, Gottlieb GL (1990) Organizing principles for single-joint movements: IV. Implications for isometric contractions. J Neurophysiol 64:1033–1042CrossRefPubMedGoogle Scholar
  5. 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 88:91–98CrossRefPubMedGoogle Scholar
  6. 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 235:2243–2258CrossRefPubMedGoogle Scholar
  7. 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 11:565–578Google Scholar
  8. Feldman AG (1980) Superposition of motor programs. I. Rhythmic forearm movements in man. Neurosci 5:81–90CrossRefGoogle Scholar
  9. Feldman AG (1986) Once more on the equilibrium-point hypothesis (λ-model) for motor control. J Mot Behav 18:17–54CrossRefPubMedGoogle Scholar
  10. Feldman AG (2015) Referent control of action and perception: challenging conventional theories in behavioral science. Springer, New YorkCrossRefGoogle Scholar
  11. Feldman AG, Orlovsky GN (1972) The influence of different descending systems on the tonic stretch reflex in the cat. Exp Neurol 37:481–494CrossRefPubMedGoogle Scholar
  12. Furmanek M, Solnik S, Piscitelli D, Rasouli O, Falaki A, Latash ML (2017) Synergies and motor equivalence in voluntary sway tasks: the effects of visual and mechanical constraints. J Mot Behav.  https://doi.org/10.1080/00222895.2017.1367642 PubMedGoogle Scholar
  13. Gelfand IM, Latash ML (1998) On the problem of adequate language in movement science. Mot Control 2:306–313CrossRefGoogle Scholar
  14. Gera G, Freitas SM, Scholz JP (2016a) Relationship of diminished interjoint coordination after stroke to hand path consistency. Exp Brain Res 234:741–751CrossRefPubMedGoogle Scholar
  15. Gera G, McGlade KE, Reisman DS, Scholz JP (2016b) Trunk muscle coordination during upward and downward reaching in stroke survivors. Mot Control 20:50–69CrossRefGoogle Scholar
  16. Ghez C, Gordon J (1987) Trajectory control in targeted force impulses. Exp Brain Res 67:225–240CrossRefPubMedGoogle Scholar
  17. Gottlieb GL, Corcos DM, Agarwal GC (1989) Strategies for the control of voluntary movements with one mechanical degree of freedom. Behav Brain Sci 12:189–250CrossRefGoogle Scholar
  18. Jo HJ, Maenza C, Good DC, Huang X, Park J, Sainburg RL, Latash ML (2016) Effects of unilateral stroke on multi-finger synergies and their feed-forward adjustments. Neurosci 319:194–205CrossRefGoogle Scholar
  19. Kang N, Cauraugh JH (2017) Bilateral synergy as an index of force coordination in chronic stroke. Exp Brain Res 235:1501–1509CrossRefPubMedGoogle Scholar
  20. Kang N, Shinohara M, Zatsiorsky VM, Latash ML (2004) Learning multi-finger synergies: an uncontrolled manifold analysis. Exp Brain Res 157:336–350CrossRefPubMedGoogle Scholar
  21. Kapur S, Friedman J, Zatsiorsky VM, Latash ML (2010) Finger interaction in a three-dimensional pressing task. Exp Brain Res 203:101–118CrossRefPubMedPubMedCentralGoogle Scholar
  22. Kilbreath SL, Gandevia SC (1994) Limited independent flexion of the thumb and fingers in human subjects. J Physiol 479:487–497CrossRefPubMedPubMedCentralGoogle Scholar
  23. Koo TK, Li MY (2016) A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropract Med 15:155–163CrossRefGoogle Scholar
  24. Kudo K, Tsutsui S, Ishikura T, Ito T, Yamamoto Y (2000) Compensatory coordination of release parameters in a throwing task. J Mot Behav 32:337–345CrossRefPubMedGoogle Scholar
  25. Latash ML (2010a) Motor synergies and the equilibrium-point hypothesis. Mot Control 14:294–322CrossRefGoogle Scholar
  26. Latash ML (2010b) Stages in learning motor synergies: A view based on the equilibrium-point hypothesis. Hum Move Sci 29:642–654CrossRefGoogle Scholar
  27. Latash ML (2012) The bliss (not the problem) of motor abundance (not redundancy). Exp Brain Res 217:1–5CrossRefPubMedPubMedCentralGoogle Scholar
  28. Latash ML (2016) Towards physics of neural processes and behavior. Neurosci Biobehav Rev 69:136–146CrossRefPubMedPubMedCentralGoogle Scholar
  29. Latash ML (2017) Biological movement and laws of physics. Mot Control 21:327–344CrossRefGoogle Scholar
  30. Latash ML, Gottlieb GL (1991) Reconstruction of elbow joint compliant characteristics during fast and slow voluntary movements. Neurosci 43:697–712CrossRefGoogle Scholar
  31. Latash ML, Huang X (2015) Neural control of movement stability: lessons from studies of neurological patients. Neurosci 301:39–48CrossRefGoogle Scholar
  32. Latash ML, Zatsiorsky VM (2016) Biomechanics and Motor Control: Defining Central Concepts. Academic Press, New YorkGoogle Scholar
  33. Latash ML, Scholz JF, Danion F, Schöner G (2001) Structure of motor variability in marginally redundant multi-finger force production tasks. Exp Brain Res 141:153–165CrossRefPubMedGoogle Scholar
  34. Latash ML, Scholz JP, Schöner G (2007) Toward a new theory of motor synergies. Mot Control 11:275–307Google Scholar
  35. Leone FC, Nottingham RB, Nelson LS (1961) The folded normal distribution. Technometrics 3:543–550CrossRefGoogle Scholar
  36. Li ZM, Latash ML, Zatsiorsky VM (1998) Force sharing among fingers as a model of the redundancy problem. Exp Brain Res 119:276–286CrossRefPubMedGoogle Scholar
  37. Li ZM, Zatsiorsky VM, Latash ML (1999) Contributions of the extrinsic and intrinsic hand muscles to the moments in finger joints. J Clin Biomech 15:203–211CrossRefGoogle Scholar
  38. Li ZM, Zatsiorsky VM, Latash ML (2001) The effect of finger extensor mechanism on the flexor force during isometric tasks. J Biomech 34:1097–1102CrossRefPubMedGoogle Scholar
  39. Martin JR, Budgeon MK, Zatsiorsky VM, Latash ML (2011) Stabilization of the total force in multi-finger pressing tasks studied with the ‘inverse piano’ technique. Hum Mov Sci 30:446–458CrossRefPubMedPubMedCentralGoogle Scholar
  40. Martin JR, Terekhov AA, Latash ML, Zatsiorsky VM (2013) Optimization and variability of motor behavior in multi-finger tasks: What variables does the brain use? J Motor Behav 45:289–305CrossRefGoogle Scholar
  41. Matthews PBC (1959) The dependence of tension upon extension in the stretch reflex of the soleus of the decerebrate cat. J Physiol 47:521–546CrossRefGoogle 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 106:1424–1436CrossRefPubMedPubMedCentralGoogle Scholar
  43. Mattos D, Schöner G, Zatsiorsky VM, Latash ML (2015) Motor equivalence during accurate multi-finger force production. Exp Brain Res 233:487–502CrossRefPubMedGoogle Scholar
  44. Müller H, Sternad D (2003) A randomization method for the calculation of covariation in multiple nonlinear relations: illustrated with the example of goal-directed movements. Biol Cybern 89:22–33PubMedGoogle Scholar
  45. Ohtsuki T (1981) Inhibition of individual fingers during grip strength exertion. Ergonomics 24:21–36CrossRefPubMedGoogle Scholar
  46. Olafsdottir HB, Zatsiorsky VM, Latash ML (2008) The effects of strength training on finger strength and hand dexterity in healthy elderly individuals. J Appl Physiol 105:1166–1178CrossRefPubMedPubMedCentralGoogle Scholar
  47. Park J, Zatsiorsky VM, Latash ML (2010) Optimality vs. variability: an example of multi-finger redundant tasks. Exp Brain Res 207:119–132CrossRefPubMedPubMedCentralGoogle Scholar
  48. Parsa B, O’Shea DJ, Zatsiorsky VM, Latash ML (2016) On the nature of unintentional action: a study of force/moment drifts during multi-finger tasks. J Neurophysiol 116:698–708CrossRefPubMedGoogle Scholar
  49. Prilutsky BI, Zatsiorsky VM (2002) Optimization-based models of muscle coordination. Exer Sport Sci Rev 30:32–38CrossRefGoogle Scholar
  50. Reisman D, Scholz JP (2003) Aspects of joint coordination are preserved during pointing in persons with post-stroke hemiparesis. Brain 126:2510–2527CrossRefPubMedGoogle Scholar
  51. Reschechtko S, Latash ML (2017) Stability of hand force production: I. Hand level control variables and multi-finger synergies. J Neurophysiol 118:3152–3164CrossRefPubMedGoogle Scholar
  52. Reschechtko S, Zatsiorsky VM, Latash ML (2014) Stability of multi-finger action in different spaces. J Neurophysiol 112:3209–3218CrossRefPubMedPubMedCentralGoogle Scholar
  53. Schieber MH, Santello M (2004) Hand function: peripheral and central constraints on performance. J Appl Physiol 96:2293–2300CrossRefPubMedGoogle Scholar
  54. Scholz JP, Schöner G (1999) The uncontrolled manifold concept: Identifying control variables for a functional task. Exp Brain Res 126:289–306CrossRefPubMedGoogle Scholar
  55. Scholz JP, Danion F, Latash ML, Schöner G (2002) Understanding finger coordination through analysis of the structure of force variability. Biol Cybern 86:29–39CrossRefPubMedGoogle Scholar
  56. Scholz JP, Schöner G, Hsu WL, Jeka JJ, Horak F, Martin V (2007) Motor equivalent control of the center of mass in response to support surface perturbations. Exp Brain Res 180:163–179CrossRefPubMedGoogle Scholar
  57. Seif-Naraghi AH, Winters JM (1990) Optimized strategies for scaling goal-directed dynamic limb movements. In: Winters JM, Woo SL-Y (eds) Multiple muscle systems. Biomechanics and movement organization. Springer, New York, pp 312–334CrossRefGoogle Scholar
  58. Shim JK, Lay B, Zatsiorsky VM, Latash ML (2004) Age-related changes in finger coordination in static prehension tasks. J Appl Physiol 97:213–224CrossRefPubMedPubMedCentralGoogle Scholar
  59. Singh T, SKM V, Zatsiorsky VM, Latash ML (2010) Fatigue and motor redundancy: adaptive increase in force variance in multi-finger tasks. J Neurophysiol 103:2990–3000CrossRefPubMedPubMedCentralGoogle Scholar
  60. Tawy GF, Rowe P, Biant L (2018) Gait variability and motor control in patients with knee osteoarthritis as measured by the uncontrolled manifold technique. Gait Posture 59:272–277CrossRefPubMedGoogle Scholar
  61. Tokuda K, Anan M, Takahashi M, Sawada T, Tanimoto K, Kito N, Shinkoda K (2018) Biomechanical mechanism of lateral trunk lean gait for knee osteoarthritis patients. J Biomech 66:10–17CrossRefPubMedGoogle Scholar
  62. Wu Y-H, Latash ML (2014) The effects of practice on coordination. Exerc Sport Sci Rev 42:37–42CrossRefPubMedPubMedCentralGoogle Scholar
  63. Wu Y-H, Pazin N, Zatsiorsky VM, Latash ML (2012) Practicing elements vs. practicing coordination: changes in the structure of variance. J Motor Behav 44:471–478CrossRefGoogle Scholar
  64. Wu Y-H, Pazin N, Zatsiorsky VM, Latash ML (2013) Improving finger coordination in young and elderly persons. Exp Brain Res 226:273–283CrossRefPubMedPubMedCentralGoogle Scholar
  65. Zatsiorsky VM, Latash ML (2008) Multi-finger prehension: An overview. J Mot Behav 40:446–476CrossRefPubMedPubMedCentralGoogle Scholar
  66. Zatsiorsky VM, Li ZM, Latash ML (2000) Enslaving effects in multi-finger force production. Exp Brain Res 131:187–195CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Paulo B. de Freitas
    • 1
    • 2
    • 3
  • Sandra M. S. F. Freitas
    • 2
    • 3
    • 4
  • Mechelle M. Lewis
    • 3
    • 5
  • Xuemei Huang
    • 3
    • 5
    • 6
    • 7
  • Mark L. Latash
    • 2
  1. 1.Interdisciplinary Graduate Program in Healthy SciencesCruzeiro do Sul UniversitySão PauloBrazil
  2. 2.Department of Kinesiology, Rec.Hall-267The Pennsylvania State UniversityUniversity ParkUSA
  3. 3.Department of Neurology, Milton S. Hershey Medical CenterThe Pennsylvania State UniversityHersheyUSA
  4. 4.Graduate Program in Physical TherapyCity University of São PauloSão PauloBrazil
  5. 5.Department of Pharmacology, Milton S. Hershey Medical CenterThe Pennsylvania State UniversityHersheyUSA
  6. 6.Department of Radiology, Milton S. Hershey Medical CenterThe Pennsylvania State UniversityHersheyUSA
  7. 7.Department of Neurosurgery, Milton S. Hershey Medical CenterThe Pennsylvania State UniversityHersheyUSA

Personalised recommendations