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Unsteady steady-states: central causes of unintentional force drift

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Abstract

We applied the theory of synergies to analyze the processes that lead to unintentional decline in isometric fingertip force when visual feedback of the produced force is removed. We tracked the changes in hypothetical control variables involved in single fingertip force production based on the equilibrium-point hypothesis, namely the fingertip referent coordinate (R FT) and its apparent stiffness (C FT). The system’s state is defined by a point in the {R FT; C FT} space. We tested the hypothesis that, after visual feedback removal, this point (1) moves along directions leading to drop in the output fingertip force, and (2) has even greater motion along directions that leaves the force unchanged. Subjects produced a prescribed fingertip force using visual feedback and attempted to maintain this force for 15 s after the feedback was removed. We used the “inverse piano” apparatus to apply small and smooth positional perturbations to fingers at various times after visual feedback removal. The time courses of R FT and C FT showed that force drop was mostly due to a drift in R FT toward the actual fingertip position. Three analysis techniques, namely hyperbolic regression, surrogate data analysis, and computation of motor-equivalent and non-motor-equivalent motions, suggested strong covariation in R FT and C FT stabilizing the force magnitude. Finally, the changes in the two hypothetical control variables {R FT; C FT} relative to their average trends also displayed covariation. On the whole, the findings suggest that unintentional force drop is associated with (a) a slow drift of the referent coordinate that pulls the system toward a low-energy state and (b) a faster synergic motion of R FT and C FT that tends to stabilize the output fingertip force about the slowly drifting equilibrium point.

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References

  • Ambike S, Paclet F, Zatsiorsky VM, Latash ML (2014) Factors affecting grip force: anatomy, mechanics, and referent configurations. Exp Brain Res 232:1219–1231

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 

  • Ambike S, Mattos D, Zatsiorsky VM, Latash ML (2016a) The nature of constant and cyclic force production: unintentional force-drift characteristics. Exp Brain Res 234:197–208

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Babinski F (1899) De l’asynergie cerebelleuse. Rev Neurol 7:806–816

    Google Scholar 

  • Bernstein NA (1947) On the construction of movements. Medgiz, Moscow (in Russian)

    Google Scholar 

  • Bernstein N (1967) The coordination and regulation of movements. Pergamon Press, Oxford

    Google Scholar 

  • Coombes SA, Corcos DM, Vaillancourt DE (2011) Spatiotemporal tuning of brain activity and force performance. Neuroimage 54:2226–2236

    Article  PubMed  Google Scholar 

  • Corcos DM, Gottlieb GL, Latash ML, Almeida GL, Agarwal GC (1992) Electromechanical delay: an experimental artifact. J Electromyogr Kinesiol 2:59–68

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • DeWald JP, Pope PS, Given JD, Buchanan TS, Rymer WZ (1995) Abnormal muscle coactivation patterns during isometric torque generation at the elbow and shoulder in hemiparetic subjects. Brain 118:495–510

    Article  PubMed  Google Scholar 

  • 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 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Book  Google Scholar 

  • Gelfand IM, Latash ML (1998) On the problem of adequate language in motor control. Mot Control 2(4):306–313

    Article  CAS  Google Scholar 

  • Goldman-Rakic PS (1988) Topography of cognition: parallel distributed networks in primate association cortex. Ann Rev Neurosci 11:137–156

    Article  CAS  PubMed  Google Scholar 

  • Gorniak SL, Duarte M, Latash ML (2008) Do synergies improve accuracy? A study of speed-accuracy trade-offs during finger force production. Mot Control 12:151–172

    Article  Google Scholar 

  • Heijnen MJ, Muir BC, Rietdyk S (2012) Factors leading to obstacle contact during adaptive locomotion. Exp Brain Res 223:219–231

    Article  PubMed  Google Scholar 

  • Heijnen MJ, Romine NL, Stumpf DM, Rietdyk S (2014) Memory-guided obstacle crossing: more failures were observed for the trail limb versus lead limb. Exp Brain Res 232:2131–2142

    Article  PubMed  Google Scholar 

  • Hollerbach JM (1982) Computers, brains and the control of movement. Trends Neurosci 6:189–192

    Article  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kawato M (1999) Internal models for motor control and trajectory planning. Curr Opin Neurobiol 9:718–727

    Article  CAS  PubMed  Google Scholar 

  • Latash ML (1994) Reconstruction of equilibrium trajectories and joint stiffness patterns during single-joint voluntary movements under different instructions. Biol Cybern 71:441–450

    Article  CAS  PubMed  Google Scholar 

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

    Book  Google Scholar 

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

    Article  Google Scholar 

  • 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 

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

    Google Scholar 

  • Latash ML, Scholz JP, Schöner G (2002) Motor control strategies revealed in the structure of motor variability. Exerc Sport Sci Rev 30:26–31

    Article  PubMed  Google Scholar 

  • Latash ML, Shim JK, Smilga AV, Zatsiorsky VM (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 

  • Latash ML, Scholz JP, Schoner G (2007) Towards a new theory of motor synergies. Mot Control 11:276–308

    Article  Google Scholar 

  • Martin JR, Budgeon MK, Zatsiorsky VM, Latash ML (2011a) Stabilization of the total force in multi-finger pressing tasks studied with the ‘inverse piano’ technique. Hum Mov Sci 30:446–458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin JR, Zatsiorsky VM, Latash ML (2011b) Multi-finger interaction during involuntary and voluntary single finger force changes. Exp Brain Res 208:423–435

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mattos D, Schoner G, Zatsiorsky VM, Latash ML (2014) Motor equivalence during multi-finger force production. Exp Brain Res 233:487–502

    Article  PubMed  PubMed Central  Google Scholar 

  • Muller H, Sternad D (2003) A randomization method for the calculation of co-variation in multiple nonlinear relations: illustrated with the example of goal-directed movements. Biol Cybern 89:22–33

    PubMed  Google Scholar 

  • Ostry DJ, Feldman AG (2003) A critical evaluation of the force control hypothesis in motor control. Exp Brain Res 153:275–288

    Article  PubMed  Google Scholar 

  • Poon C, Chin-Cottongim LG, Coombes SA, Corcos DM, Vaillancourt DE (2012) Spatiotemporal dynamics of brain activity during the transition from visually guided to memory-guided force control. J Neurophysiol 108:1335–1348

    Article  PubMed  PubMed Central  Google Scholar 

  • Reschechtko S, Zatsiorsky VM, Latash ML (2015) Task-specific stability of multifinger steady-state action. J Mot Behav 47:365–377

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Selemon LD, Goldman-Rakic PS (1988) Common cortical and subcortical targets of the dorsolateral prefrontal and posterior parietal cortices in the rhesus monkey: evidence for a distributed neural network subserving spatially guided behavior. J Neurosci 8:4049–4068

    CAS  PubMed  Google Scholar 

  • Slifkin AB, Vaillancourt DE, Newell KM (2000) Intermittency in the control of continuous force production. J Neurophysiol 84:1708–1718

    CAS  PubMed  Google Scholar 

  • Ting LH, Macpherson JM (2005) A limited set of muscle synergies for force control during a postural task. J Neurophysiol 93:609–613

    Article  PubMed  Google Scholar 

  • 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 

  • Vaillancourt DE, Thulborn K, Corcos DM (2003) Neural basis for the processes that underlie visually guided and internally guided force control in humans. J Neurophysiol 90:3330–3340

    Article  PubMed  Google Scholar 

  • Wilhelm L, Zatsiorsky VM, Latash ML (2013) Equifinality and its violations in a redundant system: multi-finger accurate force production. J Neurophysiol 110:1965–1973

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Zhou T, Solnik S, Wu Y-H, Latash ML (2014) Unintentional movements produced by back-coupling between actual and referent body configurations: violations of equifinality in multi-joint positional tasks. Exp Brain Res 232:3847–3859

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou T, Zhang L, Latash ML (2015) Intentional and unintentional multi-joint movements: their nature and structure of variance. Neurosc 289:181–193

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The study was in part supported by NIH Grants NS-035032 and AR-048563.

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Authors and Affiliations

  1. Department of Health and Kinesiology, Purdue University, 800 West Stadium Ave, West Lafayette, IN, 47907, USA

    Satyajit Ambike

  2. Program in Occupational Therapy, Washington University School of Medicine, Saint Louis, MO, USA

    Daniela Mattos

  3. Department of Kinesiology, The Pennsylvania State University, University Park, PA, USA

    Vladimir M. Zatsiorsky & Mark L. Latash

Authors
  1. Satyajit Ambike
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  2. Daniela Mattos
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  3. Vladimir M. Zatsiorsky
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  4. Mark L. Latash
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Correspondence to Satyajit Ambike.

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Ambike, S., Mattos, D., Zatsiorsky, V.M. et al. Unsteady steady-states: central causes of unintentional force drift. Exp Brain Res 234, 3597–3611 (2016). https://doi.org/10.1007/s00221-016-4757-7

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  • DOI: https://doi.org/10.1007/s00221-016-4757-7

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