Skip to main content
Log in

Optimality and stability of intentional and unintentional actions: II. Motor equivalence and structure of variance

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

We address the nature of unintentional changes in performance in two papers. This second paper tested hypotheses related to stability of task-specific performance variables estimated using the framework of the uncontrolled manifold (UCM) hypothesis. Our first hypothesis was that selective stability of performance variables would be observed even when the magnitudes of those variables drifted unintentionally because of the lack of visual feedback. Our second hypothesis was that stability of a variable would depend on the number of explicit task constraints. Subjects performed four-finger isometric pressing tasks that required the accurate production of a combination of total moment and total force with natural or modified finger involvement under full visual feedback, which was removed later for some or all of the salient variables. We used inter-trial analysis of variance and drifts in the space of finger forces within the UCM and within the orthogonal to the UCM space. The two variance components were used to estimate a synergy index stabilizing the force/moment combination, while the two drift components were used to estimate motor equivalent and non-motor equivalent force changes, respectively. Without visual feedback, both force and moment drifted toward lower absolute magnitudes. The non-motor equivalent component of motion in the finger force space was larger than the motor equivalent component for variables that stopped receiving visual feedback. In contrast, variables that continued to receive visual feedback showed larger motor equivalent component, compared to non-motor equivalent component, over the same time interval. These data falsified the first hypothesis; indeed, selective stabilization of a variable over the duration of a trial allows expecting comparably large motor equivalent components both with and without visual feedback. Adding a new constraint (presented as a target magnitude of middle finger force) resulted in a drop in the synergy index in support of the second hypothesis. We interpret the force drift as a natural relaxation process toward states with lower potential energy in the physical (physiological) system involved in the task. The results show that presenting sensory feedback on a performance variable makes synergies stabilizing that variable dependent on that particular sensory feedback.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • 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 (2016) Unsteady steady-states: central causes of unintentional force drift. Exp Brain Res (in press)

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

    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  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 

  • Diedrichsen J (2007) Optimal task-dependent changes of bimanual feedback control and adaptation. Curr Biol 17:1675–1679

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Diedrichsen J, Shadmehr R, Ivry RB (2010) The coordination of movement: optimal feedback control and beyond. Trends Cogn Sci 14:31–39

    Article  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 movement science. Mot Control 2:306–313

    Article  CAS  Google Scholar 

  • Hammond PH (1954) Involuntary activity in biceps following the sudden application of velocity to the abducted forearm. J Physiol 127:23P–25P

    Google Scholar 

  • Harris CM, Wolpert DM (1998) Signal-dependent noise determines motor planning. Nature 394:780–784

    Article  CAS  PubMed  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 

  • 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. Neuroscience 319:194–205

    Article  CAS  PubMed  Google Scholar 

  • Kugler PN, Turvey MT (1987) Information, natural law, and the self-assembly of rhythmic movement. Erlbaum, Hillsdale

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

    Article  PubMed  Google Scholar 

  • Latash ML, Huang X (2015) Neural control of movement stability: lessons from studies of neurological patients. Neuroscience 301:39–48

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

    Article  CAS  PubMed  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 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 

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

    Article  Google Scholar 

  • Latash ML, Levin MF, Scholz JP, Schöner G (2010) Motor control theories and their applications. Medicina 46:382–392

    PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  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, Kuhl J, Scholz JP, Latash ML (2013) Motor equivalence (ME) during reaching: is ME observable at the muscle level? Mot Control 17:145–175

    Article  Google Scholar 

  • Mattos D, Schöner G, Zatsiorsky VM, Latash ML (2015) Motor equivalence during accurate multi-finger force production. Exp Brain Res 233:487–502

    Article  PubMed  Google Scholar 

  • Newell KM, Carlton LG (1993) Force variability in isometric responses. J Exp Psychol Hum Percept Perform 14:37–44

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park J, Zatsiorsky VM, Latash ML (2010) Optimality vs. variability: An example of multi-finger redundant tasks. Exp Brain Res 207:119–132

    Article  PubMed  PubMed Central  Google Scholar 

  • Park J, Wu Y-H, Lewis MM, Huang X, Latash ML (2012) Changes in multi-finger interaction and coordination in Parkinson’s disease. J Neurophysiol 108:915–924

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 116:698–708

    Article  PubMed  Google Scholar 

  • Parsa B, Terekhov A, Zatsiorsky VM, Latash ML (2017) Optimality and stability of intentional and unintentional actions: I. Origins of drifts in performance. Exp Brain Res (the companion paper)

  • Ranganathan R, Newell KM (2008) Motor synergies: feedback and error compensation within and between trials. Exp Brain Res 186:561–570

    Article  PubMed  Google Scholar 

  • Ranganathan R, Newell KM (2009) Influence of augmented feedback on coordination strategies. J Mot Behav 41:317–330

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Scholz JP, Schöner G (2014) Use of the uncontrolled manifold (UCM) approach to understand motor variability, motor equivalence, and self-motion. Adv Exp Med Biol 826:91–100

    Article  PubMed  Google Scholar 

  • Scholz JP, Schöner G, Latash ML (2000) Identifying the control structure of multijoint coordination during pistol shooting. Exp Brain Res 135:382–404

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Scholz JP, Dwight-Higgin T, Lynch JE, Tseng YW, Martin V, Schöner G (2011) Motor equivalence and self-motion induced by different movement speeds. Exp Brain Res 209:319–332

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • Shemmel J, Krutky MA, Perreault EJ (2010) Stretch sensitive reflexes as an adaptive mechanism for maintaining limb stability. Clin Neurophysiol 121:1680–1689

    Article  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 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Tatton WG, Bawa P, Bruce IC, Lee RG (1978) Long loop reflexes in monkeys: an interpretive base for human reflexes. Prog Clin Neurophysiol 4:229–245

    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 

  • Todorov E, Jordan MI (2002) Optimal feedback control as a theory of motor coordination. Nat Neurosci 5:1226–1235

    Article  CAS  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 

  • Venkadesan M, Guckenheimer J, Valero-Cuevas FJ (2007) Manipulating the edge of instability. J Biomech 40:1653–1661

    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. Neuroscience 289:181–193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We are very much grateful to Dr. Satyajit Ambike for the productive discussions at early stages of this project. The study was in part supported by NIH Grants NS035032 and AR048563.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mark L. Latash.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Parsa, B., Zatsiorsky, V.M. & Latash, M.L. Optimality and stability of intentional and unintentional actions: II. Motor equivalence and structure of variance. Exp Brain Res 235, 457–470 (2017). https://doi.org/10.1007/s00221-016-4806-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-016-4806-2

Keywords

Navigation