Skip to main content
SpringerLink
Log in

Motor equivalence and structure of variance: multi-muscle postural synergies in Parkinson’s disease

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

Abstract

We explored posture-stabilizing multi-muscle synergies with two methods of analysis of multi-element, abundant systems: (1) Analysis of inter-cycle variance; and (2) Analysis of motor equivalence, both quantified within the framework of the uncontrolled manifold (UCM) hypothesis. Data collected in two earlier studies of patients with Parkinson’s disease (PD) were re-analyzed. One study compared synergies in the space of muscle modes (muscle groups with parallel scaling of activation) during tasks performed by early-stage PD patients and controls. The other study explored the effects of dopaminergic medication on multi-muscle-mode synergies. Inter-cycle variance and absolute magnitude of the center of pressure displacement across consecutive cycles were quantified during voluntary whole-body sway within the UCM and orthogonal to the UCM space. The patients showed smaller indices of variance within the UCM and motor equivalence compared to controls. The indices were also smaller in the off-drug compared to on-drug condition. There were strong across-subject correlations between the inter-cycle variance within/orthogonal to the UCM and motor equivalent/non-motor equivalent displacements. This study has shown that, at least for cyclical tasks, analysis of variance and analysis of motor equivalence lead to metrics of stability that correlate with each other and show similar effects of disease and medication. These results show, for the first time, intimate links between indices of variance and motor equivalence. They suggest that analysis of motor equivalence, which requires only a handful of trials, could be used broadly in the field of motor disorders to analyze problems with action stability.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  • Almeida QJ, Wishart LR, Lee TD (2002) Bimanual coordination deficits with Parkinson’s disease: the influence of movement speed and external cueing. Mov Disord 17:30–37

    PubMed  Google Scholar 

  • Boonstra TA, van Vugt JPP, van der Kooij H, Bloem BR (2014) Balance asymmetry in Parkinson’s disease and its contribution to freezing of gait. PLoS One 9:e102493

    PubMed  PubMed Central  Google Scholar 

  • Cavanaugh JT, Guskiewicz KM, Stergiou N (2005) A nonlinear dynamic approach for evaluating postural control: new directions for the management of sport-related cerebral concussion. Sports Med 35:935–950

    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

    CAS  PubMed  Google Scholar 

  • Criswell E, Cram JR (2011) Cram’s introduction to surface electromyography, 2nd edn. Jones and Bartlett, Sudbury

    Google Scholar 

  • Danna-Dos-Santos A, Slomka K, Zatsiorsky VM, Latash ML (2007) Muscle modes and synergies during voluntary body sway. Exp Brain Res 179:533–550

    PubMed  Google Scholar 

  • d’Avella A, Bizzi E (2005) Shared and specific muscle synergies in natural motor behaviors. PNAS 102:3076–3081

    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

    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

    PubMed  Google Scholar 

  • Falaki A, Lewis MM, Huang X, Latash ML (2016) Impaired synergic control of posture in Parkinson’s patients without postural instability. Gait Posture 44:209–215

    PubMed  Google Scholar 

  • Falaki A, Huang X, Lewis MM, Latash ML (2017) Dopaminergic modulation of multi-muscle synergies in postural tasks performed by patients with Parkinson’s disease. J Electromyogr Kinesiol 33:20–26

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

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Friedman J, Varadhan SKM, 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

    PubMed  PubMed Central  Google Scholar 

  • Goodman SR, Shim JK, Zatsiorsky VM, Latash ML (2005) Motor variability within a multi-effector system: experimental and analytical studies of multi-finger production of quick force pulses. Exp Brain Res 163:75–85

    PubMed  PubMed Central  Google Scholar 

  • Hausdorff JM, Purdon PL, Peng CK, Ladin Z, Wei JY, Goldberger AL (1985) Fractal dynamics of human gait: stability of long-range correlations in stride interval fluctuations. J Appl Physiol 80:1448–1457

    Google Scholar 

  • Hoehn M, Yahr M (1967) Parkinsonism: onset, progression and mortality. Neurology 17:427–442

    CAS  PubMed  Google Scholar 

  • Houk JC (2005) Agents of the mind. Biol Cybern 92:427–437

    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

    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. Neurosci 319:194–205

    CAS  Google Scholar 

  • King LA, St George RJ, Carlson-Kuhta P, Nutt JG, Horak FB (2010) Preparation for compensatory forward stepping in Parkinson’s disease. Arch Phys Med Rehab 91:1332–1338

    Google Scholar 

  • Klous M, Mikulic P, Latash ML (2011) Two aspects of feed-forward postural control: anticipatory postural adjustments and anticipatory synergy adjustments. J Neurophysiol 105:2275–2288

    PubMed  PubMed Central  Google Scholar 

  • Krishnamoorthy V, Latash ML, Scholz JP, Zatsiorsky VM (2003) Muscle synergies during shifts of the center of pressure by standing persons. Exp Brain Res 152:281–292

    PubMed  Google Scholar 

  • Krishnan V, Aruin AS, Latash ML (2011) Two stages and three components of postural preparation to action. Exp Brain Res 212:47–63

    PubMed  PubMed Central  Google Scholar 

  • Krishnan V, Latash ML, Aruin AS (2012) Early and late components of feed-forward postural adjustments to predictable perturbations. Clin Neurophysiol 123:1016–1026

    PubMed  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  • Latash ML (2017) Biological movement and laws of physics. Mot Control (in press)

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

    CAS  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

    CAS  PubMed  Google Scholar 

  • 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 

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

    Google Scholar 

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

    Google Scholar 

  • Lewis MM, Lee E-Y, Jo HJ, Park J, Latash ML, Huang X (2016) Synergy as a new and sensitive marker of basal ganglia dysfunction: a study of asymptomatic welders. Neurotoxicology 56:76–85

    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

    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

    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

    PubMed  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

    CAS  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

    PubMed  PubMed Central  Google Scholar 

  • Park J, Jo HJ, Lewis MM, Huang X, Latash ML (2013) Effects of Parkinson’s disease on optimization and structure of variance in multi-finger tasks. Exp Brain Res 231:51–63

    PubMed  PubMed Central  Google Scholar 

  • Park J, Lewis MM, Huang X, Latash ML (2014) Dopaminergic modulation of motor coordination in Parkinson’s disease. Parkinsonism Rel Disord 20:64–68

    Google Scholar 

  • Pastor MA, Jahanshahi M, Artieda J, Obeso JA (1992) Performance of repetitive wrist movements in Parkinson’s disease. Brain 115:875–891

    PubMed  Google Scholar 

  • Reisman D, Scholz JP (2003) Aspects of joint coordination are preserved during pointing in persons with post-stroke hemiparesis. Brain 126:2510–2527

    PubMed  Google Scholar 

  • Riva F, Bisi MC, Stagni R (2013) Orbital stability analysis in biomechanics: a systematic review of a nonlinear technique to detect instability of motor tasks. Gait Posture 37:1–11

    CAS  PubMed  Google Scholar 

  • Rogers MW, Kennedy R, Palmer S, Pawar M, Reising M, Martinez KM, Simuni T, Zhang Y, MacKinnon CD (2011) Postural preparation to stepping in patients with Parkinson’s disease. J Neurophysiol 106:915–924

    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

    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

    PubMed  Google Scholar 

  • 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 180:163–179

    CAS  PubMed  Google Scholar 

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

    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

    PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Tomlinson CL, Stowe R, Patel S, Rick C, Gray R, Clarke CE (2010) Systematic review of Levodopa dose equivalency report in Parkinson’s disease. Mov Disord 25:2649–2685

    PubMed  Google Scholar 

  • 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  Google Scholar 

  • van Emmerik RE, Jones SL, Busa MA, Remelius JG, Averill JL (2014) Enhancing postural stability and adaptability in multiple sclerosis. Adv Exp Med Biol 826:251–276

    PubMed  Google Scholar 

  • Visser JE, Carpenter MG, van der Kooij H, Bloem BR (2008) The clinical utility of posturography. Clin Neurophysiol 119:2424–2436

    PubMed  Google Scholar 

  • Wing AM, Keele S, Margolin DI (1984) Motor disorder and the timing of repetitive movements. Ann NY Acad Sci 423:183–192

    CAS  PubMed  Google Scholar 

  • Winter DA, Prince F, Frank JS, Powell C, Zabjek KF (1996) Unified theory regarding A/P and M/L balance in quiet stance. J Neurophysiol 75:2334–2343

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank all the participants in the study. XH and MML were supported by NIH Grants NS060722, ES019672, and NS082151 during the past 12 months. MML also has an internal grant from Penn State University but received no salary support as part of the award. MLL, AF, XH, and MML were supported by NIH Grants NS035032 and NS095873. This publication was also supported, in part, by Grants UL1 TR000127 and TL1 TR000125 from the National Center for Advancing Translational Sciences (NCATS).

Author information

Authors and Affiliations

  1. Department of Kinesiology, The Pennsylvania State University, Rec.Hall-268N, University Park, PA, 16802, USA

    Ali Falaki & Mark L. Latash

  2. Department of Neurology, Pennsylvania State University-Milton S. Hershey Medical Center, Hershey, PA, 17033, USA

    Xuemei Huang & Mechelle M. Lewis

  3. Department of Pharmacology, Pennsylvania State University-Milton S. Hershey Medical Center, Hershey, PA, 17033, USA

    Xuemei Huang & Mechelle M. Lewis

  4. Department of Radiology, Pennsylvania State University-Milton S. Hershey Medical Center, Hershey, PA, 17033, USA

    Xuemei Huang

  5. Department of Neurosurgery, Pennsylvania State University-Milton S. Hershey Medical Center, Hershey, PA, 17033, USA

    Xuemei Huang

Authors
  1. Ali Falaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xuemei Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mechelle M. Lewis
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mark L. Latash
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mark L. Latash.

Ethics declarations

Conflict of interest

No conflicts of interest are claimed by any of the authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Falaki, A., Huang, X., Lewis, M.M. et al. Motor equivalence and structure of variance: multi-muscle postural synergies in Parkinson’s disease. Exp Brain Res 235, 2243–2258 (2017). https://doi.org/10.1007/s00221-017-4971-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-017-4971-y

Keywords

Search

Navigation