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Stability of vertical posture explored with unexpected mechanical perturbations: synergy indices and motor equivalence

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Abstract

We explored the relations between indices of mechanical stability of vertical posture and synergy indices under unexpected perturbations. The main hypotheses predicted higher posture-stabilizing synergy indices and higher mechanical indices of center of pressure stability during perturbations perceived by subjects as less challenging. Healthy subjects stood on a force platform and held in fully extended arms a bar attached to two loads acting downward and upward. One of the loads was unexpectedly released by the experimenter causing a postural perturbations. In different series, subjects either knew or did not know which of the two loads would be released. Forward perturbations were perceived as more challenging and accompanied by co-activation patterns among the main agonist–antagonist pairs. Backward perturbation led to reciprocal muscle activation patterns and was accompanied by indices of mechanical stability and of posture-stabilizing synergy which indicated higher stability. Changes in synergy indices were observed as early as 50–100 ms following the perturbation reflecting involuntary mechanisms. In contrast, predictability of perturbation direction had weak or no effect on mechanical and synergy indices of stability. These observations are interpreted within a hierarchical scheme of synergic control of motor tasks and a hypothesis on the control of movements with shifts of referent coordinates. The findings show direct correspondence between stability indices based on mechanics and on the analysis of multi-muscle synergies. They suggest that involuntary posture-stabilizing mechanisms show synergic organization. They also show that predictability of perturbation direction has strong effects on anticipatory postural adjustment but not corrective adjustments. We offer an interpretation of co-activation patterns that questions their contribution to postural stability.

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References

  • Alexander MR (2002) Energetics and optimization of human walking and running: the 2000 Raymond Pearl memorial lecture. Am J Hum Biol 14:641–648

    Article  Google Scholar 

  • Ambike SS, Tillman M (2017) Cue-induced changes in the stability of finger force-production tasks revealed by the uncontrolled-manifold analysis. J Neurophysiol. https://doi.org/10.1152/jn.00519.2017

    PubMed  Google Scholar 

  • Arias P, Espinosa N, Robles-García V, Cao R, Cudeiro J (2012) Antagonist muscle co-activation during straight walking and its relation to kinematics: insight from young, elderly and Parkinson’s disease. Brain Res 1455:124–131

    Article  CAS  PubMed  Google Scholar 

  • Aruin AS, Almeida GL (1996) A coactivation strategy in anticipatory postural adjustments in persons with down syndrome. Mot Control 1:178–191

    Article  Google Scholar 

  • Aruin AS, Latash ML (1995) Directional specificity of postural muscles in feed-forward postural reactions during fast voluntary arm movements. Exp Brain Res 103:323–332

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Chen B, Lee YJ, Aruin AS (2015) Anticipatory and compensatory postural adjustments in conditions of body asymmetry induced by holding an object. Exp Brain Res 233:3087–3096

    Article  PubMed  PubMed Central  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 

  • Crowninshield RD, Brand RA (1981) A physiologically based criterion of muscle force prediction in locomotion. J Biomech 14:793–801

    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  PubMed  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

    Article  PubMed  Google Scholar 

  • Danna-Dos-Santos A, Degani AM, Latash ML (2008) Flexible muscle modes and synergies in challenging whole-body tasks. Exp Brain Res 189:171–187

    Article  PubMed  PubMed Central  Google Scholar 

  • Dean JC, Alexander NB, Kuo AD (2007) The effect of lateral stabilization on walking in young and old adults. IEEE Trans Biomed Eng 54:1919–1926

    Article  CAS  PubMed  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 

  • 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

    Article  PubMed  Google Scholar 

  • 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 

  • 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, NY

    Book  Google Scholar 

  • Foisy M, Feldman AG (2006) Threshold control of arm posture and movement adaptation to load. Exp Brain Res 175:726–744

    Article  PubMed  Google Scholar 

  • Forghani A, Preuss R, Milner T (2017a) Postural response characterization of standing humans to multi-directional, predictable and unpredictable perturbations to the arm. J Electromyogr Kinesiol 32:83–92

    Article  PubMed  Google Scholar 

  • Forghani A, Preuss R, Milner TE (2017b) Effects of amplitude and predictability of perturbations to the arm on anticipatory and reactionary muscle responses to maintain balance. J Electromyogr Kinesiol 35:30–39

    Article  PubMed  Google Scholar 

  • Forghani A, Preuss R, Milner TE (2017c) Short-latency muscle response patterns to multi-directional, unpredictable perturbations to balance applied to the arm are context dependent. Neurosci 352:170–179

    Article  CAS  Google Scholar 

  • Gatts S (2008) Neural mechanisms underlying balance control in Tai Chi. Med Sport Sci 52:87–103

    Article  PubMed  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 

  • Gilles M, Wing AM, Kirker SG (1999) Lateral balance organisation in human stance in response to a random or predictable perturbation. Exp Brain Res 124:137–144

    Article  CAS  PubMed  Google Scholar 

  • Habib Perez O, Singer JC, Mochizuki G (2016) The effects of predictability on inter-limb postural synchronization prior to bouts of postural instability. Gait Posture 46:167–172

    Article  PubMed  Google Scholar 

  • Hair JF, Anderson RE, Tatham RL, Black WC (1995) Factor analysis. In: Borkowski D (ed) Multivariate data analysis. Prentice Hall, Englewood Cliffs, pp 364–404

    Google Scholar 

  • Hughlings Jackson J (1889) On the comparative stuy of disease of the nervous system. Br Med J 17:355–362

    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 

  • Jones SL, Henry SM, Raasch CC, Hitt JR, Bunn JY (2008) Responses to multi-directional surface translations involve redistribution of proximal versus distal strategies to maintain upright posture. Exp Brain Res 187:407–417

    Article  PubMed  Google Scholar 

  • Kaiser HF (1960) The application of electronic computers to factor analysis. Educ Psychol Meas 20:141–151

    Article  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

    Article  PubMed  PubMed Central  Google Scholar 

  • Krishnamoorthy V, Goodman SR, Latash ML, Zatsiorsky VM (2003a) Muscle synergies during shifts of the center of pressure by standing persons: identification of muscle modes. Biol Cybern 89:152–161

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Krishnamoorthy V, Latash ML, Scholz JP, Zatsiorsky VM (2004) Muscle modes during shifts of the center of pressure by standing persons: effects of instability and additional support. Exp Brain Res 157:18–31

    Article  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

    Article  PubMed  PubMed Central  Google Scholar 

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

    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  PubMed Central  Google Scholar 

  • Latash ML (2018) Muscle co-activation: definitions, mechanisms, and functions. J Neurophysiol (in press)

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

    Article  Google Scholar 

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

    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 

  • Lee YJ, Aruin AS (2014) Isolated and combined effects of asymmetric stance and pushing movement on the anticipatory and compensatory postural control. Clin Neurophysiol 125:768–776

    Article  PubMed  Google Scholar 

  • Lee PJ, Rogers EL, Granata KP (2006) Active trunk stiffness increases with co-contraction. J Electromyogr Kinesiol 216:51–57

    Article  Google Scholar 

  • Lee YJ, Chen B, Aruin AS (2015) Older adults utilize less efficient postural control when performing pushing task. J Electromyogr Kinesiol 25:966–972

    Article  PubMed  PubMed Central  Google Scholar 

  • Loeb GE (1999) What might the brain know about muscles, limbs and spinal circuits? Prog Brain Res 123:405–409

    Article  CAS  PubMed  Google Scholar 

  • Mari S, Serrao M, Casali C, Conte C, Martino G, Ranavolo A, Coppola G, Draicchio F, Padua L, Sandrini G, Pierelli F (2014) Lower limb antagonist muscle co-activation and its relationship with gait parameters in cerebellar ataxia. Cerebellum 13:226–236

    Article  CAS  PubMed  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 

  • Massion J (1992) Movement, posture and equilibrium—interaction and coordination. Prog Neurobiol 38:35–56

    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, 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 

  • Maurer C, Mergner T, Peterka RJ (2006) Multisensory control of human upright stance. Exp Brain Res 171(2):231– 250

    Article  CAS  PubMed  Google Scholar 

  • Mergner T (2007) Modeling sensorimotor control of human upright stance. Prog Brain Res 165:283–297

    Article  PubMed  Google Scholar 

  • Mergner T, Maurer C, Peterka RJ (2003) A multisensory posture control model of human upright stance. Prog Brain Res 142:189–201

    Article  CAS  PubMed  Google Scholar 

  • Nashner LM, Shupert CL, Horak FB, Black FO (1989) Organization of posture controls: an analysis of sensory and mechanical constraints. Prog Brain Res 80:411–418

    Article  CAS  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Piscitelli D, Falaki A, Solnik S, Latash ML (2017) Anticipatory postural adjustments and anticipatory synergy adjustments: preparing to a postural perturbation with predictable and unpredictable direction. Exp Brain Res 235:713–730

    Article  PubMed  Google Scholar 

  • Prilutsky BI, Zatsiorsky VM (2002) Optimization-based models of muscle coordination. Exer Sport Sci Rev 30:32–38

    Article  Google Scholar 

  • Raptis H, Burtet L, Forget R, Feldman AG (2010) Control of wrist position and muscle relaxation by shifting spatial frames of reference for motoneuronal recruitment: possible involvement of corticospinal pathways. J Physiol 588:1551–1570

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santos MJ, Kanekar N, Aruin AS (2010) The role of anticipatory postural adjustments in compensatory control of posture: 1. Electromyographic analysis. J Electromyogr Kinesiol 20:388–397

    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, 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

    Article  CAS  PubMed  Google Scholar 

  • Slijper H, Latash ML (2000) The effects of instability and additional hand support on anticipatory postural adjustments in leg, trunk, and arm muscles during standing. Exp Brain Res 135:81–93

    Article  CAS  PubMed  Google Scholar 

  • Slijper HP, Latash ML (2004) The effects of muscle vibration on anticipatory postural adjustments. Brain Res 1015:57–72

    Article  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 

  • 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. Nature Neurosci 5:1226–1235

    Article  CAS  PubMed  Google Scholar 

  • Torres-Oviedo G, Ting LH (2010) Subject-specific muscle synergies in human balance control are consistent across different biomechanical contexts. J Neurophysiol 103:3084–3098

    Article  PubMed  PubMed Central  Google Scholar 

  • Toussaint HM, Michies YM, Faber MN, Commissaris DA, van Dieën JH (1998) Scaling anticipatory postural adjustments dependent on confidence of load estimation in a bi-manual whole-body lifting task. Exp Brain Res 120:85–94

    Article  CAS  PubMed  Google Scholar 

  • Tresch MC, Jarc A (2009) The case for and against muscle synergies. Curr Opin Neurobiol 19:601–607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uno Y, Kawato M, Suzuki R (1989) Formation and control of optimal trajectory in human multijoint arm movement. Biol Cybern 61:89–101

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Zatsiorsky VM, Latash ML (2006) Muscle synergies in preparation to a step made under self-paced and reaction-time instructions. Clin Neurophysiol 117:41–56

    Article  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

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The study was in part supported by an NIH Grant R21 NS095873.

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Correspondence to Mark L. Latash.

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Yamagata, M., Falaki, A. & Latash, M.L. Stability of vertical posture explored with unexpected mechanical perturbations: synergy indices and motor equivalence. Exp Brain Res 236, 1501–1517 (2018). https://doi.org/10.1007/s00221-018-5239-x

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  • DOI: https://doi.org/10.1007/s00221-018-5239-x

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