Abstract
We examined the control of postural stability in preparation to a discrete, quick whole-body sway toward a target and back to the initial position. Several predictions were tested based on the theory of control with referent body orientation and the notion of multi-muscle synergies stabilizing center of pressure (COP) coordinate. Healthy, young adults performed fast, discrete whole-body motion forward-and-back and backward-and-back under visual feedback on the COP. We used two methods to assess COP stability, analysis of inter-trial variance and analysis of motor equivalence in the muscle activation space. Actions were always preceded by COP counter-movements. Backward COP shifts were faster, and the indices of multi-muscle synergies stabilizing COP were higher prior to those actions. Patterns of muscle activation at the motion onset supported the idea of a gradual shift in the referent body orientation. Prior to the backward movements, there was a trend toward higher muscle co-activation, compared to reciprocal activation. We found strong correlations between the sets of indices of motor equivalence and those of inter-trial variance. Overall, the results support the theory of control with referent coordinates and the idea of multi-muscle synergies stabilizing posture by confirming a number of non-trivial predictions based on these concepts. The findings favor using indices of motor equivalence in clinical studies to minimize the number of trials performed by each subject.
Similar content being viewed by others
References
Akulin VM, Carlier F, Solnik S, Latash ML (2018) Sloppy, but acceptable, control of biological movement: Algorithm-based stabilization of subspaces in abundant spaces. J Hum Kinet. https://doi.org/10.2478/hukin-2018-0086
Belenkiy VY, Gurfinkel VS, Pal’tsev YI (1967) Elements of control of voluntary movements. Biofizika 10:135–141
Bennett DJ, Hollerbach JM, Xu Y, Hunter IW (1992) Time-varying stiffness of human elbow joint during cyclic voluntary movement. Exp Brain Res 88:433–442
Bizzi E, Giszter SF, Loeb E, Mussa-Ivaldi FA, Saltiel P (1995) Modular organization of motor behavior in the frog’s spinal cord. Trends Neurosci 18:442–446
Breniere Y, Do MC (1986) When and how does steady state gait movement induced from upright posture begin? J Biomech 19:1035–1040
Corcos DM, Gottlieb GL, Agarwal GC (1989) Organizing principles for single joint movements. II. A speed-sensitive strategy. J Neurophysiol 62:358–368
Corcos DM, Gottlieb GL, Latash ML, Almeida GL, Agarwal GC (1992) Electromechanical delay: an experimental artifact. J Electromyogr Kinesiol 2:59–68
Crenna P, Frigo C (1991) A motor programme for the initiation of forward-oriented movements in humans. J Physiologie 437:635–653
Criswell E, Cram JR (2011) Cram’s Introduction to Surface Electromyography. Jones and Bartlett, Sudbury
Cuadra C, Bartsch A, Tiemann P, Reschechtko S, Latash ML (2018) Multi-finger synergies and the muscular apparatus of the hand. Exp Brain Res 236:1383–1393
d’Avella A, Bizzi E (2005) Shared and specific muscle synergies in natural motor behaviors. Proc Nat Acad Sci USA 102:3076–3081
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
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
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
De Freitas PB, Freitas SMSF, Lewis MM, Huang X, Latash ML (2018) Stability of steady hand force production explored across spaces and methods of analysis. Exp Brain Res 236:1545–1562
Diedrichsen J, Shadmehr R, Ivry RB (2010) The coordination of movement: optimal feedback control and beyond. Trends Cogn Sci 14:31–39
Duarte M, Freitas SMSF (2005) Speed-accuracy trade-off in voluntary postural movements. Mot Control 9:180–196
Falaki A, Huang X, Lewis MM, Latash ML (2016) Impaired synergic control of posture in Parkinson’s patients without postural instability. Gait Posture 44:209–216
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
Falaki A, Jo HJ, Lewis MM, O’Connell B, De Jesus S, McInerney J, Huang X, Latash ML (2018) Systemic effects of deep brain stimulation on synergic control in Parkinson’s disease. Clin Neurophysiol 129:1320–1332
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
Feldman AG (1986) Once more on the equilibrium-point hypothesis (λ-model) for motor control. J Mot Behav 18:17–54
Feldman AG (2015) Referent control of action and perception: Challenging conventional theories in behavioral science. Springer, New York
Freitas SMSF, de Freitas PB, Lewis MM, Huang X, Latash ML (2019) Quantitative analysis of multi-element synergies stabilizing performance: Comparison of three methods with respect to their use in clinical studies. Exp Brain Res 237:453–465
Frysinger RC, Bourbonnais D, Kalaska JF, Smith AM (1984) Cerebellar cortical activity during antagonist cocontraction and reciprocal inhibition of forearm muscles. J Neurophysiol 51:32–49
Gottlieb GL, Corcos DM, Agarwal GC (1989) Strategies for the control of voluntary movements with one mechanical degree of freedom. Behav Brain Sci 12:189–250
Hafström A, Modig F, Magnusson M, Fransson PA (2014) Effectuation of adaptive stability and postural alignment strategies are decreased by alcohol intoxication. Hum Mov Sci 35:30–49
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
Harris CM, Wolpert DM (1998) Signal-dependent noise determines motor planning. Nature 394:780–784
Hirokawa S, Solomonow M, Luo Z, Lu Y, D’Ambrosia R (1991) Muscular co-contraction and control of knee stability. J Electromyogr Kinesiol 1:199–208
Hogan N, Sternad D (2007) On rhythmic and discrete movements: reflections, definitions and implications for motor control. Exp Brain Res 181:13–30
Ivanenko YP, Poppele RE, Lacquaniti F (2004) Five basic muscle activation patterns account for muscle activity during human locomotion. J Physiol 556:267–282
Kaiser HF (1960) The application of electronic computers to factor analysis. Educ Psychol Meas 20:141–151
Kargo WJ, Ramakrishnan A, Hart CB, Rome LC, Giszter SF (2010) A simple experimentally based model using proprioceptive regulation of motor primitives captures adjusted trajectory formation in spinal frogs. J Neurophysiol 103:573–590
Kawato M (1999) Internal models for motor control and trajectory planning. Curr Opin Neurobiol 9:718–727
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
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
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
Krishnan V, Aruin AS, Latash ML (2011) Two stages and three components of postural preparation to action. Exp Brain Res 212:47–63
Krishnan V, Latash ML, Aruin AS (2012) Early and late components of feed-forward postural adjustments to predictable perturbations. Clin Neurophysiol 123:1016–1026
Latash ML (2008) Synergy. Oxford University Press, New York
Latash ML (2010) Motor synergies and the equilibrium-point hypothesis. Mot Control 14:294–322
Latash ML (2012) The bliss (not the problem) of motor abundance (not redundancy). Exp Brain Res 217:1–5
Latash ML (2016) Towards physics of neural processes and behavior. Neurosci Biobehav Rev 69:136–146
Latash ML (2017) Biological movement and laws of physics. Mot Control 21:327–344
Latash ML (2018) Muscle co-activation: definitions, mechanisms, and functions. J Neurophysiol 120:88–104
Latash ML, Gottlieb GL (1991) Reconstruction of elbow joint compliant characteristics during fast and slow voluntary movements. Neurosci 43:697–712
Latash ML, Huang X (2015) Neural control of movement stability: Lessons from studies of neurological patients. Neurosci 301:39–48
Latash ML, Scholz JP, Schöner G (2002) Motor control strategies revealed in the structure of motor variability. Exer Sport Sci Rev 30:26–31
Latash ML, Scholz JP, Schöner G (2007) Toward a new theory of motor synergies. Mot Control 11:276–308
Leone FC, Nottingham RB, Nelson LS (1961) The folded normal distribution. Technometrics 3:543–550
Massion J (1992) Movement, posture and equilibrium—interaction and coordination. Progs Neurobiol 38:35–56
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
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
Milner TE, Cloutier C (1993) Compensation for mechanically unstable loading in voluntary wrist movement. Exp Brain Res 94:522–532
Mullick AA, Turpin NA, Hsu SC, Subramanian SK, Feldman AG, Levin MF (2018) Referent control of the orientation of posture and movement in the gravitational field. Exp Brain Res 236:381–398
Nielsen JB, Kagamihara Y (1992) The regulation of disynaptic reciprocal Ia inhibition during co-contraction of antagonistic muscles in man. J Physiol 456:373–391
Olafsdottir H, Yoshida N, Zatsiorsky VM, Latash ML (2005) Anticipatory covariation of finger forces during self-paced and reaction time force production. Neurosci Letts 381:92–96
Olafsdottir H, Yoshida N, Zatsiorsky VM, Latash ML (2007) Elderly show decreased adjustments of motor synergies in preparation to action. Clin Biomech 22:44–51
Park J, Lewis MM, Huang X, Latash ML (2014) Dopaminergic modulation of motor coordination in Parkinson’s disease. Parkinsonism Rel Disord 20:64–68
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
Polit A, Bizzi E (1978) Processes controlling arm movements in monkey. Science 201:1235–1237
Rand MK, Van Gemmert AW, Hossain AB, Shimansky YP, Stelmach GE (2012) Control of aperture closure initiation during trunk-assisted reach-to-grasp movements. Exp Brain Res 219:293–304
Robert T, Zatsiorsky VM, Latash ML (2008) Multi-muscle synergies in an unusual postural task: quick shear force production. Exp Brain Res 187:237–253
Scholz JP, Schöner G (1999) The uncontrolled manifold concept: Identifying control variables for a functional task. Exp Brain Res 126:289–306
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
Shadmehr R, Wise SP (2005) The computational neurobiology of reaching and pointing. MIT Press, Cambridge
Shim JK, Olafsdottir H, Zatsiorsky VM, Latash ML (2005) The emergence and disappearance of multi-digit synergies during force production tasks. Exp Brain Res 164:260–270
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
Slijper HP, Latash ML (2004) The effects of muscle vibration on anticipatory postural adjustments. Brain Res 1015:57–72
Tillman M, Ambike S (2018) Cue-induced changes in the stability of finger force-production tasks revealed by the uncontrolled manifold analysis. J Neurophysiol 119:21–32
Ting LH, Macpherson JM (2005) A limited set of muscle synergies for force control during a postural task. J Neurophysiol 93:609–613
Todorov E (2004) Optimality principles in sensorimotor control. Nat Neurosci 7:907–915
Venkadesan M, Guckenheimer J, Valero-Cuevas FJ (2007) Manipulating the edge of instability. J Biomech 40:1653–1661
Wang Y, Zatsiorsky VM, Latash ML (2005) Muscle synergies involved in shifting center of pressure during making a first step. Exp Brain Res 167:196–210
Wang Y, Asaka T, Zatsiorsky VM, Latash ML (2006) Muscle synergies during voluntary body sway: Combining across-trials and within-a-trial analyses. Exp Brain Res 174:679–693
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
Wolpert DM, Miall RC, Kawato M (1998) Internal models in the cerebellum. Trends Cogn Sci 2:338–347
Yamagata M, Falaki A, Latash ML (2018) Effects of voluntary agonist-antagonist co-activation on stability of vertical posture. Mot Control. https://doi.org/10.1123/mc.2018-0038
Zatsiorsky VM, Prilutsky BI (2012) Biomechanics of Skeletal Muscles. Human Kinetics, Urbana
Acknowledgements
The study was supported in part by an NIH grant NS082151. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES) to Nardini—Finance Code 001. Freitas is grateful to CNPq/Brazil.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Nardini, A.G., Freitas, S.M.S.F., Falaki, A. et al. Preparation to a quick whole-body action: control with referent body orientation and multi-muscle synergies. Exp Brain Res 237, 1361–1374 (2019). https://doi.org/10.1007/s00221-019-05510-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-019-05510-5