Abstract
We explored two aspects of feed-forward postural control, anticipatory postural adjustments (APAs) and anticipatory synergy adjustments (ASAs) seen prior to self-triggered unloading with known and unknown direction of the perturbation. In particular, we tested two main hypotheses predicting contrasting changes in APAs and ASAs. The first hypothesis predicted no major changes in ASAs. The second hypothesis predicted delayed APAs with predominance of co-contraction patterns when perturbation direction was unknown. Healthy subjects stood on the force plate and held a bar with two loads acting in the forward and backward directions. They pressed a trigger that released one of the loads causing a postural perturbation. In different series, the direction of the perturbation was either known (the same load released in all trials) or unknown (the subjects did not know which of the two loads would be released). Surface electromyograms were recorded and used to quantify APAs, synergies stabilizing center of pressure coordinate (within the uncontrolled manifold hypothesis), and ASA. APAs and ASAs were seen in all conditions. APAs were delayed, and predominance of co-contraction patterns was seen under the conditions with unpredictable direction of perturbation. In contrast, no significant changes in synergies and ASAs were seen. Overall, these results show that feed-forward control of vertical posture has two distinct components, reflected in APAs and ASAs, which show qualitatively different adjustments with changes in predictability of the direction of perturbation. These results are interpreted within the recently proposed hierarchical scheme of the synergic control of motor tasks. The observations underscore the complexity of the feed-forward postural control, which involves separate changes in salient performance variables (such as coordinate of the center of pressure) and in their stability properties.
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References
Aimola E, Santello M, La Grua G, Casabona A (2011) Anticipatory postural adjustments in reach-to-grasp: effect of object mass predictability. Neurosci Lett 502:84–88
Akulin VM, Carlier F, Solnik S, Latash ML (2015) Neural control of redundant (abundant) systems as algorithms stabilizing subspaces. Preprint: arXiv:1506.06920
Alexandrov AV, Frolov AA, Massion J (2001) Biomechanical analysis of movement strategies in human forward trunk bending. I. Modeling. Biol Cybern 84:425–434
Aruin AS (2002) The organization of anticipatory postural adjustments. J Autom Control 12:31–37
Aruin AS (2003) The effect of changes in the body configuration on anticipatory postural adjustments. Mot Control 7:264–277
Aruin AS, Almeida GL (1997) A coactivation strategy in anticipatory postural adjustment in persons with Down syndrome. Mot Control 2:178–191
Aruin AS, Latash ML (1995) The role of motor action in anticipatory postural adjustments studied with self-induced and externally-triggered perturbations. Exp Brain Res 106:291–300
Aruin AS, Forrest WR, Latash ML (1998) Anticipatory postural adjustments in conditions of postural instability. Electroencephalog Clin Neurophysiol 109:350–359
Asaka T, Wang Y (2011) Feedforward postural muscle modes and multi-mode coordination in mild cerebellar ataxia. Exp Brain Res 210:153–163
Bazalgette D, Zattara M, Bathien N, Bouisset S, Rondot P (1986) Postural adjustments associated with rapid voluntary arm movements in patients with Parkinson’s disease. Adv Neurol 45:371–374
Belenkiy VY, Gurfinkel VS, Pal’tsev YI (1967) Elements of control of voluntary movements. Biofizika 10:135–141
Bernstein NA (1947) On the construction of movements. Medgiz, Moscow
Bouisset S, Zattara M (1987) Biomechanical study of the programming of anticipatory postural adjustments associated with voluntary movement. J Biomech 20:735–742
Braido P, Zhang X (2004) Quantitative analysis of finger motion coordination in hand manipulative and gestic acts. Hum Mov Sci 22:661–678
Chen B, Lee Y-J, Aruin AS (2015) Anticipatory and compensatory postural adjustments in conditions of body asymmetry induced by holding an object. Exp Brain Res 233:3087–3096
Corcos DM, Gottlieb GL, Latash ML, Almeida GL, Agarwal GC (1992) Electromechanical delay: an experimental artifact. J Electromyogr Kinesiol 2:59–68
Cordo PJ, Nashner LM (1982) Properties of postural adjustments associated with rapid arm movements. J Neurophysiol 47:1888–1905
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
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
De Wolf S, Slijper H, Latash ML (1998) Anticipatory postural adjustments during self-paced and reaction-time movements. Exp Brain Res 121:7–19
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
Falaki A, Towhidkhah F, Zhou T, Latash ML (2014) Task-specific stability in muscle activation space during unintentional movements. Exp Brain Res 232:3645–3658
Falaki A, Huang X, Lewis MM, Latash ML (2016) Impaired synergic control of posture in Parkinson’s patients without postural instability. Gait Posture 44:209–215
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, NewYork
Friedman J, SKM V, 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
Gantchev GN, Dimitrova DM (1996) Anticipatory postural adjustments associated with arm movements during balancing on unstable support surface. Int J Psychophysiol 22(1–2):117–122
Gelfand IM, Latash ML (1998) On the problem of adequate language in movement science. Mot Control 2:306–313
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
Hirschfeld H, Forssberg H (1991) Phase-dependent modulations of anticipatory postural activity during human locomotion. J Neurophysiol 66:12–19
Horak FB, Nashner LM (1986) Central programming of postural movements: adaptation to altered support-surface configurations. J Neurophysiol 55:1369–1381
Jerde TE, Soechting JF, Flanders M (2003) Coarticulation in fluent fingerspelling. J Neurosci 23:2383–2393
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
Kanekar N, Aruin AS (2014) The effect of aging on anticipatory postural control. Exp Brain Res 232:1127–1136
Kendall FP, McCreary EK, Provance PG, Rodgers MM, Romani WA (2005) Muscles: testing and function with posture and pain, 5th edn. Lippincott Williams and Wilkins, Baltimore
Klous M, Danna-dos-Santos A, Latash ML (2010) Multi-muscle synergies in a dual postural task: evidence for the principle of superposition. Exp Brain Res 202:457–471
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, Latash ML (2005) Reversals of anticipatory postural adjustments during voluntary sway. J Physiol 565:675–684
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, Hadders-Algra M (2008) What is posture and how is it controlled? In: Hadders-Algra M, Carlberg EB (eds) Posture: a key issue in developmental disorders. MacKeith Press, London, pp 3–21
Latash ML, Huang X (2015) Neural control of movement stability: lessons from studies of neurological patients. Neuroscience 301:39–48
Latash ML, Zatsiorsky VM (1993) Joint stiffness: myth or reality? Hum Mov Sci 12:653–692
Latash ML, Zatsiorsky VM (2016) Biomechanics and motor control: defining central concepts. Academic Press, New York
Latash ML, Scholz JP, Schoner G (2007) Toward a new theory of motor synergies. Mot Control 11:276–308
Lee WA, Buchanan TS, Rogers MW (1987) Effects of arm acceleration and behavioral conditions on the organization of postural adjustments during arm flexion. Exp Brain Res 66:257–270
Massion J (1992) Movement, posture and equilibrium: interaction and coordination. Prog Neurobiol 38:35–56
Massion J (1998) Postural control systems in developmental perspective. Neurosci Biobehav Rev 22:465–472
Nadin M (ed) (2015) Anticipation: learning from the past. The Russian/Soviet contributions to the science of anticipation. Springer, New York
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
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, 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
Piscitelli D (2016) Motor rehabilitation should be based on knowledge of motor control. Arch Physiother 6:5
Ramos CF, Stark LW (1990) Postural maintenance during fast forward bending: a model simulation experiment determines the “reduced trajectory”. Exp Brain Res 82:651–657
Reisman D, Scholz JP (2003) Aspects of joint coordination are preserved during pointing in persons with post-stroke hemiparesis. Brain 126:2510–2527
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
Santos MJ, Kanekar N, Aruin AS (2010) The role of anticipatory postural adjustments in compensatory control of posture: 2. Biomechanical analysis. J Electromyogr Kinesiol 20:398–405
Schmitz C, Martin N, Assaiante C (2002) Building anticipatory postural adjustment during childhood: a kinematic and electromyographic analysis of unloading in children from 4 to 8 years of age. Exp Brain Res 142:354–364
Scholz JP, Schöner G (1999) The uncontrolled manifold concept: identifying control variables for a functional task. Exp Brain Res 126:289–306
Schöner G (1995) Recent developments and problems in human movement science and their conceptual implications. Ecol Psychol 8:291–314
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
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
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
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
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
Woollacott M, Inglin B, Manchester D (1988) Response preparation and posture control. Neuromuscular changes in the older adult. Ann N Y Acad Sci 515:42–53
Zatsiorsky VM, Latash ML, Gao F, Shim JK (2004) The principle of superposition in human prehension. Robotica 22:231–234
Zhou T, Wu Y-H, Bartsch A, Cuadra C, Zatsiorsky VM, Latash ML (2013) Anticipatory synergy adjustments: preparing a quick action in an unknown direction. Exp Brain Res 226:565–573
Acknowledgements
The study was in part supported by an NIH Grant R01 NS035032. We are grateful to Dr. Mu Qiao for his advice on early stages of the project and to Professor C.G. Cerri for facilitating the visit of DP to the Motor Control Laboratory of the Pennsylvania State University.
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Piscitelli, D., Falaki, A., Solnik, S. et al. Anticipatory postural adjustments and anticipatory synergy adjustments: preparing to a postural perturbation with predictable and unpredictable direction. Exp Brain Res 235, 713–730 (2017). https://doi.org/10.1007/s00221-016-4835-x
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DOI: https://doi.org/10.1007/s00221-016-4835-x