Abstract
We used robot-generated perturbations applied during position-holding tasks to explore stability of induced unintentional movements in a multidimensional space of muscle activations. Healthy subjects held the handle of a robot against a constant bias force and were instructed not to interfere with hand movements produced by changes in the external force. Transient force changes were applied leading to handle displacement away from the initial position and then back toward the initial position. Intertrial variance in the space of muscle modes (eigenvectors in the muscle activations space) was quantified within two subspaces, corresponding to unchanged handle coordinate and to changes in the handle coordinate. Most variance was confined to the former subspace in each of the three phases of movement, the initial steady state, the intermediate position, and the final steady state. The same result was found when the changes in muscle activation were analyzed between the initial and final steady states. Changes in the dwell time between the perturbation force application and removal led to different final hand locations undershooting the initial position. The magnitude of the undershot scaled with the dwell time, while the structure of variance in the muscle activation space did not depend on the dwell time. We conclude that stability of the hand coordinate is ensured during both intentional and unintentional actions via similar mechanisms. Relative equifinality in the external space after transient perturbations may be associated with varying states in the redundant space of muscle activations. The results fit a hierarchical scheme for the control of voluntary movements with referent configurations and redundant mapping between the levels of the hierarchy.
Similar content being viewed by others
References
Ambike S, Paclet F, Zatsiorsky VM, Latash ML (2014) Factors affecting grip force: anatomy, mechanics, and referent configurations. Exp Brain Res 232:1219–1231
Asaka T, Wang Y, Fukushima J, Latash ML (2008) Learning effects on muscle modes and multi-mode postural synergies. Exp Brain Res 184:323–338
Bernstein NA (1967) The co-ordination and regulation of movements. Pergamon Press, Oxford
Bizzi E, Polit A, Morasso P (1976) Mechanisms underlying achievement of final head position. J Neurophysiol 39:435–444
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
Danna-Dos-Santos A, Shapkova EYu, Shapkova AL, Degani AM, Latash ML (2009) Postural control during upper body locomotor-like movements: similar synergies built on dissimilar muscle modes. Exp Brain Res 193:565–579
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
Feldman AG (1966) Functional tuning of nervous system with control of movement or maintenance of a steady posture. II. Controllable parameters of the muscles. Biophysics 11:565–578
Feldman AG (1980) Superposition of motor programs. I. Rhythmic forearm movements in man. Neurosci 5:81–90
Feldman AG (1986) Once more on the equilibrium-point hypothesis (lambda model) for motor control. J Mot Behav 18:17–54
Feldman AG (2009) Origin and advances of the equilibrium-point hypothesis. Adv Exp Med Biol 629:637–643
Flash T, Hochner B (2005) Motor primitives in vertebrates and invertebrates. Curr Opin Neurobiol 15:660–666
Gelfand IM, Latash ML (1998) On the problem of adequate language in movement science. Motor Control 2:306–313
Hogan N, Sternad D (2012) Dynamic primitives of motor behavior. Biol Cybern 106:727–739
Ivanenko YP, Poppele RE, Lacquaniti F (2004) Five basic muscle activation patterns account for muscle activity during human locomotion. J Physiol 556:267–282
Ivanenko YP, Cappellini G, Dominici N, Poppele RE, Lacquaniti F (2005) Coordination of locomotion with voluntary movements in humans. J Neurosci 25:7238–7253
Kaiser HF (1960) The application of electronic computers to factor analysis. Educ Psychol Meas 20:141–151
Kelso JA, Holt KG (1980) Exploring a vibratory systems analysis of human movement production. J Neurophysiol 43:1183–1196
Kendall FP, McCreary EK, Provance PG, Rodgers MM, Romani WA (2005) Muscles: testing and function with posture and pain, 5th edn. Lippincott Williams & 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
Krishnamoorthy V, Goodman S, Zatsiorsky V, Latash ML (2003) 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 (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
Krishnamoorthy V, Scholz JP, Latash ML (2007) The use of flexible arm muscle synergies to perform an isometric stabilization task. Clin Neurophysiol 118:525–537
Latash ML (1992) Virtual trajectories, joint stiffness, and changes in the limb natural frequency during single-joint oscillatory movements. Neurosci 49:209–220
Latash ML (1994) Reconstruction of equilibrium trajectories and joint stiffness patterns during single-joint voluntary movements under different instructions. Biol Cybern 71:441–450
Latash ML (2010) Motor synergies and the equilibrium-point hypothesis. Motor 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, Gottlieb GL (1990) Compliant characteristics of single joints: preservation of equifinality with phasic reactions. Biol Cybern 62:331–336
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
Latash ML, Scholz JP, Schöner G (2007) Toward a new theory of motor control. Motor Control 11:276–308
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? Motor Control 17:145–175
Perotto AO, Delagi EF, Iazzetti J, Morrison D (2011) Anatomical guide for the electromyographer: The limbs and trunk, 5th edn. Charles C Thomas, Springfield
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
Schmidt RA, McGown C (1980) Terminal accuracy of unexpected loaded rapid movements: evidence for a mass-spring mechanism in programming. J Mot Behav 12:149–161
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
Shapkova EYu, Shapkova AL, Goodman SR, Zatsiorsky VM, Latash ML (2008) Do synergies decrease force variability? A study of single-finger and multi-finger force production. Exp Brain Res 188:411–425
Slifkin AB, Vaillancourt DE, Newell KM (2000) Intermittency in the control of continuous force production. J Neurophysiol 84:1708–1718
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
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
Ting LH, Macpherson JM (2005) A limited set of muscle synergies for force control during a postural task. J Neurophysiol 93:609–613
Ting LH, McKay JL (2007) Neuromechanics of muscle synergies for posture and movement. Curr Opin Neurobiol 17:622–628
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
Vaillancourt DE, Russell DM (2002) Temporal capacity of short-term visuomotor memory in continuous force production. Exp Brain Res 145:275–285
Wang Y, Zatsiorsky VM, Latash ML (2006) Muscle synergies involved in preparation to a step made under the self-paced and reaction time instructions. Clin Neurophysiol 117:41–56
Wilhelm L, Zatsiorsky VM, Latash ML (2013) Equifinality and its violations in a redundant system: multi-finger accurate force production. J Neurophysiol 110:1965–1973
Zhou T, Solnik S, Wu Y-H, Latash ML (2014) Equifinality and its violations in a redundant system: control with referent configurations in a multi-joint positional task. Motor Control (in press)
Acknowledgments
The study was supported in part by an NIH Grant NS-035032.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Falaki, A., Towhidkhah, F., Zhou, T. et al. Task-specific stability in muscle activation space during unintentional movements. Exp Brain Res 232, 3645–3658 (2014). https://doi.org/10.1007/s00221-014-4048-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-014-4048-0