Skip to main content
Top
Published in: Experimental Brain Research 6/2018

01-06-2018 | Research Article

Stability of steady hand force production explored across spaces and methods of analysis

Authors: Paulo B. de Freitas, Sandra M. S. F. Freitas, Mechelle M. Lewis, Xuemei Huang, Mark L. Latash

Published in: Experimental Brain Research | Issue 6/2018

Login to get access

Abstract

We used the framework of the uncontrolled manifold (UCM) hypothesis and explored the reliability of several outcome variables across different spaces of analysis during a very simple four-finger accurate force production task. Fourteen healthy, young adults performed the accurate force production task with each hand on 3 days. Small spatial finger perturbations were generated by the “inverse piano” device three times per trial (lifting the fingers 1 cm/0.5 s and lowering them). The data were analyzed using the following main methods: (1) computation of indices of the structure of inter-trial variance and motor equivalence in the space of finger forces and finger modes, and (2) analysis of referent coordinates and apparent stiffness values for the hand. Maximal voluntary force and the index of enslaving (unintentional finger force production) showed good to excellent reliability. Strong synergies stabilizing total force were reflected in both structure of variance and motor equivalence indices. Variance within the UCM and the index of motor equivalent motion dropped over the trial duration and showed good to excellent reliability. Variance orthogonal to the UCM and the index of non-motor equivalent motion dropped over the 3 days and showed poor to moderate reliability. Referent coordinate and apparent stiffness indices co-varied strongly and both showed good reliability. In contrast, the computed index of force stabilization showed poor reliability. The findings are interpreted within the scheme of neural control with referent coordinates involving the hierarchy of two basic commands, the r-command and c-command. The data suggest natural drifts in the finger force space, particularly within the UCM. We interpret these drifts as reflections of a trade-off between stability and optimization of action. The implications of these findings for the UCM framework and future clinical applications are explored in the discussion. Indices of the structure of variance and motor equivalence show good reliability and can be recommended for applied studies.
Literature
go back to reference Ambike S, Mattos D, Zatsiorsky VM, Latash ML (2016) Synergies in the space of control variables within the equilibrium-point hypothesis. Neurosci 315:150–161CrossRef Ambike S, Mattos D, Zatsiorsky VM, Latash ML (2016) Synergies in the space of control variables within the equilibrium-point hypothesis. Neurosci 315:150–161CrossRef
go back to reference Bernstein NA (1967) The co-ordination and regulation of movements. Pergamon Press, Oxford Bernstein NA (1967) The co-ordination and regulation of movements. Pergamon Press, Oxford
go back to reference Cicchetti DV (1994) Guidelines, criteria, and rules of thumb for evaluating normed and standardized assessment instruments in psychology. Psychol Assess 6:284–290CrossRef Cicchetti DV (1994) Guidelines, criteria, and rules of thumb for evaluating normed and standardized assessment instruments in psychology. Psychol Assess 6:284–290CrossRef
go back to reference Corcos DM, Agarwal GC, Flaherty BP, Gottlieb GL (1990) Organizing principles for single-joint movements: IV. Implications for isometric contractions. J Neurophysiol 64:1033–1042CrossRefPubMed Corcos DM, Agarwal GC, Flaherty BP, Gottlieb GL (1990) Organizing principles for single-joint movements: IV. Implications for isometric contractions. J Neurophysiol 64:1033–1042CrossRefPubMed
go back to reference Danion F, Schöner G, Latash ML, Li S, Scholz JP, Zatsiorsky VM (2003) A force mode hypothesis for finger interaction during multi-finger force production tasks. Biol Cybern 88:91–98CrossRefPubMed Danion F, Schöner G, Latash ML, Li S, Scholz JP, Zatsiorsky VM (2003) A force mode hypothesis for finger interaction during multi-finger force production tasks. Biol Cybern 88:91–98CrossRefPubMed
go back to reference 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 235:2243–2258CrossRefPubMedPubMedCentral 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 235:2243–2258CrossRefPubMedPubMedCentral
go back to reference 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 (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
go back to reference Feldman AG (1980) Superposition of motor programs. I. Rhythmic forearm movements in man. Neurosci 5:81–90CrossRef Feldman AG (1980) Superposition of motor programs. I. Rhythmic forearm movements in man. Neurosci 5:81–90CrossRef
go back to reference Feldman AG (1986) Once more on the equilibrium-point hypothesis (λ-model) for motor control. J Mot Behav 18:17–54CrossRefPubMed Feldman AG (1986) Once more on the equilibrium-point hypothesis (λ-model) for motor control. J Mot Behav 18:17–54CrossRefPubMed
go back to reference Feldman AG (2015) Referent control of action and perception: challenging conventional theories in behavioral science. Springer, New YorkCrossRef Feldman AG (2015) Referent control of action and perception: challenging conventional theories in behavioral science. Springer, New YorkCrossRef
go back to reference Feldman AG, Orlovsky GN (1972) The influence of different descending systems on the tonic stretch reflex in the cat. Exp Neurol 37:481–494CrossRefPubMed Feldman AG, Orlovsky GN (1972) The influence of different descending systems on the tonic stretch reflex in the cat. Exp Neurol 37:481–494CrossRefPubMed
go back to reference Gelfand IM, Latash ML (1998) On the problem of adequate language in movement science. Mot Control 2:306–313CrossRef Gelfand IM, Latash ML (1998) On the problem of adequate language in movement science. Mot Control 2:306–313CrossRef
go back to reference Gera G, Freitas SM, Scholz JP (2016a) Relationship of diminished interjoint coordination after stroke to hand path consistency. Exp Brain Res 234:741–751CrossRefPubMed Gera G, Freitas SM, Scholz JP (2016a) Relationship of diminished interjoint coordination after stroke to hand path consistency. Exp Brain Res 234:741–751CrossRefPubMed
go back to reference Gera G, McGlade KE, Reisman DS, Scholz JP (2016b) Trunk muscle coordination during upward and downward reaching in stroke survivors. Mot Control 20:50–69CrossRef Gera G, McGlade KE, Reisman DS, Scholz JP (2016b) Trunk muscle coordination during upward and downward reaching in stroke survivors. Mot Control 20:50–69CrossRef
go back to reference Gottlieb GL, Corcos DM, Agarwal GC (1989) Strategies for the control of voluntary movements with one mechanical degree of freedom. Behav Brain Sci 12:189–250CrossRef Gottlieb GL, Corcos DM, Agarwal GC (1989) Strategies for the control of voluntary movements with one mechanical degree of freedom. Behav Brain Sci 12:189–250CrossRef
go back to reference 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 319:194–205CrossRef 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 319:194–205CrossRef
go back to reference Kang N, Cauraugh JH (2017) Bilateral synergy as an index of force coordination in chronic stroke. Exp Brain Res 235:1501–1509CrossRefPubMed Kang N, Cauraugh JH (2017) Bilateral synergy as an index of force coordination in chronic stroke. Exp Brain Res 235:1501–1509CrossRefPubMed
go back to reference Kang N, Shinohara M, Zatsiorsky VM, Latash ML (2004) Learning multi-finger synergies: an uncontrolled manifold analysis. Exp Brain Res 157:336–350CrossRefPubMed Kang N, Shinohara M, Zatsiorsky VM, Latash ML (2004) Learning multi-finger synergies: an uncontrolled manifold analysis. Exp Brain Res 157:336–350CrossRefPubMed
go back to reference Koo TK, Li MY (2016) A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropract Med 15:155–163CrossRef Koo TK, Li MY (2016) A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropract Med 15:155–163CrossRef
go back to reference Kudo K, Tsutsui S, Ishikura T, Ito T, Yamamoto Y (2000) Compensatory coordination of release parameters in a throwing task. J Mot Behav 32:337–345CrossRefPubMed Kudo K, Tsutsui S, Ishikura T, Ito T, Yamamoto Y (2000) Compensatory coordination of release parameters in a throwing task. J Mot Behav 32:337–345CrossRefPubMed
go back to reference Latash ML (2010a) Motor synergies and the equilibrium-point hypothesis. Mot Control 14:294–322CrossRef Latash ML (2010a) Motor synergies and the equilibrium-point hypothesis. Mot Control 14:294–322CrossRef
go back to reference Latash ML (2010b) Stages in learning motor synergies: A view based on the equilibrium-point hypothesis. Hum Move Sci 29:642–654CrossRef Latash ML (2010b) Stages in learning motor synergies: A view based on the equilibrium-point hypothesis. Hum Move Sci 29:642–654CrossRef
go back to reference Latash ML (2017) Biological movement and laws of physics. Mot Control 21:327–344CrossRef Latash ML (2017) Biological movement and laws of physics. Mot Control 21:327–344CrossRef
go back to reference Latash ML, Gottlieb GL (1991) Reconstruction of elbow joint compliant characteristics during fast and slow voluntary movements. Neurosci 43:697–712CrossRef Latash ML, Gottlieb GL (1991) Reconstruction of elbow joint compliant characteristics during fast and slow voluntary movements. Neurosci 43:697–712CrossRef
go back to reference Latash ML, Huang X (2015) Neural control of movement stability: lessons from studies of neurological patients. Neurosci 301:39–48CrossRef Latash ML, Huang X (2015) Neural control of movement stability: lessons from studies of neurological patients. Neurosci 301:39–48CrossRef
go back to reference Latash ML, Zatsiorsky VM (2016) Biomechanics and Motor Control: Defining Central Concepts. Academic Press, New York Latash ML, Zatsiorsky VM (2016) Biomechanics and Motor Control: Defining Central Concepts. Academic Press, New York
go back to reference Latash ML, Scholz JF, Danion F, Schöner G (2001) Structure of motor variability in marginally redundant multi-finger force production tasks. Exp Brain Res 141:153–165CrossRefPubMed Latash ML, Scholz JF, Danion F, Schöner G (2001) Structure of motor variability in marginally redundant multi-finger force production tasks. Exp Brain Res 141:153–165CrossRefPubMed
go back to reference Latash ML, Scholz JP, Schöner G (2007) Toward a new theory of motor synergies. Mot Control 11:275–307 Latash ML, Scholz JP, Schöner G (2007) Toward a new theory of motor synergies. Mot Control 11:275–307
go back to reference Leone FC, Nottingham RB, Nelson LS (1961) The folded normal distribution. Technometrics 3:543–550CrossRef Leone FC, Nottingham RB, Nelson LS (1961) The folded normal distribution. Technometrics 3:543–550CrossRef
go back to reference Li ZM, Latash ML, Zatsiorsky VM (1998) Force sharing among fingers as a model of the redundancy problem. Exp Brain Res 119:276–286CrossRefPubMed Li ZM, Latash ML, Zatsiorsky VM (1998) Force sharing among fingers as a model of the redundancy problem. Exp Brain Res 119:276–286CrossRefPubMed
go back to reference Li ZM, Zatsiorsky VM, Latash ML (1999) Contributions of the extrinsic and intrinsic hand muscles to the moments in finger joints. J Clin Biomech 15:203–211CrossRef Li ZM, Zatsiorsky VM, Latash ML (1999) Contributions of the extrinsic and intrinsic hand muscles to the moments in finger joints. J Clin Biomech 15:203–211CrossRef
go back to reference Li ZM, Zatsiorsky VM, Latash ML (2001) The effect of finger extensor mechanism on the flexor force during isometric tasks. J Biomech 34:1097–1102CrossRefPubMed Li ZM, Zatsiorsky VM, Latash ML (2001) The effect of finger extensor mechanism on the flexor force during isometric tasks. J Biomech 34:1097–1102CrossRefPubMed
go back to reference Martin JR, Budgeon MK, Zatsiorsky VM, Latash ML (2011) Stabilization of the total force in multi-finger pressing tasks studied with the ‘inverse piano’ technique. Hum Mov Sci 30:446–458CrossRefPubMedPubMedCentral Martin JR, Budgeon MK, Zatsiorsky VM, Latash ML (2011) Stabilization of the total force in multi-finger pressing tasks studied with the ‘inverse piano’ technique. Hum Mov Sci 30:446–458CrossRefPubMedPubMedCentral
go back to reference Martin JR, Terekhov AA, Latash ML, Zatsiorsky VM (2013) Optimization and variability of motor behavior in multi-finger tasks: What variables does the brain use? J Motor Behav 45:289–305CrossRef Martin JR, Terekhov AA, Latash ML, Zatsiorsky VM (2013) Optimization and variability of motor behavior in multi-finger tasks: What variables does the brain use? J Motor Behav 45:289–305CrossRef
go back to reference Matthews PBC (1959) The dependence of tension upon extension in the stretch reflex of the soleus of the decerebrate cat. J Physiol 47:521–546CrossRef Matthews PBC (1959) The dependence of tension upon extension in the stretch reflex of the soleus of the decerebrate cat. J Physiol 47:521–546CrossRef
go back to reference Mattos D, Latash ML, Park E, Kuhl J, Scholz JP (2011) Unpredictable elbow joint perturbation during reaching results in multijoint motor equivalence. J Neurophysiol 106:1424–1436CrossRefPubMedPubMedCentral Mattos D, Latash ML, Park E, Kuhl J, Scholz JP (2011) Unpredictable elbow joint perturbation during reaching results in multijoint motor equivalence. J Neurophysiol 106:1424–1436CrossRefPubMedPubMedCentral
go back to reference Mattos D, Schöner G, Zatsiorsky VM, Latash ML (2015) Motor equivalence during accurate multi-finger force production. Exp Brain Res 233:487–502CrossRefPubMed Mattos D, Schöner G, Zatsiorsky VM, Latash ML (2015) Motor equivalence during accurate multi-finger force production. Exp Brain Res 233:487–502CrossRefPubMed
go back to reference Müller H, Sternad D (2003) A randomization method for the calculation of covariation in multiple nonlinear relations: illustrated with the example of goal-directed movements. Biol Cybern 89:22–33PubMed Müller H, Sternad D (2003) A randomization method for the calculation of covariation in multiple nonlinear relations: illustrated with the example of goal-directed movements. Biol Cybern 89:22–33PubMed
go back to reference Ohtsuki T (1981) Inhibition of individual fingers during grip strength exertion. Ergonomics 24:21–36CrossRefPubMed Ohtsuki T (1981) Inhibition of individual fingers during grip strength exertion. Ergonomics 24:21–36CrossRefPubMed
go back to reference Olafsdottir HB, Zatsiorsky VM, Latash ML (2008) The effects of strength training on finger strength and hand dexterity in healthy elderly individuals. J Appl Physiol 105:1166–1178CrossRefPubMedPubMedCentral Olafsdottir HB, Zatsiorsky VM, Latash ML (2008) The effects of strength training on finger strength and hand dexterity in healthy elderly individuals. J Appl Physiol 105:1166–1178CrossRefPubMedPubMedCentral
go back to reference Parsa B, O’Shea DJ, Zatsiorsky VM, Latash ML (2016) On the nature of unintentional action: a study of force/moment drifts during multi-finger tasks. J Neurophysiol 116:698–708CrossRefPubMed Parsa B, O’Shea DJ, Zatsiorsky VM, Latash ML (2016) On the nature of unintentional action: a study of force/moment drifts during multi-finger tasks. J Neurophysiol 116:698–708CrossRefPubMed
go back to reference Prilutsky BI, Zatsiorsky VM (2002) Optimization-based models of muscle coordination. Exer Sport Sci Rev 30:32–38CrossRef Prilutsky BI, Zatsiorsky VM (2002) Optimization-based models of muscle coordination. Exer Sport Sci Rev 30:32–38CrossRef
go back to reference Reisman D, Scholz JP (2003) Aspects of joint coordination are preserved during pointing in persons with post-stroke hemiparesis. Brain 126:2510–2527CrossRefPubMed Reisman D, Scholz JP (2003) Aspects of joint coordination are preserved during pointing in persons with post-stroke hemiparesis. Brain 126:2510–2527CrossRefPubMed
go back to reference Reschechtko S, Latash ML (2017) Stability of hand force production: I. Hand level control variables and multi-finger synergies. J Neurophysiol 118:3152–3164CrossRefPubMed Reschechtko S, Latash ML (2017) Stability of hand force production: I. Hand level control variables and multi-finger synergies. J Neurophysiol 118:3152–3164CrossRefPubMed
go back to reference Schieber MH, Santello M (2004) Hand function: peripheral and central constraints on performance. J Appl Physiol 96:2293–2300CrossRefPubMed Schieber MH, Santello M (2004) Hand function: peripheral and central constraints on performance. J Appl Physiol 96:2293–2300CrossRefPubMed
go back to reference Scholz JP, Schöner G (1999) The uncontrolled manifold concept: Identifying control variables for a functional task. Exp Brain Res 126:289–306CrossRefPubMed Scholz JP, Schöner G (1999) The uncontrolled manifold concept: Identifying control variables for a functional task. Exp Brain Res 126:289–306CrossRefPubMed
go back to reference Scholz JP, Danion F, Latash ML, Schöner G (2002) Understanding finger coordination through analysis of the structure of force variability. Biol Cybern 86:29–39CrossRefPubMed Scholz JP, Danion F, Latash ML, Schöner G (2002) Understanding finger coordination through analysis of the structure of force variability. Biol Cybern 86:29–39CrossRefPubMed
go back to reference 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 180:163–179CrossRefPubMed 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 180:163–179CrossRefPubMed
go back to reference Seif-Naraghi AH, Winters JM (1990) Optimized strategies for scaling goal-directed dynamic limb movements. In: Winters JM, Woo SL-Y (eds) Multiple muscle systems. Biomechanics and movement organization. Springer, New York, pp 312–334CrossRef Seif-Naraghi AH, Winters JM (1990) Optimized strategies for scaling goal-directed dynamic limb movements. In: Winters JM, Woo SL-Y (eds) Multiple muscle systems. Biomechanics and movement organization. Springer, New York, pp 312–334CrossRef
go back to reference Singh T, SKM V, Zatsiorsky VM, Latash ML (2010) Fatigue and motor redundancy: adaptive increase in force variance in multi-finger tasks. J Neurophysiol 103:2990–3000CrossRefPubMedPubMedCentral Singh T, SKM V, Zatsiorsky VM, Latash ML (2010) Fatigue and motor redundancy: adaptive increase in force variance in multi-finger tasks. J Neurophysiol 103:2990–3000CrossRefPubMedPubMedCentral
go back to reference Tawy GF, Rowe P, Biant L (2018) Gait variability and motor control in patients with knee osteoarthritis as measured by the uncontrolled manifold technique. Gait Posture 59:272–277CrossRefPubMed Tawy GF, Rowe P, Biant L (2018) Gait variability and motor control in patients with knee osteoarthritis as measured by the uncontrolled manifold technique. Gait Posture 59:272–277CrossRefPubMed
go back to reference Tokuda K, Anan M, Takahashi M, Sawada T, Tanimoto K, Kito N, Shinkoda K (2018) Biomechanical mechanism of lateral trunk lean gait for knee osteoarthritis patients. J Biomech 66:10–17CrossRefPubMed Tokuda K, Anan M, Takahashi M, Sawada T, Tanimoto K, Kito N, Shinkoda K (2018) Biomechanical mechanism of lateral trunk lean gait for knee osteoarthritis patients. J Biomech 66:10–17CrossRefPubMed
go back to reference Wu Y-H, Pazin N, Zatsiorsky VM, Latash ML (2012) Practicing elements vs. practicing coordination: changes in the structure of variance. J Motor Behav 44:471–478CrossRef Wu Y-H, Pazin N, Zatsiorsky VM, Latash ML (2012) Practicing elements vs. practicing coordination: changes in the structure of variance. J Motor Behav 44:471–478CrossRef
go back to reference Zatsiorsky VM, Li ZM, Latash ML (2000) Enslaving effects in multi-finger force production. Exp Brain Res 131:187–195CrossRefPubMed Zatsiorsky VM, Li ZM, Latash ML (2000) Enslaving effects in multi-finger force production. Exp Brain Res 131:187–195CrossRefPubMed
Metadata
Title
Stability of steady hand force production explored across spaces and methods of analysis
Authors
Paulo B. de Freitas
Sandra M. S. F. Freitas
Mechelle M. Lewis
Xuemei Huang
Mark L. Latash
Publication date
01-06-2018
Publisher
Springer Berlin Heidelberg
Published in
Experimental Brain Research / Issue 6/2018
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI
https://doi.org/10.1007/s00221-018-5238-y

Other articles of this Issue 6/2018

Experimental Brain Research 6/2018 Go to the issue