Skip to main content
Top
Published in: Experimental Brain Research 2/2019

01-02-2019 | Research Article

Quantitative analysis of multi-element synergy stabilizing performance: comparison of three methods with respect to their use in clinical studies

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

Published in: Experimental Brain Research | Issue 2/2019

Login to get access

Abstract

A number of analyses associated with the uncontrolled manifold (UCM) hypothesis have been used recently to investigate stability of actions across populations. We explored whether some of those methods have an advantage for clinical studies because they require fewer trials to achieve consistent findings. We compared the number of trials needed for the analysis of inter-trial variance, analysis of motor equivalence, and analysis in the space of referent coordinates. Young healthy adults performed four-finger accurate force production tasks under visual feedback with the right (dominant) and left hand over three days. Three methods [analytical (M1), experimental (M2), and cumulative mean (M3) methods] were used to define the minimal number of trials required to reach certain statistical criteria. Two of these methods, M1 and M2, showed qualitatively similar results. Fewer trials (M1: 5–13, M2: 4–10) were needed for analysis of motor equivalence compared to inter-trial variance analysis (M1: 14–24, M2: 10–14). The third method (M3) showed no major differences among the outcome variables. The index of synergy in the inter-trial variance analysis required a very small number of trials (M1, M2: 2–4). Variables related to referent coordinates required only a few trials (under 3), whereas the synergy index in this analysis required the largest number of trials (M1: 24–34, M2: 12–16). This is the first study to quantify the number of trials needed for UCM-based methods of assessing motor coordination broadly used in clinical studies. Clinical studies can take advantage of specific recommendations based on the current data regarding the number of trials needed for each analysis thus allowing minimizing the test session duration without compromising data reliability.
Appendix
Available only for authorised users
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 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(5):1383–1393CrossRefPubMedPubMedCentral 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(5):1383–1393CrossRefPubMedPubMedCentral
go back to reference Falaki A, Huang X, Lewis MM, Latash ML (2017a) Dopaminergic modulation of multi-muscle synergies in postural tasks performed by patients with Parkinson’s disease. J Electromyogr Kinesiol 33:20–26CrossRefPubMedPubMedCentral Falaki A, Huang X, Lewis MM, Latash ML (2017a) Dopaminergic modulation of multi-muscle synergies in postural tasks performed by patients with Parkinson’s disease. J Electromyogr Kinesiol 33:20–26CrossRefPubMedPubMedCentral
go back to reference Falaki A, Huang X, Lewis MM, Latash ML (2017b) 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 (2017b) Motor equivalence and structure of variance: multi-muscle postural synergies in Parkinson’s disease. Exp Brain Res 235:2243–2258CrossRefPubMedPubMedCentral
go back to reference 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(6):1320–1332CrossRefPubMedPubMedCentral 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(6):1320–1332CrossRefPubMedPubMedCentral
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 (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 Hamill J, McNiven SL (1990) Reliability of selected ground reaction force parameters during walking. Hum Mov Sci 9(2):117–131CrossRef Hamill J, McNiven SL (1990) Reliability of selected ground reaction force parameters during walking. Hum Mov Sci 9(2):117–131CrossRef
go back to reference Harris CM, Wolpert DM (1998) Signal-dependent noise determines motor planning. Nature 394(6695):780–784CrossRefPubMed Harris CM, Wolpert DM (1998) Signal-dependent noise determines motor planning. Nature 394(6695):780–784CrossRefPubMed
go back to reference Hogan N, Sternad D (2007) On rhythmic and discrete movements: reflections, definitions and implications for motor control. Exp Brain Res 181(1):13–30CrossRefPubMed Hogan N, Sternad D (2007) On rhythmic and discrete movements: reflections, definitions and implications for motor control. Exp Brain Res 181(1):13–30CrossRefPubMed
go back to reference James CR, Herman JA, Dufek JS, Bates BT (2007) Number of trials necessary to achieve performance stability of selected ground reaction force variables during landing. J Sport Sci Med 6(1):126–134 James CR, Herman JA, Dufek JS, Bates BT (2007) Number of trials necessary to achieve performance stability of selected ground reaction force variables during landing. J Sport Sci Med 6(1):126–134
go back to reference Jo HJ, Park J, Lewis MM, Huang X, Latash ML (2015) Prehension synergies and hand function in early-stage Parkinson’s disease. Exp Brain Res 233:425–440CrossRefPubMed Jo HJ, Park J, Lewis MM, Huang X, Latash ML (2015) Prehension synergies and hand function in early-stage Parkinson’s disease. Exp Brain Res 233:425–440CrossRefPubMed
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 Jo HJ, Mattos D, Lucassen EB, Huang X, Latash ML (2017) Changes in multidigit synergies and their feed-forward adjustments in multiple sclerosis. J Motor Beh 49:218–228CrossRef Jo HJ, Mattos D, Lucassen EB, Huang X, Latash ML (2017) Changes in multidigit synergies and their feed-forward adjustments in multiple sclerosis. J Motor Beh 49:218–228CrossRef
go back to reference Krishnamoorthy V, Latash ML, Scholz JP, Zatsiorsky VM (2003) Muscle synergies during shifts of the center of pressure by standing persons. Exp Brain Res 152:281–292CrossRefPubMed Krishnamoorthy V, Latash ML, Scholz JP, Zatsiorsky VM (2003) Muscle synergies during shifts of the center of pressure by standing persons. Exp Brain Res 152:281–292CrossRefPubMed
go back to reference Latash ML (2010) Motor synergies and the equilibrium-point hypothesis. Mot Control 14:294–322CrossRef Latash ML (2010) Motor synergies and the equilibrium-point hypothesis. Mot Control 14:294–322CrossRef
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, 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, Scholz JP, Schöner G (2002) Motor control strategies revealed in the structure of motor variability. Exerc Sport Sci Rev 30:26–31CrossRefPubMed Latash ML, Scholz JP, Schöner G (2002) Motor control strategies revealed in the structure of motor variability. Exerc Sport Sci Rev 30:26–31CrossRefPubMed
go back to reference Latash ML, Levin MF, Scholz JP, Schöner G (2010) Motor control theories and their applications. Medicina 46:382–392CrossRefPubMed Latash ML, Levin MF, Scholz JP, Schöner G (2010) Motor control theories and their applications. Medicina 46:382–392CrossRefPubMed
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 Lewis MM, Lee EY, Jo HJ, Du G, Park J, Flynn MR, Kong L, Latash ML, Huang X (2016) Synergy as a new and sensitive marker of basal ganglia dysfunction: a study of asymptomatic welders. Neurotoxicology 56:76–85CrossRefPubMedPubMedCentral Lewis MM, Lee EY, Jo HJ, Du G, Park J, Flynn MR, Kong L, Latash ML, Huang X (2016) Synergy as a new and sensitive marker of basal ganglia dysfunction: a study of asymptomatic welders. Neurotoxicology 56:76–85CrossRefPubMedPubMedCentral
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 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 Olafsdottir H, Yoshida N, Zatsiorsky VM, Latash ML (2005) Anticipatory covariation of finger forces during self-paced and reaction time force production. Neurosc Lett 381(1–2):92–96CrossRef Olafsdottir H, Yoshida N, Zatsiorsky VM, Latash ML (2005) Anticipatory covariation of finger forces during self-paced and reaction time force production. Neurosc Lett 381(1–2):92–96CrossRef
go back to reference Park J, Wu YH, Lewis MM, Huang X, Latash ML (2012) Changes in multifinger interaction and coordination in Parkinson’s disease. J Neurophysiol 108:915–924CrossRefPubMedPubMedCentral Park J, Wu YH, Lewis MM, Huang X, Latash ML (2012) Changes in multifinger interaction and coordination in Parkinson’s disease. J Neurophysiol 108:915–924CrossRefPubMedPubMedCentral
go back to reference Park J, Lewis MM, Huang X, Latash ML (2013) Effects of olivo-ponto-cerebellar atrophy (OPCA) on finger interaction and coordination. Clin Neurophysiol 124:991–998CrossRefPubMed Park J, Lewis MM, Huang X, Latash ML (2013) Effects of olivo-ponto-cerebellar atrophy (OPCA) on finger interaction and coordination. Clin Neurophysiol 124:991–998CrossRefPubMed
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 116:698–708CrossRefPubMedPubMedCentral 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 116:698–708CrossRefPubMedPubMedCentral
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 118:3152–3164CrossRefPubMedPubMedCentral Reschechtko S, Latash ML (2017) Stability of hand force production: I. Hand level control variables and multi-finger synergies. J Neurophysiol 118:3152–3164CrossRefPubMedPubMedCentral
go back to reference Reschechtko S, Latash ML (2018) Stability of hand force production: II. Ascending and descending synergies. J Neurophysiol 120:1045–1060CrossRefPubMed Reschechtko S, Latash ML (2018) Stability of hand force production: II. Ascending and descending synergies. J Neurophysiol 120:1045–1060CrossRefPubMed
go back to reference Sainburg RL (2005) Handedness: differential specializations for control of trajectory and position. Exerc Sport Sci Rev 33:206–213CrossRefPubMed Sainburg RL (2005) Handedness: differential specializations for control of trajectory and position. Exerc Sport Sci Rev 33:206–213CrossRefPubMed
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, Kang N, Patterson D, Latash ML (2003) Uncontrolled manifold analysis of single trials during multi-finger force production by persons with and without Down syndrome. Exp Brain Res 153:45–58CrossRefPubMed Scholz JP, Kang N, Patterson D, Latash ML (2003) Uncontrolled manifold analysis of single trials during multi-finger force production by persons with and without Down syndrome. Exp Brain Res 153:45–58CrossRefPubMed
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 Mot Behav 44:471–478CrossRefPubMedPubMedCentral Wu Y-H, Pazin N, Zatsiorsky VM, Latash ML (2012) Practicing elements vs. practicing coordination: changes in the structure of variance. J Mot Behav 44:471–478CrossRefPubMedPubMedCentral
Metadata
Title
Quantitative analysis of multi-element synergy stabilizing performance: comparison of three methods with respect to their use in clinical studies
Authors
Sandra M. S. F. Freitas
Paulo B. de Freitas
Mechelle M. Lewis
Xuemei Huang
Mark L. Latash
Publication date
01-02-2019
Publisher
Springer Berlin Heidelberg
Published in
Experimental Brain Research / Issue 2/2019
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI
https://doi.org/10.1007/s00221-018-5436-7

Other articles of this Issue 2/2019

Experimental Brain Research 2/2019 Go to the issue