Abstract
This study tests the following hypotheses in multi-digit circular object prehension: the principle of superposition (i.e., a complex action can be decomposed into independently controlled sub-actions) and the hierarchical organization (i.e., individual fingers at the lower level are coordinated to generate a desired task-specific outcome of the virtual finger at the higher level). Subjects performed 25 trials while statically holding a circular handle instrumented with five six-component force/moment sensors under seven external torque conditions. We performed a principal component (PC) analysis on forces and moments of the thumb and virtual finger (VF: an imagined finger producing the same mechanical effects of all finger forces and moments combined) to test the applicability of the principle of superposition in a circular object prehension. The synergy indices, measuring synergic actions of the individual finger (IF) moments for the stabilization of the VF moment, were calculated to test the hierarchical organization. Mixed-effect ANOVAs were used to test the dependent variable differences for different external torque conditions and different fingers at the VF and IF levels. The PC analysis showed that the elemental variables were decoupled into two groups: one group related to grasping stability control (normal force control) and the other group associated with rotational equilibrium control (tangential force control), which supports the principle of superposition. The synergy indices were always positive, suggesting error compensations between IF moments for the VF moment stabilization, which confirms the hierarchical organization of multi-digit prehension.
Similar content being viewed by others
References
Adams SK, Peterson PJ (1988) Maximum voluntary hand grip torque for circular electrical connectors. Hum Factors 30 30:733–745
Amis AA (1987) Variation of finger forces in maximal isometric grasp tests on a range of cylinder diameters. J Biomed Eng 9:313–320
Arimoto S, Nguyen PTA (2001) Principle of superposition for realising dexterous pinching motions of a pair of robot fingers with soft-tips. IEICE Trans Fundam Electron Commun Comp Sci E 84A:39–47
Arimoto S, Tahara K, Yamaguchi M, Nguyen PTA, Han HY (2001) Principles of superposition for controlling pinch motions by means of robot fingers with soft tips. Robotica 19:21–28
Arimoto S, Tahara K, Bae JH, Yoshida M (2003) A stability theory of a manifold: concurrent realization of grasp and orientation control of an object by a pair of robot fingers. Robotica 21:163–178
Baud-Bovy G, Soechting JF (2001) Two virtual fingers in the control of the tripod grasp. J Neurophysiol 86:604–615
Bernstein NA (1935) The problem of interrelaton between coordination and localization. Arch Biol Sci 38:1–35
Bernstein NA (1967) The co-ordination and regulation of movements. Pergamon, Oxford
Bilodeau M, Keen DA, Sweeney PJ, Shields RW, Enoka RM (2000) Strength training can improve steadiness in persons with essential tremor. Muscle Nerve 23:771–778
Book WF (1908) The psychology of skill. Montana, Missoula
Bryan WL, Harter N (1899) Studies on the telegraphic language: the acquisition of a hierarchy of habits. Psychol Rev 6:345–175
Buys EJ, Lemon RN, Mantel GW, Muir RB (1986) Selective facilitation of different hand muscles by single corticospinal neurones in the conscious monkey. J Physiol 381:529–549
Cutkosky MR, Howe RD (1990) Dextrous Robot Hands. Springer, Heidelberg
Danion F, Schoner G, Latash ML, Li S, Scholz JP, Zatsiorsky VM (2003) A mode hypothesis for finger interaction during multi-finger force-production tasks. Biol Cybern 88:91–98
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
DJ C, MW R (1986) The effects of handle shape and size on exerted force. Human Factors 28:253–265
Doulgeri Z, Fasoulas J, Arimoto S (2002) Feedback control for object manipulation by a pair of soft tip fingers. Robotica 20:1–11
Fetz EE, Finocchio DV, Baker MA, Soso MJ (1980) Sensory and motor responses of precentral cortex cells during comparable passive and active joint movements. J Neurophysiol 43:1070–1089
Flanagan JR, Wing AM (1995) The stability of precision grip forces during cyclic arm movements with a hand-held load. Exp Brain Res 105:455–464
Fullerton GS, Carttell J (1892) On the perception of small differences. University of Pennsylvania Press, Philadelphia
Gallistel CR (1980) THe organization of action. Erlbaum, Hillsdale
Gelfand IM, Tsetlin M (1966) On mathematical modeling of the mechanisms of the central nervous system. In: Gelfand IM, Gurfinkel VS, Fomin SV, Tsetlin ML (eds) Models of the structural–functional organization of certain biological systems. Nauka, Moscow (a translation is available in 1971 edition) MIT Press, Cambridge, pp 9–26
Gregory RW (2002) Biomechanics and control of force and torque production in multi-finger prehension. In: Department of Kinesiology. The Pennsylvania State University, State College
Gurram R, Rakheja S, Gouw GJ (1995) A study of hand grip pressure distribution and EMG of finger flexor muscles under dynamic loads. Ergonomics 38:684–699
Hall C (1997) External pressure at the hand during object handling and work with tools. Int J Ind Ergon 20:191–206
Hamilton AF, Jones KE, Wolpert DM (2004) The scaling of motor noise with muscle strength and motor unit number in humans. Exp Brain Res 157:417–430
Iberall T (1997) Human prehension and dexterous robot hands. Int J Robot Res 16:285–299
Imrhan SN, Loo CH (1988) Modelling wrist-twisting strength of the elderly. Ergonomics 31:1807–1819
Johansson RS (1998) Sensory input and control of grip (discussion 59–63). Novartis Found Symp 218:45–59
Kaiser HF (1960) The application of electronic computers to factor analysis. Psychol Meas 20:141–151
Kang N, Shinohara M, Zatsiorsky VM, Latash ML (2004) Learning multi-finger synergies: an uncontrolled manifold analysis. Exp Brain Res 157:336–350
Kilbreath SL, Gorman RB, Raymond J, Gandevia SC (2002) Distribution of the forces produced by motor unit activity in the human flexor digitorum profundus. J Physiol 543:289–296
Kim SW, Shim JK, Zatsiorsky VM, Latash ML (2006) Anticipatory adjustments of multi-finger synergies in preparation to self-triggered perturbations. Exp Brain Res 174:604–612
Kinoshita H, Francis PR (1996) A comparison of prehension force control in young and elderly individuals. Eur J Appl Physiol Occup Physiol 74:450–460
Krishnamoorthy V, Latash ML, Scholz JP, Zatsiorsky VM (2003) Muscle synergies during shifts of the center of pressure by standing persons. Exp Brain Res 152:281–292
Lang CE, Schieber MH (2004) Human finger independence: limitations due to passive mechanical coupling versus active neuromuscular control. J Neurophysiol 92:2802–2810
Latash M (2000) There is no motor redundancy in human movements. There is motor abundance. Motor Control 4:259–260
Latash ML, Scholz JP, Schoner G (2002) Motor control strategies revealed in the structure of motor variability. Exerc Sport Sci Rev 30:26–31
Latash ML, Shim JK, Gao F, Zatsiorsky VM (2004a) Rotational equilibrium during multi-digit pressing and prehension. Motor Control 8:392–404
Latash ML, Shim JK, Zatsiorsky VM (2004b) Is there a timing synergy during multi-finger production of quick force pulses? Exp Brain Res 159:65–71
Latash ML, Olafsdottir H, Shim JK, Zatsiorsky VM (2005a) Synergies that stabilize and destabilize action. In: Gantchev N (ed) From basic motor control to functional recovery-IV. Marin Drinov Academic Publishing House, Sofia, pp 19–25
Latash ML, Shim JK, Smilga AV, Zatsiorsky VM (2005b) A central back-coupling hypothesis on the organization of motor synergies: a physical metaphor and a neural model. Biol Cybern 92:186–191
Lee JW, Rim K (1991) Measurement of finger joint angles and maximum finger forces during cylinder grip activity. J Biomed Eng 13:152–162
Li ZM, Latash ML, Zatsiorsky VM (1998) Force sharing among fingers as a model of the redundancy problem. Exp Brain Res 119:276–286
Mason MT, Salisbury KJ (1985) Robot Hands and the Mechanics of Manipulation (artificial intelligence). MIT Press, Cambridge
Michon JA (1967) Timing in temporal tracking. Institute for Perception RVO-TNO, Sesterberg
Moritz CT, Barry BK, Pascoe MA, Enoka RM (2005) Discharge rate variability influences the variation in force fluctuations across the working range of a hand muscle. J Neurophysiol 93:2449–2459
Nagashima K, Konz S (1986) Jar lids: effect of diameter, gripping amterials and knurling. In: Proceedings of the human Factors Society thirtieth annual meeting. The Human Factors Society, Santa Monica
Neter J, Wasserman W (1974) Applied linear statistical models. Richard D. Irwin, Homewood
Newell KM, Carlton LG (1988) Force variability in isometric tasks. J Exp Psychol Human Percept Perform14:32–44
Newell KM, Corcos DM (1993) Variability and motor control. Human Kinetics, Champaign
Nguyen PTA, Arimoto S (2002) Dexterous manipulation of an object by means of multi-dof robotic fingers with soft tips. J Robot Sys 19:349–362
Olafsdottir H, Yoshida N, Zatsiorsky VM, Latash ML (2005a) Anticipatory covariation of finger forces during self-paced and reaction time force production. Neurosci Lett 381:92–96
Olafsdottir H, Zatsiorsky VM, Latash ML (2005b) Is the thumb a fifth finger? A study of digit interaction during force production tasks. Exp Brain Res 160:203–213
Pataky T, Latash M, Zatsiorsky V (2004) Tangential load sharing among fingers during prehension. Ergonomics 47:876–889
Pheasant S, O’Neill D (1975) Performance in gripping and turning: a study in hand/handle effectiveness. Appl Ergon 6:205–208
Radhakrishnan S, Nagaravindra M (1993) Analysis of hand forces in health and disease during maximum isometric grasping of cylinders. Med Biol Eng Comput 31:372–376
Reilly KT, Hammond GR (2000) Independence of force production by digits of the human hand. Neurosci Lett 290:53–56
Rohles FH, Moldrup KL, Laviana JE (1983) Opening jars: an anthropometric study of the wrist twisting strength in elderly. In: Proceedings of the human factors society, twenty-seventh annual meeting
Santello M, Soechting JF (1997) Matching object size by controlling finger span and hand shape. Somatosens Mot Res 14:203–212
Santello M, Soechting JF (2000) Force synergies for multifingered grasping. Exp Brain Res 133:457–467
Santello M, Flanders M, Soechting JF (2002) Patterns of hand motion during grasping and the influence of sensory guidance. J Neurosci 22:1426–1435
Scholz JP, Schoner G (1999) The uncontrolled manifold concept: identifying control variables for a functional task. Exp Brain Res 126:289–306
von Schroeder HP, Botte MJ (2001) Anatomy and functional significance of the long extensors to the fingers and thumb. Clin Orthop Relat Res: 74–83
von Schroeder HP, Botte MJ, Gellman H (1990) Anatomy of the juncturae tendinum of the hand. J Hand Surg Am 15:595–602
Sherrington CS (1947) The integrative action of the nervous system, New edn. Yale University Press, New Hampshire
Shim JK, Latash ML, Zatsiorsky VM (2003a) The human central nervous system needs time to organize task-specific covariation of finger forces. Neurosci Lett 353:72–74
Shim JK, Latash ML, Zatsiorsky VM (2003b) Prehension synergies: trial-to-trial variability and hierarchical organization of stable performance. Exp Brain Res 152:173–184
Shim JK, Latash ML, Zatsiorsky VM (2004a) Finger coordination during moment production on a mechanically fixed object. Exp Brain Res 157:457–467
Shim JK, Latash ML, Zatsiorsky VM (2004b) Prehension synergies in three dimensions. J Neurophysiol 93:766–776
Shim JK, Lay BS, Zatsiorsky VM, Latash ML (2004c) Age-related changes in finger coordination in static prehension tasks. J Appl Physiol 97:213–224
Shim JK, Latash ML, Zatsiorsky VM (2005a) Prehension synergies: Trial-to-trial variability and principle of superposition during static prehension in three dimensions. J Neurophysiol 93:3649–3658
Shim JK, Olafsdottir H, Latash ML, Zatsiorsky VM (2005b) The emergency and disappearance of multi-digit synergies during force production tasks. Exp Brain Res 164:260–270
Shim JK, Huang J, Latash ML, Zatsiorsky VM (2006a) Multi-digit maximum voluntary torque productions on a circular object. Ergonomics (in press)
Shim JK, Oliveira MA, Hsu J, Huang J, Park J, Clark JE (2006b) Hand digit control in children: age-related changes in hand digit force interactions during maximum flexion and extension force production tasks. Exp Brain Res (in press)
Shim JK, Park J, Zatsiorsky VM, Latash ML (2006c) Adjustments of prehension synergies in response to self-triggered and experimenter-triggered loading and torque perturbations. Exp Brain Res 175:641–653
Shimoga KB, Goldenberg AA (1996) Soft robotic fingertips 2. Modeling and impedance regulation. Int J Robot Res 15:335–350
Shinoda Y, Zarzecki P, Asanuma H (1979) Spinal branching of pyramidal tract neurons in the monkey. Exp Brain Res 34:59–72
Shinohara M, Li S, Kang N, Zatsiorsky VM, Latash ML (2003) Effects of age and gender on finger coordination in MVC and submaximal force-matching tasks. J Appl Physiol 94:259–270
Shinohara M, Scholz JP, Zatsiorsky VM, Latash ML (2004) Finger interaction during accurate multi-finger force production tasks in young and elderly persons. Exp Brain Res 156:282–292
Sosnoff JJ, Newell KM (2006) Are age-related increases in force variability due to decrements in strength? Exp Brain Res 174:86–94
Taylor JR (1997) Introduction to error analysis. the study of uncertiainties in physical mesurement. University Science Books, Sausalito
Turvey MT (1977) Preliminaries to a theory of action with reference to vision. Erlbaum, Hillasdale
Turvey MT (1990) Coordination. Amer Psychol 45:938–953
Weiss P (1941) Self-differentiation of the basic patterns of coordination. Comp Psychol Monogr 17:1–96
Yoshikawa T (1999) Virtual truss model for characterization of internal forces for multiple finger grasps. IEEE Trans Robot Autom 15:941–947
Zatsiorsky VM (2002) Kinetics of Human Motion. Human Kinetics, Champaign
Zatsiorsky VM, Latash ML (2004) Prehension synergies. Exerc Sport Sci Rev 32:75–80
Zatsiorsky VM, Li ZM, Latash ML (2000) Enslaving effects in multi-finger force production. Exp Brain Res 131:187–195
Zatsiorsky VM, Gregory RW, Latash ML (2002) Force and torque production in static multifinger prehension: biomechanics and control. I. Biomechanics. Biol Cybern 87:50–57
Zatsiorsky VM, Gao F, Latash ML (2003) Prehension synergies: effects of object geometry and prescribed torques. Exp Brain Res 148:77–87
Zatsiorsky VM, Latash ML, Gao F, Shim JK (2004) The principle of superposition in human prehension. Robotica 22:231–234
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Shim, J.K., Park, J. Prehension synergies: principle of superposition and hierarchical organization in circular object prehension. Exp Brain Res 180, 541–556 (2007). https://doi.org/10.1007/s00221-007-0872-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-007-0872-9