Abstract
We investigated the effects of exercise-induced fatigue of a digit on the biomechanics of a static prehension task. The participants were divided into two groups. One group performed the fatiguing exercise using the thumb (group-thumb) and the second group performed the exercise using the index finger (group-index). We analyzed the prehensile action as being based on a two-level hierarchy. Our first hypothesis was that fatigue of the thumb would have stronger effects at the upper level (action shared between the thumb and all four fingers combined—virtual finger) and fatigue of the index finger would have stronger effects at the lower level of the hierarchy (action of the virtual finger shared among actual fingers). We also hypothesized that fatigue would cause a decrease in the normal force applied by the exercised digit and correspondingly lead to a decrease in the normal force applied by the opposing digit(s). Our third hypothesis was that fatigue would leave the tangential forces unaffected. Fatigue led to a significant drop in the normal force of both exercised and non-exercised (opposing) digits. The tangential forces of the exercised digits increased after fatigue. This led to a drop in the safety margin in the group-thumb, but not group-index. As such, the results supported the first two hypotheses but not the third hypothesis. Overall, the results suggested that fatigue triggered a chain reaction that involved both forces and moments of force produced by individual digits leading to a violation of the principle of superposition. The findings are interpreted within the framework of the referent configuration hypothesis.
Similar content being viewed by others
References
Arbib MA, Iberall T, Lyons D (1985) Coordinated control programs for movements of the hand. Exp Brain Res Suppl 10:111–129
Balestra C, Duchateau J, Hainaut K (1992) Effects of fatigue on the stretch reflex in a human muscle. Electroencephalogr Clin Neurophysiol 85:46–52
Baud-Bovy G, Soechting JF (2001) Two virtual fingers in the control of the tripod grasp. J Neurophysiol 86:604–615
Bigland B, Lippold OCJ (1954) Motor unit activity in the voluntary contraction of human muscle. J Physiol 125:322–335
Birznieks I, Wheat HE, Redmond SJ, Salo LM, Lovell NH, Goodwin AW (2010) Encoding of tangential torque in responses of tactile afferent fibres innervating the fingerpad of the monkey. J Physiol 588:1057–1072
Burstedt MKO, Birznieks I, Edin BB, Johansson RS (1997) Control of forces applied by individual fingers engaged in restraint of an active object. J Neurophysiol 78:117–128
Cain W, Stevens J (1971) Effort in sustained and phasic handgrip contractions. Am J Psychol 84:52–65
Contessa P, Adam A, DeLuca CJ (2009) Motor unit control and force fluctuation during fatigue. J Appl Physiol 107:235–243
Cutkosky MR (1989) On grasp choice, grasp models, and the design of hands for manufacturing tasks. IEEE Trans Robot Autom 5:269–279
Danna-dos-Santos A, Poston B, Jesunathadas M, Bobich LR, Hamm TM, Santello M (2010) The influence of fatigue on hand muscle coordination and EMG–EMG coherence during three-digit grasping. J Neurophysiol 104:3576–3587
Dartnall TJ, Nordstrom MA, Semmler JG (2008) Motor unit synchronization is increased in biceps brachii after exercise-induced damage to elbow flexor muscles. J Neurophysiol 99:1008–1019
Edin BB, Westling G, Johansson RS (1992) Independent control of fingertip forces at individual digits during precision lifting in humans. J Physiol 450:547–564
Edman KAP, Lou F (1990) Changes in force and stiffness induced by fatigue and intracellular acidification in frog muscle fibres. J Physiol 424:133–149
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 (1986) Once more on the equilibrium-point hypothesis (lambda model) for motor control. J Mot Behav 18:17–54
Feldman AG (2009) New insights into action–perception coupling. Exp Brain Res 194:39–58
Flanagan JR, Tresilian J, Wing AM (1993) Coupling of grip force and load force during arm movements with grasped objects. Neurosci Lett 152:53–56
Fuglevand AJ (1996) Neural aspects of fatigue. Neuroscientist 2:203–206
Gandevia SC (2001) Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 81:1725–1790
Gibson ASC, Noakes TD (2004) Evidence for complex system integration and dynamic neural regulation of skeletal muscle recruitment during exercise in humans. Br J Sports Med 38:797–806
Gorniak SL, Zatsiorsky VM, Latash ML (2009) Hierarchical control of static prehension: I. Biomechanics. Exp Brain Res 193:615–631
Haugland MK, Hoffer JA (1994) Slip information provided by nerve cuff signals: application in closed-loop control of functional electrical stimulation. IEEE Trans Rehabil Eng 2:29–36
Hockensmith GB, Lowell SY, Fuglevand AJ (2005) Common input across motor nuclei mediating precision grip in humans. J Neurosci 25:4560–4564
Iberall T (1997) Human prehension and dexterous robot hands. Int J Robot Res 16:285–299
Johansson RS (1996) Sensory control of dexterous manipulation in humans. In: Wing AM, Haggard P, Flanagan JF (eds) Hand and brain: the neurophysiology and psychology of hand movements. Academic, San Diego, pp 381–414
Johansson RS, Westling G (1984) Roles of glabrous skin receptors and sensorimotor memory in automatic control of precision grip when lifting rougher or more slippery objects. Exp Brain Res 56:550–564
Jones LA, Hunter IW (1983) Force and EMG correlates of constant effort contractions. Eur J Appl Physiol Occup Physiol 51:75–83
Latash ML (2010) Motor synergies and the equilibrium-point hypothesis. Mot Control 14:294–322
Luu BL, Day BL, Cole JD, Fitzpatrick RC (2011) The fusimotor and reafferent origin of the sense of force and weight. J Physiol 589:3135–3147
Martin PG, Weerakkody N, Gandevia SC, Taylor JL (2008) Group III and IV muscle afferents differentially affect the motor cortex and motoneurones in humans. J Physiol 586:1277–1289
Mason MT (2001) Mechanics of robotic manipulation. The MIT Press, Cambridge
Mason MT, Salisbury JK (1985) Robot hands and the mechanics of manipulation. The MIT Press, Cambridge
Niu X, Latash ML, Zatsiorsky VM (2007) Prehension synergies in the grasps with complex friction patterns: local versus synergic effects and the template control. J Neurophysiol 98:16–28
Park J, Singh T, Zatsiorsky VM, Latash ML (2012) Optimality versus variability: effect of fatigue in multi-finger redundant tasks. Exp Brain Res 216:591–607
Pataky TC (2005) Soft tissue strain energy minimization: a candidate control scheme for intra-finger normal–tangential force coordination. J Biomech 38:1723–1727
Pataky TC, Latash ML, Zatsiorsky VM (2004) Tangential load sharing among fingers during prehension. Ergonomics 47:876–889
Prattichizzo D, Trinkle JC (2008) Grasping. In: Siciliano B, Khatib O (eds) Springer handbook of robotics. Springer, Berlin, pp 671–700
Savescu AV, Latash ML, Zatsiorsky VM (2008) A technique to determine friction at the finger tips. J Appl Biomech 24:43–50
Seo NJ, Armstrong TJ, Drinkaus P (2009) A comparison of two methods of measuring static coefficient of friction at low normal forces: a pilot study. Ergonomics 52:121–135
Shim JK, Latash ML, Zatsiorsky VM (2005) Prehension synergies in three dimensions. J Neurophysiol 93:766–776
Singh T, SKM V, Zatsiorsky VM, Latash ML (2010a) Adaptive increase in force variance during fatigue in tasks with low redundancy. Neurosci Lett 485:201–207
Singh T, SKM V, Zatsiorsky VM, Latash ML (2010b) Fatigue and motor redundancy: adaptive increase in finger force variance in multi-finger tasks. J Neurophysiol 103:2990–3000
Taylor JL, Gandevia SC (2008) A comparison of central aspects of fatigue in submaximal and maximal voluntary contractions. J Appl Physiol 104:542–550
Vallejo G, Ato M, Valdés T (2008) Consequences of misspecifying the error covariance structure in linear mixed models for longitudinal data. Methodol Eur J Res Methods Behav Soc Sci 4:10–21
Vilaplana JM, Coronado JL (2006) A neural network model for coordination of hand gesture during reach to grasp. Neural Netw 19:12–30
Westling G, Johansson RS (1984) Factors influencing the force control during precision grip. Exp Brain Res 53:277–284
Westling G, Johansson RS (1987) Responses in glabrous skin mechanoreceptors during precision grip in humans. Exp Brain Res 66:128–140
Williams C, Shang D, Carnahan H (2010) Pressure is a viable controlled output of motor programming for object manipulation tasks. In: Kappers AML, van Erp JBF, Bergmann Tiest WM, van der Helm FCT (eds) Haptics: generating and perceiving tangible sensations. Springer, New York, pp 339–344
Winges SA, Santello M (2004) Common input to motor units of digit flexors during multi-digit grasping. J Neurophysiol 92:3210–3220
Yao W, Fuglevand RJ, Enoka RM (2000) Motor-unit synchronization increases EMG amplitude and decreases force steadiness of simulated contractions. J Neurophysiol 83:441–452
Zatsiorsky VM, Latash ML (2009) Digit forces in multi-digit grasps. In: Nowak DA, Hermsdörfer J (eds) Sensorimotor control of grasping: physiology and pathophysiology. Cambridge University Press, Cambridge, pp 33–51
Zatsiorsky VM, Latash ML, Gao F, Shim JK (2004) The principle of superposition in human prehension. Robotica 22:231–234
Zatsiorsky VM, Gao F, Latash ML (2005) Motor control goes beyond physics: differential effects of gravity and inertia on finger forces during manipulation of hand-held objects. Exp Brain Res 162:300–308
Zhang LQ, Rymer WZ (2001) Reflex and intrinsic changes induced by fatigue of human elbow extensor muscles. J Neurophysiol 86:1086–1094
Acknowledgments
The study was in part supported by NIH grants AG-018751, NS-035032, and AR-048563. We would also like to thank Cristián Cuadra González and Angelo Bartsch for their help with data collection.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Singh, T., Zatsiorsky, V.M. & Latash, M.L. Adaptations to fatigue of a single digit violate the principle of superposition in a multi-finger static prehension task. Exp Brain Res 225, 589–602 (2013). https://doi.org/10.1007/s00221-013-3403-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-013-3403-x