Skip to main content
Log in

Adaptations to fatigue of a single digit violate the principle of superposition in a multi-finger static prehension task

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

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

    Google Scholar 

  • Balestra C, Duchateau J, Hainaut K (1992) Effects of fatigue on the stretch reflex in a human muscle. Electroencephalogr Clin Neurophysiol 85:46–52

    Article  PubMed  CAS  Google Scholar 

  • Baud-Bovy G, Soechting JF (2001) Two virtual fingers in the control of the tripod grasp. J Neurophysiol 86:604–615

    PubMed  CAS  Google Scholar 

  • Bigland B, Lippold OCJ (1954) Motor unit activity in the voluntary contraction of human muscle. J Physiol 125:322–335

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Cain W, Stevens J (1971) Effort in sustained and phasic handgrip contractions. Am J Psychol 84:52–65

    Article  PubMed  CAS  Google Scholar 

  • Contessa P, Adam A, DeLuca CJ (2009) Motor unit control and force fluctuation during fatigue. J Appl Physiol 107:235–243

    Article  PubMed  Google Scholar 

  • Cutkosky MR (1989) On grasp choice, grasp models, and the design of hands for manufacturing tasks. IEEE Trans Robot Autom 5:269–279

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Feldman AG (1986) Once more on the equilibrium-point hypothesis (lambda model) for motor control. J Mot Behav 18:17–54

    PubMed  CAS  Google Scholar 

  • Feldman AG (2009) New insights into action–perception coupling. Exp Brain Res 194:39–58

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Fuglevand AJ (1996) Neural aspects of fatigue. Neuroscientist 2:203–206

    Article  Google Scholar 

  • Gandevia SC (2001) Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 81:1725–1790

    PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Gorniak SL, Zatsiorsky VM, Latash ML (2009) Hierarchical control of static prehension: I. Biomechanics. Exp Brain Res 193:615–631

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Hockensmith GB, Lowell SY, Fuglevand AJ (2005) Common input across motor nuclei mediating precision grip in humans. J Neurosci 25:4560–4564

    Article  PubMed  CAS  Google Scholar 

  • Iberall T (1997) Human prehension and dexterous robot hands. Int J Robot Res 16:285–299

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Jones LA, Hunter IW (1983) Force and EMG correlates of constant effort contractions. Eur J Appl Physiol Occup Physiol 51:75–83

    Article  PubMed  CAS  Google Scholar 

  • Latash ML (2010) Motor synergies and the equilibrium-point hypothesis. Mot Control 14:294–322

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Mason MT (2001) Mechanics of robotic manipulation. The MIT Press, Cambridge

    Google Scholar 

  • Mason MT, Salisbury JK (1985) Robot hands and the mechanics of manipulation. The MIT Press, Cambridge

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Pataky TC (2005) Soft tissue strain energy minimization: a candidate control scheme for intra-finger normal–tangential force coordination. J Biomech 38:1723–1727

    Article  PubMed  Google Scholar 

  • Pataky TC, Latash ML, Zatsiorsky VM (2004) Tangential load sharing among fingers during prehension. Ergonomics 47:876–889

    Article  PubMed  Google Scholar 

  • Prattichizzo D, Trinkle JC (2008) Grasping. In: Siciliano B, Khatib O (eds) Springer handbook of robotics. Springer, Berlin, pp 671–700

    Chapter  Google Scholar 

  • Savescu AV, Latash ML, Zatsiorsky VM (2008) A technique to determine friction at the finger tips. J Appl Biomech 24:43–50

    PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Shim JK, Latash ML, Zatsiorsky VM (2005) Prehension synergies in three dimensions. J Neurophysiol 93:766–776

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Taylor JL, Gandevia SC (2008) A comparison of central aspects of fatigue in submaximal and maximal voluntary contractions. J Appl Physiol 104:542–550

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Vilaplana JM, Coronado JL (2006) A neural network model for coordination of hand gesture during reach to grasp. Neural Netw 19:12–30

    Article  PubMed  Google Scholar 

  • Westling G, Johansson RS (1984) Factors influencing the force control during precision grip. Exp Brain Res 53:277–284

    Article  PubMed  CAS  Google Scholar 

  • Westling G, Johansson RS (1987) Responses in glabrous skin mechanoreceptors during precision grip in humans. Exp Brain Res 66:128–140

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Zatsiorsky VM, Latash ML, Gao F, Shim JK (2004) The principle of superposition in human prehension. Robotica 22:231–234

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Zhang LQ, Rymer WZ (2001) Reflex and intrinsic changes induced by fatigue of human elbow extensor muscles. J Neurophysiol 86:1086–1094

    PubMed  CAS  Google Scholar 

Download references

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

Authors

Corresponding author

Correspondence to Tarkeshwar Singh.

Rights and permissions

Reprints 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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-013-3403-x

Keywords

Navigation