Experimental Brain Research

, Volume 181, Issue 1, pp 49–67

Threshold position control of arm movement with anticipatory increase in grip force

  • Jean-François Pilon
  • Sophie J. De Serres
  • Anatol G. Feldman
Research Article


The grip force holding an object between fingers usually increases before or simultaneously with arm movement thus preventing the object from sliding. We experimentally analyzed and simulated this anticipatory behavior based on the following notions. (1) To move the arm to a new position, the nervous system shifts the threshold position at which arm muscles begin to be recruited. Deviated from their activation thresholds, arm muscles generate activity and forces that tend to minimize this deviation by bringing the arm to a new position. (2) To produce a grip force, with or without arm motion, the nervous system changes the threshold configuration of the hand. This process defines a threshold (referent) aperture (Ra) of appropriate fingers. The actual aperture (Qa) is constrained by the size of the object held between the fingers whereas, in referent position Ra, the fingers virtually penetrate the object. Deviated by the object from their thresholds of activation, hand muscles generate activity and grip forces in proportion to the gap between the Qa and Ra. Thus, grip force emerges since the object prevents the fingers from reaching the referent position. (3) From previous experiences, the system knows that objects tend to slide off the fingers when arm movements are made and, to prevent sliding, it starts narrowing the referent aperture simultaneously with or somewhat before the onset of changes in the referent arm position. (4) The interaction between the fingers and the object is accomplished via the elastic pads on the tips of fingers. The pads are compressed not only due to the grip force but also due to the tangential inertial force (“load”) acting from the object on the pads along the arm trajectory. Compressed by the load force, the pads move back and forth in the gap between the finger bones and object, thus inevitably changing the normal component of the grip force, in synchrony with and in proportion to the load force. Based on these notions, we simulated experimental elbow movements and grip forces when subjects rapidly changed the elbow angle while holding an object between the index finger and the thumb. It is concluded that the anticipatory increase in the grip force with or without correlation with the tangential load during arm motion can be explained in neurophysiological and biomechanical terms without relying on programming of grip force based on an internal model.


Motor control Referent arm-hand configuration Threshold aperture Anticipatory actions Computer simulations 


  1. Adamovich SV, Burlachkova NI, Fel’dman AG (1984) A wave nature of the central regulation the trajectory of the articular angle in man. Biofizika 29:122–125PubMedGoogle Scholar
  2. Archambault PS, Mihaltchev P, Levin MF, Feldman AG (2005) Basic elements of arm postural control analyzed by unloading. Exp Brain Res 164(2):225–241PubMedCrossRefGoogle Scholar
  3. Asatryan DG, Feldman AG (1965) Functional tuning of the nervous system with control of movements or maintenance of a steady posture: I. Mechanographic analysis of the work of the joint on execution of a postural task. Biophysics 10:925–935Google Scholar
  4. Belen’kii VY, Gurfinkel VS, Pal’tsev Y (1967) Elements of control of voluntary movements, Biofizika 10:135–141Google Scholar
  5. Blakemore SJ, Goodbody SJ, Wolpert DM (1998) Predicting the consequences of our own actions: the role of sensorimotor context estimation. J Neurosci 18:7511–7518PubMedGoogle Scholar
  6. Boudreau MJ, Smith AM (2001) Activity in rostral motor cortex in response to predictable force-pulse perturbations in a precision grip task. J Neurophysiol 86(3):1079–1085PubMedGoogle Scholar
  7. Capaday C (1995) The effects of baclofen on the stretch reflex parameters of the cat. Exp Brain Res 104:287–296PubMedCrossRefGoogle Scholar
  8. Dancause N, Taylor MD, Plautz EJ, Radel JD, Whittaker T, Nudo RJ, Feldman AG (2007) A stretch reflex in extraocular muscles of species purportedly lacking muscle spindles. Exp Brain Res, Jan 10 (Epub ahead of print)Google Scholar
  9. Deuschl G, Feifel E, Guschlbauer B, Lucking CH (1995) Hand muscle reflexes following air puff stimulation. Exp Brain Res 105(1):138–46PubMedCrossRefGoogle Scholar
  10. Dubois DM (2001) Computing anticipatory systems. In: AIP conference proceedings 573XI:706Google Scholar
  11. Edin BB, Westling G, Johansson RS (1992) Independent control of human finger-tip forces at individual digits during precision lifting. J Physiol 450:547–564PubMedGoogle Scholar
  12. Fagergren A, Ekeberg Ö, Forssberg H (2003) Control strategies correcting inaccurately programmed fingertip forces: Model predictions derived from human behavior. J Neurophys 89:2904–2916CrossRefGoogle Scholar
  13. Fedirchuk B, Dai Y (2004) Monoamines increase the excitability of spinal neurones in the neonatal rat by hyperpolarizing the threshold for action potential production. J Physiol 557:355–561PubMedCrossRefGoogle Scholar
  14. Feldman AG (1993) The coactivation command for antagonist muscles involving Ib interneurons in mammalian motor control systems: An electrophysiologically testable model. Neurosci Let 155:167–170CrossRefGoogle Scholar
  15. Feldman AG (2007) Equilibrium point control (an essay). In: Karniel A (ed) Encyclopedic reference of neuroscience. Field: computational motor control (in press)Google Scholar
  16. Feldman AG, Levin FM (1995) The origin and use of positional frames of reference in motor control. Behav Brain Sci 18:723–806CrossRefGoogle Scholar
  17. Feldman AG, Latash ML (2005) Testing hypotheses and the advancement of sciences: recent attempts to falsify the equilibrium point hypothesis. Exp Brain Res 161:91–103PubMedCrossRefGoogle Scholar
  18. Feldman AG, Orlovsky GN (1972) The influence of different descending systems on the tonic stretch reflex in the cat. Exp Neurol 37(3):481–494PubMedCrossRefGoogle Scholar
  19. Feldman AG, Levin MF Mitnitski AM, Archambault P (1998) 1998 ISEK congress keynote lecture multi-muscle control in human movements. J Electromyogr Kin 8:383–390CrossRefGoogle Scholar
  20. Flanagan JR, Wing AM (1993) Modulation of grip force with load force during point-to-point arm movements. Exp Brain Res 95:131–143PubMedCrossRefGoogle Scholar
  21. Flanagan JR, Wing AM (1995) The stability of precision grip forces during cyclic arm movements with a hand-held load. Exp Brain Res 105(3):455–64PubMedGoogle Scholar
  22. Flanagan JR, Wing AM (1997) The role of internal models in motion planning and control: evidence from grip force adjustments during movements of hand-held loads. J Neurosci 17(4):1519–1528PubMedGoogle Scholar
  23. Flanagan JR, Ostry DJ, Feldman AG (1993) Control of trajectory modifications in target-directed reaching. J Mot Behav 25(3):140–152PubMedCrossRefGoogle Scholar
  24. Foisy M, Feldman AG (2006) Threshold control of arm posture and movement adaptation to load. Exp Brain Res 18 Jul 2006 (Epub ahead of print)Google Scholar
  25. Forget R, Lamarre Y (1995) Postural adjustments associated with different unloadings of the forearm: effects of proprioceptive and cutaneous afferent deprivation. Can J Physiol Pharmacol 73:285–294PubMedGoogle Scholar
  26. Gribble PL, Ostry DJ, Sanguineti V, Laboissière R (1998) Are complex control signals required for human arm movement? J Neurophysiol 79:1409–1424PubMedGoogle Scholar
  27. Grillner S (2003) The motor infrastructure: from ion channels to neuronal networks. Nat Rev Neurosci 4:573–586PubMedCrossRefGoogle Scholar
  28. Günther M, Ruder H (2003) Synthesis of two–dimensional human walking: a test of the λ–model. Biol Cybern 89(2):89–106PubMedCrossRefGoogle Scholar
  29. Gurfinkel VS, Lipshits MI, Lestienne FG (1988) Anticipatory neck muscle activity associated with rapid arm movements. Neurosci Lett 94(1–2):104–108PubMedCrossRefGoogle Scholar
  30. Henneman E (1981) Recruitment of motor neurons: the size principle. In: Desmedt JE (ed) Progress in clinical neurophysiology: motor units types, recruitment and plasticity in health and disease, vol 9. Karger, Basel Google Scholar
  31. Hodges PW, Gurfinkel VS, Brumagne S, Smith TC, Cordo PC (2002) Coexistence of stability and mobility in postural control: evidence from postural compensation for respiration. Exp Brain Res 144:293–302PubMedCrossRefGoogle Scholar
  32. Huxley H, Hanson J (1954) Changes in the cross-striations of muscle during contraction and stretch and their structural interpretation. Nature 173(4412):973–976PubMedCrossRefGoogle Scholar
  33. Issler H, Stephens JA (1983) The maturation of cutaneous reflexes studied in the upper limb in man. J Physiol 335:643–654PubMedGoogle Scholar
  34. Jenner JR, Stephens JA (1982) Cutaneous reflex responses and their central nervous pathways studied in man. J Physiol 333:405–419PubMedGoogle Scholar
  35. 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(3):550–564PubMedCrossRefGoogle Scholar
  36. Johansson RS, Westling G (1988) Programmed and triggered actions to rapid load changes during precision grip. Exp Brain Res 71:72–86PubMedGoogle Scholar
  37. Kawato M (1999) Internal models for motor control and trajectory planning. Curr Opin Neurobiol 9:718–727PubMedCrossRefGoogle Scholar
  38. Laboissière R, Ostry DJ, Feldman AG (1996) The control of multi-muscle systems: human jaw and hyoid movements. Biol Cybern 74:373–384PubMedCrossRefGoogle Scholar
  39. Latash ML, Li S, Danion F, Zatsiorsky VM (2002) Central mechanisms of finger interaction during one- and two-hand force production at distal and proximal phalanges. Brain Research 924:198–208PubMedCrossRefGoogle Scholar
  40. Lepelley MC, Thullier F, Koral J, Lestienne FG (2006) Muscle coordination in complex movements during Jete in skilled ballet dancers. Exp Brain Res 175:321–331PubMedCrossRefGoogle Scholar
  41. Lestienne FG, Thullier F, Archambault P, Levin MF, Feldman AG (2000) Multi-muscle control of head movements in monkeys: the referent configuration hypothesis. Neurosci Lett 283(1):65–68PubMedCrossRefGoogle Scholar
  42. Levin MF, Dimov M (1997) Spatial zones for muscle coactivation and the control of postural stability. Brain Res 757(1):43–59PubMedCrossRefGoogle Scholar
  43. Li S, Danion F, Latash ML, Li Z-M, Zatsiorsky VM (2000) Finger coordination in multi-finger force production tasks involving fingers of the right hand and/or fingers of the left hand. J Appl Biomech 16:379–391Google Scholar
  44. Li S, Danion F, Latash ML, Li Z-M, Zatsiorsky VM (2001) Bilateral deficit and symmetry in finger force production during two-hand multi-finger tasks. Exp Brain Res 141:530–540PubMedCrossRefGoogle Scholar
  45. Matthews PBC (1959) A study of certain factors influencing the stretch reflex of the decerebrate cat. J Physiol 147:547–564PubMedGoogle Scholar
  46. Munoz DP, Pelisson D, Guitton D (1991) Movement of neural activity on the superior colliculus motor map during gaze shifts. Science 251:1358–60PubMedCrossRefGoogle Scholar
  47. Nichols TR, Steeves JD (1986) Resetting of resultant stiffness in ankle flexor and extensor muscles in the decerebrated cat. Exp Brain Res 62:401–410PubMedCrossRefGoogle Scholar
  48. Ostry DA, Feldman AG (2003) A critical evaluation of the force control hypothesis in motor control. Exp Brain Res 153:275–288PubMedCrossRefGoogle Scholar
  49. Picard N, Smith AM (1992a) Primary motor cortical responses to perturbations of prehension in the monkey. J Neurophysiol 68(5):1882–94Google Scholar
  50. Picard N, Smith AM (1992b) Primary motor cortical activity related to the weight and texture of grasped objects in the monkey. J Neurophysiol 68(5):1867–1881Google Scholar
  51. Pilon J-F, Feldman AG (2006) Threshold control of motor actions prevents destabilizing effects of proprioceptive delays. Exp Brain Res 174(2):229–239PubMedCrossRefGoogle Scholar
  52. Pilon J-F, De Serres SJ, Feldman AG (2005a) Precision grip during arm movement examined in the context of threshold control. In: Proceedings of progress in motor control V conference, Pennsylvania (USA)Google Scholar
  53. Pilon J-F, De Serres SJ, Feldman AG (2005b) Threshold control of arm movement while holding an objects: no need for invoking internal models. In: The 35th Neuroscience meeting (abstracts)Google Scholar
  54. Rosen R (1985) Anticipatory systems. Philosophical, mathematical and methodological foundations. Pergamon, New YorkGoogle Scholar
  55. Serina ER, Mote CD Jr, Rempel D (1997) Force response of the fingertip pulp to repeated compression–effects of loading rate, loading angle and anthropometry. J Biomech 30(10):1035–1040PubMedCrossRefGoogle Scholar
  56. Serina ER, Mockensturm E, Mote CD Jr, Rempel D (1998) A structural model of the forced compression of the fingertip pulp. J Biomech 31(7):639–646PubMedCrossRefGoogle Scholar
  57. St-Onge N, Feldman AG (2004) Referent configuration of the body: a global factor in the control of multiple skeletal muscles. Exp Brain Res 155:291–300PubMedCrossRefGoogle Scholar
  58. St-Onge N, Adamovich SV, Feldman AG (1997) Control processes underlying elbow flexion movements may be independent of kinematic and electromyographic patterns: experimental study and modelling. Neurosci 79(1):295–316CrossRefGoogle Scholar
  59. Weeks DL, Aubert MP, Feldman AG, Levin MF (1996) One-trial adaptation of movement to changes in load. J Neurophysiol 75(1):60–74PubMedGoogle Scholar
  60. Wolpert DM, Kawato M (1998) Multiple-paired forward and inverse models for motor control. Neural Netw 11:1317–1329PubMedCrossRefGoogle Scholar
  61. Wu JZ, Dong RG, Smutz WP, Schopper AW (2003) Modeling of time-dependant force responses of fingertip to dynamic loading. J Biomech 36:383–392PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Jean-François Pilon
    • 1
    • 2
  • Sophie J. De Serres
    • 3
    • 4
  • Anatol G. Feldman
    • 1
    • 2
    • 3
  1. 1.Department of Physiology, Neurological Science Research Center, Institute of Biomedical EngineeringUniversity of MontrealMontrealCanada
  2. 2.Center for Interdisciplinary Research in Rehabilitation (CRIR)Rehabilitation Institute of MontrealMontrealCanada
  3. 3.Center for Interdisciplinary Research in RehabilitationJewish Rehabilitation HospitalLavalCanada
  4. 4.School of Physical and Occupational TherapyMcGill UniversityMontrealCanada

Personalised recommendations