Experimental Brain Research

, Volume 236, Issue 10, pp 2531–2544 | Cite as

Intermittent coupling between grip force and load force during oscillations of a hand-held object

  • Francis Grover
  • Maurice Lamb
  • Scott Bonnette
  • Paula L. Silva
  • Tamara Lorenz
  • Michael A. RileyEmail author
Research Article


Tightly coordinated grip force adaptations in response to changing load forces have been reported as continuous, stable, and proportional to the load force changes. Considering the existence of inherent sensorimotor feedback delays, current accounts of grip force–load force coupling invoke explicit predictive mechanisms in the form of internal models for feedforward control to account for anticipatory grip force modulations. However, recent findings suggest that the stability and regularity of grip force–load force coupling is less persistent than previously thought. Thus, the objective of the current study was to comprehensively quantify the time-varying characteristics of grip force–load force coupling. Investigations into the coupling’s dynamics during continuous 30 s bouts of load force oscillation revealed intermittent phases of coordination, as well as phases that varied in stability, rather than a persistent and continuously stable pattern of coordination. These findings have important implications for accounts of grip force–load force coupling and of anticipation in motor control, more broadly.


Grip Coupling Intermittency Cross-recurrence quantification analysis 


  1. Ambike S, Zhou T, Zatsiorsky VM, Latash ML (2015) Moving a hand-held object: Reconstruction of referent coordinate and apparent stiffness trajectories. Neuroscience 298:336–356. CrossRefPubMedPubMedCentralGoogle Scholar
  2. Augurelle AS, Smith AM, Lejeune T, Thonnard JL (2003) Importance of cutaneous feedback in maintaining a secure grip during manipulation of hand-held objects. J Neurophysiol 89(2):665–671. CrossRefPubMedGoogle Scholar
  3. Blakemore SJ, Goodbody SJ, Wolpert DM (1998) Predicting the consequences of our own actions: the role of sensorimotor context estimation. J Neurosci, 18(18), 7511–7518CrossRefPubMedGoogle Scholar
  4. Blank R, Breitenbach A, Nitschke M, Heizer W, Letzgus S, Hermsdörfer J (2001) Human development of grip force modulation relating to cyclic movement-induced inertial loads. Exp Brain Res 138(2):193–199. CrossRefPubMedGoogle Scholar
  5. Byblow WD, Carson RG, Goodman D (1994) Expressions of asymmetries and anchoring in bimanual coordination. Hum Mov Sci 13:3–28CrossRefGoogle Scholar
  6. Coco MI, Dale R (2016) Cross-recurrence quantification analysis of categorical and continuous time series: an R package. Front Psychol 5(355):1–31. CrossRefGoogle Scholar
  7. Cole KJ (1991) Grasp force control in older adults. J Mot Behav 23(4):251–258CrossRefPubMedGoogle Scholar
  8. Cole KJ, Abbs JH (1988) Grip force adjustments evoked by load force perturbations of a grasped object. J Neurophysiol 60(4):1513–1522CrossRefPubMedGoogle Scholar
  9. Cole KJ, Rotella DL, Harper JG (1999) Mechanisms for age-related changes of fingertip forces during precision gripping and lifting in adults. J Neurosci 19(8):3238–3247CrossRefPubMedGoogle Scholar
  10. Danion F (2004) How dependent are grip force and arm actions during holding an object? Exp Brain Res 158(1):109–119. CrossRefPubMedGoogle Scholar
  11. Danion F, Sarlegna FR (2007) Can the human brain predict the consequences of arm movement corrections when transporting an object? Hints from grip force adjustments. J Neurosci 27(47):12839–12843. CrossRefPubMedGoogle Scholar
  12. Danion F, Descoins M, Bootsma RJ (2007) Aging affects the predictive control of grip force during object manipulation. Exp Brain Res 180(1):123–137. CrossRefPubMedGoogle Scholar
  13. Danion F, Descoins M, Bootsma RJ (2009) When the fingers need to act faster than the arm: coordination between grip force and load force during oscillation of a hand-held object. Exp Brain Res 193(1):85–94. CrossRefPubMedGoogle Scholar
  14. Faisal AA, Selen LPJ, Wolpert DM (2008) Noise in the nervous system. Nat Rev Neurosci 9(4):292–303. CrossRefPubMedPubMedCentralGoogle Scholar
  15. Fink PW, Foo P, Jirsa VK, Kelso JS (2000) Local and global stabilization of coordination by sensory information. Exp Brain Res 134(1):9–20. CrossRefPubMedGoogle Scholar
  16. Flanagan JR, Tresilian JR (1994) Grip-load force coupling: a general control strategy for transporting objects. J Exp Psychol Hum Percept Perform 20(5):944–957CrossRefPubMedGoogle Scholar
  17. Flanagan JR, Wing AM (1993) Modulation of grip force with load force during point-to-point arm movements. Exp Brain Res 95(1):131–143. CrossRefPubMedGoogle Scholar
  18. 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):455–464. CrossRefPubMedGoogle Scholar
  19. 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):1519–1528. CrossRefPubMedGoogle Scholar
  20. Flanagan JR, Treslihan J, Wing AM (1993) Coupling of grip force and load force during arm movements with grasped objects. Neurosci Lett 152(1):53–56. CrossRefPubMedGoogle Scholar
  21. Flanagan JR, Bowman MC, Johansson RS (2006) Control strategies in object manipulation tasks. Curr Opin Neurobiol 16(6):650–659. CrossRefPubMedGoogle Scholar
  22. Gysin P, Kaminski TR, Hass CJ, Grobet CE, Gordon AM (2008) Effects of gait variations on grip force coordination during object transport. J Neurophysiol 100(5):2477–2485. CrossRefPubMedGoogle Scholar
  23. Hadjiosif AM, Smith MA (2015) Flexible control of safety margins for action based on environmental variability. J Neurosci 35(24):9106–9121. CrossRefPubMedPubMedCentralGoogle Scholar
  24. Jaric S, Russell EM, Collins JJ, Marwaha R (2005) Coordination of hand grip and load forces in uni- and bidirectional static force production tasks. Neurosci Lett 381(1–2):51–56. CrossRefPubMedGoogle Scholar
  25. 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):550–564. CrossRefPubMedGoogle Scholar
  26. Johansson RS, Westling G (1987) Signals in tactile afferents from the fingers eliciting adaptive motor responses during precision grip. Exp Brain Res 66(1):141–154. CrossRefPubMedGoogle Scholar
  27. Johansson RS, Häger C, Bäckström L (1992) Somatosensory control of precision grip during unpredictable pulling loads. Exp Brain Res 89(1):204–213CrossRefPubMedGoogle Scholar
  28. Kawato M (1999) Internal models for motor control and trajectory planning. Curr Opin Neurobiol 9(6):718–727. CrossRefPubMedGoogle Scholar
  29. Kay BA, Kelso JAS, Saltzman EL, Schöner G (1987) Space–time behavior of single and bimanual rhythmical movements: data and limit cycle model. J Exp Psychol Hum Percept Perform 13(2):178–192. CrossRefPubMedGoogle Scholar
  30. Kudo K, Park H, Kay BA, Turvey MT (2006) Environmental coupling modulates the attractors of rhythmic coordination. J Exp Psychol Hum Percept Perform 32(3):599–609. CrossRefPubMedGoogle Scholar
  31. Latash ML, Friedman J, Kim SW, Feldman AG, Zatsiorsky VM (2010) Prehension synergies and control with referent hand configurations. Exp Brain Res 202(1):213–229. CrossRefPubMedGoogle Scholar
  32. Loram ID, Maganaris CN, Lakie M (2005) Human postural sway results from frequent, ballistic bias impulses by soleus and gastrocnemius. J Physiol 564(1):295–311. CrossRefPubMedPubMedCentralGoogle Scholar
  33. Loram ID, Gollee H, Lakie M, Gawthrop PJ (2011) Human control of an inverted pendulum: Is continuous control necessary? Is intermittent control effective? Is intermittent control physiological? J Physiol 589(2):307–324. CrossRefPubMedGoogle Scholar
  34. Marwan N, Kurths J (2002) Nonlinear analysis of bivariate data with cross recurrence plots. Phys Lett Sect A Gen At Solid State Phys 302(5–6):299–307. CrossRefGoogle Scholar
  35. Marwan N, Wessel N, Meyerfeldt U, Schirdewan A, Kurths J (2002) Recurrence-plot-based measures of complexity and their application to heart-rate-variability data. Phys Rev E Stat Nonlinear Soft Matter Phys 66(2):1–8. CrossRefGoogle Scholar
  36. Meyer DE, Abrams RA, Kornblum S, Wright CE, Smith JEK (1988) Optimality in human motor performance: ideal control of rapid aimed movements. Psychol Rev 95(3):340–370CrossRefPubMedGoogle Scholar
  37. Miall RC, Wolpert DM (1996) Forward models for physiological motor control. Neural Netw 9(8):1265–1279CrossRefPubMedGoogle Scholar
  38. Milton JG (2013) Intermittent motor control: the “drift-and-act” hypothesis. In: Richardson MJ, Riley MA, Shockley K (eds) Progress in motor control. Springer, Berlin, pp 169–193. httpsCrossRefGoogle Scholar
  39. Mitra S, Riley MA, Turvey MT (1997) Chaos in human rhythmic movement. J Mot Behav 29(3):195–198. CrossRefPubMedGoogle Scholar
  40. Monzée J, Lamarre Y, Smith AM (2003) The effects of digital anesthesia on force control using a precision grip the effects of digital anesthesia on force control using a precision grip. J Neurophysiol 89:672–683. CrossRefPubMedGoogle Scholar
  41. Neilson PD, Neison MD, O’Dwyer NJ (1995) Adaptive optimal control of human tracking. In: Glencross DJ, Piek JP (eds) Motor control and sensory-motor integration: issues and directions. North Holland, Amsterdam, pp 97–140. CrossRefGoogle Scholar
  42. Newell KM, Slifkin AB (1998) The nature of movement variability. In: Piek JP (ed) Motor behavior and human skill: a multidisciplinary approach. Human Kinetics, Champaign, pp 143–160Google Scholar
  43. Nowak DA, Hermsdörfer J, Glasauer S, Philipp J, Meyer L, Mai N (2001) The effects of digital anaesthesia on predictive grip force adjustments during vertical movements of a grasped object. Eur J Neurosci 14(4):756–762. CrossRefPubMedGoogle Scholar
  44. Nowak DA, Hermsdörfer J, Marquardt C, Fuchs HH (2002) Grip and load force coupling during discrete vertical arm movements with a grasped object in cerebellar atrophy. Exp Brain Res 145(1):28–39. CrossRefPubMedGoogle Scholar
  45. Pilon JF, De Serres SJ, Feldman AG (2007) Threshold position control of arm movement with anticipatory increase in grip force. Exp Brain Res 181(1):49–67. CrossRefPubMedGoogle Scholar
  46. Ramdani S, Seigle B, Lagarde J, Bouchara F, Bernard PL (2009) On the use of sample entropy to analyze human postural sway data. Med Eng Phys 31(8):1023–1031. CrossRefPubMedGoogle Scholar
  47. Richman JS, Moorman JR (2000) Physiological time-series analysis using approximate entropy and sample entropy. Am J Physiol Heart Circ Physiol 276(6):H2039-2049Google Scholar
  48. Richman JS, Lake DE, Moorman JR (2004) Sample entropy. Methods Enzymol 384:172–184. CrossRefPubMedGoogle Scholar
  49. Riley MA, Turvey MT (2002) Variability and determinism in motor behavior. J Mot Behav 34(2):99–125. CrossRefPubMedGoogle Scholar
  50. Rosenblum MG, Pikovsky AS (2001) Detecting direction of coupling in interacting oscillators. Phys Rev E Stat Nonlinear Soft Matter Phys 64(4–5):45202. CrossRefGoogle Scholar
  51. Rosenblum MG, Cimponeriu L, Bezerianos A, Patzak A, Mrowka R (2002) Identification of coupling direction: application to cardiorespiratory interaction. Phys Rev E Stat Nonlinear Soft Matter Phys 65(4):11. CrossRefGoogle Scholar
  52. Slota GP, Latash ML, Zatsiorsky VM (2011) Grip forces during object manipulation: experiment, mathematical model, and validation. Exp Brain Res 213(1):125–139. CrossRefPubMedPubMedCentralGoogle Scholar
  53. Stepp N (2009) Anticipation in feedback-delayed manual tracking of a chaotic oscillator. Exp Brain Res 198(4):521–525. CrossRefPubMedPubMedCentralGoogle Scholar
  54. Stepp N, Turvey MT (2009) On strong anticipation. Cogn Syst Res 11(2):148–164CrossRefGoogle Scholar
  55. Viviani P, Lacquaniti F (2015) Grip forces during fast point-to-point and continuous hand movements. Exp Brain Res 233(11):3201–3220. CrossRefPubMedGoogle Scholar
  56. Washburn A, Kallen RW, Coey CA, Shockley K, Richardson MJ (2015) Harmony from chaos? Perceptual-motor delays enhance behavioral anticipation in social interaction. J Exp Psychol Hum Percept Perform 41(4):1166–1177. CrossRefPubMedPubMedCentralGoogle Scholar
  57. Webber CL Jr., Marwan N (eds). (2015). Recurrence quantification analysis: theory and best practices. Am J Respir Crit Care Med.
  58. Webber CL, Zbilut JP (1994) Dynamical assessment of physiological systems and states using recurrence plot strategies. J Appl Physiol 76(2):965–973CrossRefPubMedGoogle Scholar
  59. Wing AM, Lederman SJ (1998) Anticipating load torques produced by voluntary movements. J Exp Psychol Hum Percept Perform 24(6):1571–1581. CrossRefPubMedGoogle Scholar
  60. Wolpert DM, Flanagan JR (2001) Motor prediction. Curr Biol 11(18):R729–R732. CrossRefGoogle Scholar
  61. 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(3):300–308. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Francis Grover
    • 1
  • Maurice Lamb
    • 1
  • Scott Bonnette
    • 2
  • Paula L. Silva
    • 1
  • Tamara Lorenz
    • 1
    • 3
    • 4
  • Michael A. Riley
    • 1
    Email author
  1. 1.Center for Cognition, Action, and Perception, Department of Psychology, ML 0376, Edwards Center 1University of CincinnatiCincinnatiUSA
  2. 2.Division of Sports MedicineCincinnati Children’s Hospital Medical CenterCincinnatiUSA
  3. 3.Department of Mechanical and Materials EngineeringUniversity of CincinnatiCincinnatiUSA
  4. 4.Department of Electrical Engineering and Computer ScienceUniversity of CincinnatiCincinnatiUSA

Personalised recommendations