Advertisement

Experimental Brain Research

, Volume 108, Issue 1, pp 172–184 | Cite as

Control of grip force during restraint of an object held between finger and thumb: responses of muscle and joint afferents from the digits

  • Vaughan G. Macefield
  • Ronald S. Johansson
Research Article

Abstract

Pulling or pushing forces applied to an object gripped between finger and thumb excite tactile afferents in the digits in a manner awarding these afferents probable roles in triggering the reactive increases in grip force and in scaling the changes in grip force to the changes in applied load-force. In the present study we assessed the possible contributions from slowly adapting afferents supplying muscles involved in the generation of grip forces and from digital joint afferents. Impulses were recorded from single afferents via tungsten microelectrodes inserted percutaneously into the median or ulnar nerves of awake human subjects. The subject held a manipulandum with a precision grip between the receptor-related digit (index finger, middle finger, ring finger or thumb) and an opposing digit (thumb or index finger). Ramp-and-hold load forces of various amplitudes (0.5–2.0 N) and ramp rates (2–32 N/s) were delivered tangential to the parallel grip surfaces in both the distal (pulling) and the proximal (pushing) directions. Afferents from the long flexors of the digits (n=19), regardless of their muscle-spindle or tendon-organ origin, did not respond to the load forces before the onset of the automatic grip response, even with the fastest ramp rates. Their peak discharge closely followed the peak rate of increase in grip force. During the hold phase of the load stimulus, the afferents sustained a tonic discharge. The discharge rates were significantly lower with proximally directed loads despite the mean grip-force being similar in the two directions. This disparity could be explained by the differing contributions of these muscles to the finger-tip forces necessary to restrain the manipulandum in the two directions. Most afferents from the short flexors of the digits (n=17), including the lumbricals, dorsal interossei, opponens pollicis, and flexor pollicis brevis, did not respond at all, even with the fastest ramps. Furthermore, the ensemble pattern from the joint afferents (n=6) revealed no significant encoding of changes in finger-tip forces before the onset of the increase in grip force. We conclude that mechanoreceptors in the flexors of the digits and in the interphalangeal joints cannot be awarded a significant role in triggering the automatic changes in grip force. Rather, their responses appeared to reflect the reactive forces generated by the muscles to restrain the object. Hence, it appears that tactile afferents of the skin in contact with the object are the only species of receptor in the hand capable of triggering and initially scaling an appropriate change in grip force in response to an imposed change in load force, but that muscle and joint afferents may provide information related to the reactive forces produced by the subject.

Key words

Muscle afferents Joint afferents Precision grip Hand Sensorimotor integration Human 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Al-Falahe NA, Nagaoka M, Vallbo ÅB (1990) Response profiles of human muscle afferents during active finger movements. Brain 113:325–346Google Scholar
  2. Burke D, Gandevia SC (1995) The human muscle spindle and its fusimotor control. In: Ferrell WR, Proske U (eds) Neural control of movement. Plenum, New York pp 19–25Google Scholar
  3. Burke D, Gandevia SC, Macefield G (1988) Responses to passive movement of receptors in joint, skin and muscle of the human hand. J Physiol (Lond) 402:347–361Google Scholar
  4. Cole KJ, Abbs JA (1988) Grip force adjustments evoked by load force perturbations of a grasped object. J Neurophysiol 60:1513–1522Google Scholar
  5. Edin BB (1990) Finger joint movement sensitivity of non-cutaneous mechanoreceptor afferents in the human radial nerve. Exp Brain Res 82:417–422Google Scholar
  6. Edin BB, Abbs JH (1991) Finger movement responses of cutaneous mechanoreceptors in the dorsal skin of the human hand. J Neurophysiol 65:657–670Google Scholar
  7. Edin BB, Vallbo ÅB (1990a) Dynamic response of human muscle spindle afferents to stretch. J Neurophysiol 63:1297–1306Google Scholar
  8. Edin BB, Vallbo ÅB (1990b) Muscle afferent responses to isometric contractions and relaxations in humans. J Neurophysiol 63:1307–1313Google Scholar
  9. Edin BB, Westling G, Johansson RS (1992) Independent control of finger tip forces at individual digits during precision lifting in humans. J Physiol (Lond) 450:547–564Google Scholar
  10. Grigg P, Hoffman AH (1982) Properties of Ruffini afferents revealed by stress analysis of isolated sections of cat knee capsule. J Neurophysiol 47:41–54Google Scholar
  11. Häger-Ross C, Johansson RS (in press). Non-digital afferent input in reactive control of fingertip forces during precision grip. Exp Brain ResGoogle Scholar
  12. Häger-Ross C, Cole KJ, Johansson RS (In press). Grip force responses to unanticipated object loading: load direction reveals body- and gravity-referenced intrinsic variables. Exp Brain ResGoogle Scholar
  13. Johansson RS, Cole KJ (1994) Grasp stability during manipulative actions. Can J Physiol Pharmacol 72:511–524Google Scholar
  14. 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 56:550–564Google Scholar
  15. Johansson RS, Westling G (1987) Signals in tactile afferents from the fingers eliciting adaptive motor responses during precision grip. Exp Brain Res 66:141–154PubMedGoogle Scholar
  16. Johansson RS, Westling G (1988) Programmed and reflex actions to rapid load changes during precision grip. Exp Brain Res71:59–71Google Scholar
  17. Johansson RS, Westling G (1991) Afferent signals during manipulative tasks in man. In: Franzen O, Westman J (eds) Somatosensory mechanisms. Macmillan, London, pp 25–48Google Scholar
  18. Johansson RS, Riso R, Häger C, Bäckström L (1992a) Somatosensory control of precision grip during unpredictable pulling loads. I. Changes in load force amplitude. Exp Brain Res 89:181–191Google Scholar
  19. Johansson RS, Häger C, Riso R (1992b) Somatosensory control of precision grip during unpredictable pulling loads. II. Changes in load force rate. Exp Brain Res 89:192–203Google Scholar
  20. Johansson RS, Häger C, Bäckström L (1992c) Somatosensory control of precision grip during unpredictable pulling loads. III. Impairments during digital anesthesia. Exp Brain Res 89:204–213Google Scholar
  21. Johansson RS, Lemon RN, Westling G (1994) Time varying enhancement of human cortical excitability mediated by cutaneous inputs during precision grip. J Physiol (Lond) 481:761–775Google Scholar
  22. Jones LA, Hunter IW (1992) Changes in pinch force with bidirectional load forces. J Mot Behav 24:157–164Google Scholar
  23. Macefield VG, Johansson RS (1993) Behaviour of human muscle afferents from the digits during restraint of an object held in the precision grip. Soc Neurosci Abstr 19:228. 15PGoogle Scholar
  24. Macefield G, Gandevia SC, Burke D (1990) Perceptual responses to microstimulation of single afferents innervating joints, muscles and skin of the human hand. J Physiol (Lond) 429:113–129Google Scholar
  25. Macefield VG, Häger-Ross C, Johansson RS (1996) Control of grip force during restraint of an object held between finger and thumb: responses of cutaneous afferents from the digits. Exp Brain Res 108: 155–171Google Scholar
  26. Smith AM (1981) The coactivation of antagonist muscles. Can J Physiol Pharmacol 59:733–747Google Scholar
  27. Vallbo ÅB (1971) Muscle spindle response at the onset of isometic voluntary contractions in man. Time difference between fusimotor and skeletomotor effects. J Physiol (Lond) 318:405–431Google Scholar
  28. Winstein CJ, Abbs JH, Petashnick D (1991) Influences of object weight and instruction on grip force adjustments. Exp Brain Res 87:465–469Google Scholar

Copyright information

© Springer-Verlag 1996

Authors and Affiliations

  • Vaughan G. Macefield
    • 1
  • Ronald S. Johansson
    • 1
  1. 1.Department of PhysiologyUmeå UniversitySweden

Personalised recommendations