Experimental Brain Research

, Volume 66, Issue 1, pp 141–154

Signals in tactile afferents from the fingers eliciting adaptive motor responses during precision grip

  • R. S. Johansson
  • G. Westling


While human subjects lift small objects using the precision grip between the tips of the fingers and thumb the ratio between the grip force and the load force (i.e. the vertical lifting force) is adapted to the friction between the object and the skin. The present report provides direct evidence that signals in tactile afferent units are utilized in this adaptation. Tactile afferent units were readily excited by small but distinct slips between the object and the skin revealed as vibrations in the object. Following such afferent slip responses the force ratio was upgraded to a higher, stable value which provided a safety margin to prevent further slips. The latency between the onset of the a slip and the appearance of the ratio change (74 ±9 ms) was about half the minimum latency for intended grip force changes triggered by cutaneous stimulation of the fingers. This indicated that the motor responses were automatically initiated. If the subjects were asked to very slowly separate their thumb and the opposing finger while the object was held in air, grip force reflexes originating from afferent slip responses appeared to counteract the voluntary command, but the maintained upgrading of the force ratio was suppressed. In experiments with weak electrical cutaneous stimulation delivered through the surfaces of the object it was established that tactile input alone could trigger the upgrading of the force ratio. Although, varying in responsiveness, each of the three types of tactile units which exhibit a pronounced dynamic sensitivity (FA I, FA II and SA I units) could reliably signal these slips. Similar but generally weaker afferent responses, sometimes followed by small force ratio changes, also occurred in the FA I and the SA I units in the absence of detectable vibrations events. In contrast to the responses associated with clear vibratory events, the weaker afferent responses were probably caused by localized frictional slips, i.e. slips limited to small fractions of the skin area in contact with the object. Indications were found that the early adjustment to a new frictional condition, which may appear soon (ca. 0.1–0.2 s) after the object is initially gripped, might depend on the vigorous responses in the FA I units during the initial phase of the lifts (see Westling and Johansson 1987). The role of the tactile input in the adaptation of the force coordination to the frictional condition is discussed.

Key words

Precision grip Motor control Human hand Cutaneous mechanoreceptors Exteroceptive reflexes Sensori-motor memory 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Bonnet M, Requin J (1982) Long loop and spinal reflexes in man during preparation for intended directional hand movements. J Neurosci 2: 90–96Google Scholar
  2. Beradelli A, Day BL, Marsden CD, Rothwell JC (1985) Habituation of the human long latency stretch reflex. J Physiol (Lond) 362: 27PGoogle Scholar
  3. Burgess PR, Perl ER (1973) Cutaneous mechanoreceptors andn ociceptors. In: Iggo A (ed) Somatosensory system. Handbook of sensory physiology, Vol. II. Springer, Berlin, pp 29–78Google Scholar
  4. Caccia MR, McComas AJ, Upton ARM, Blogg T (1973) Cutaneous reflexes in small muscles of the hand. J Neurol Neurosurg Psychiat: 36: 960–977Google Scholar
  5. Crenna P, Frigo C (1984) Evidence of phase-dependent nociceptive reflexes during locomotion in man. Exp Neurol 85: 336–345Google Scholar
  6. Darton K, Lippold OCJ, Shahani M, Shahani U (1985) Longlatency spinal reflexes in humans. J Neurophysiol 53: 1604–1618Google Scholar
  7. Eklund G, Hagbarth KE, Torebjörk E (1978) Exteroceptive vibration-induced finger flexion reflex in man. J Neurol Neurosurg Psychiat 41: 438–443Google Scholar
  8. Evarts EV, Tanji J (1974) Gating of motor cortex reflexes by prior instruction. Brain Res 71: 479–494Google Scholar
  9. Gandevia SC, McCloskey DI (1977) Effects of related sensory inputs on motor performance in man studied through changes in perceived heaviness. J Physiol (Lond) 272: 653–672Google Scholar
  10. Garnett R, Stephens JA (1980) The reflex responses of single motor units in human first dorsal interosseous muscle following cutaneous afferent stimulation. J Physiol (Lond) 303: 351–364Google Scholar
  11. Garnett R, Stephens JA (1981) Changes in the recruitment threshold of motor units in the first human dorsal interosseous muscle following cutaneous afferent stimulation. J Physiol (Lond) 311: 463–473Google Scholar
  12. Grillner S (1981) Control of locomotion in bipeds, tetrapods, and fish. In: Brooks VB (ed) Handbook of physiology. The nervous system, Vol 2. Am Physiol Soc, Bethesda, MD, pp 1179–1236Google Scholar
  13. Hammond PH (1956) The influences of prior instructions to the subject on an apparently involuntary neuro-muscular response. J Physiol (Lond) 132: 17P-18PGoogle Scholar
  14. Hagbarth KE, Finer BL (1963) The plasticity of human withdrawal reflexes to noxious skin stimuli in lower limbs. In: Moruzzi G, Fessard A, Jasper HH (eds) Brain mechanisms. Progress Brain Research, Vol 19. Eisevier, Amsterdam, pp 65–81Google Scholar
  15. Hagbarth KE, Kugelberg E (1958) Plasticity of the human abdominal skin reflex. Brain 81: 305–318Google Scholar
  16. Houk JC, Rymers WZ (1981) Neural control of muscle length and tension. In: Brooks VB (ed) Handbook of physiology. The nervous system, Vol 2. Am Physiol Soc, Bethesda, MD, pp 257–323Google Scholar
  17. Hulliger M, Nordh E, Thelin AE, Vallbo ÅB (1979) The responses of afferent fibres from the glabrous skin of the hand during voluntary finger movements in man. J Physiol (Lond) 291: 233–249Google Scholar
  18. Iggo A (1974) Cutaneous receptors. In: Hubbard JI (ed) Peripheral nervous system. Plenum Press, New York, pp 347–404Google Scholar
  19. Ito M (1984) The cerebellum and neural control. Raven, New YorkGoogle Scholar
  20. Jenner JR, Stephens JA (1982) Cutaneous reflex responses and their central nervous pathways studied in man. J Physiol (Lond) 333: 405–419CrossRefGoogle Scholar
  21. Johansson RS (1978) Tactile sensibility in the human hand: receptive field characteristics of mechanoreceptive units in the glabrous skin area. J Physiol (Lond) 281: 101–123Google Scholar
  22. Johansson RS, Vallbo ÅB (1979) Tactile sensibility in the human hand: relative and absolute densities of four types of mechanoreceptive units in the glabrous skin. J Physiol (Lond) 286: 283–300Google Scholar
  23. Johansson RS, Vallbo ÅB (1983) Tactile sensory coding in the glabrous skin of the human hand. Trends Neurosci 6: 27–31Google Scholar
  24. Johansson RS, Westling G (1984a) Influences of cutaneous sensory input on the motor coordination during precision manipulation. In: von Euler C, Franzen O, Lindblom U, Ottoson D (eds) Somatosensory mechanisms. Macmillan Press, London, pp 249–260Google Scholar
  25. Johansson RS, Westling G (1984b) 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
  26. Johnson KO (1983) Neural mechanisms of tactual form and texture discrimination. Fed Proceed 42: 2542–2527Google Scholar
  27. Knibestöl M, Vallbo ÅB (1970) Single unit analysis of mechanoreceptor activity from the human glabrous skin. Acta physiol scand 80: 178–195Google Scholar
  28. Lund JP, Olsson KÅ (1983) The importance of reflexes and their control during jaw movement. Trends Neurosci 6: 458–463Google Scholar
  29. Loo CKC, McCloskey DI (1985) Effects of prior instruction and anaesthesia on long-latency responses to stretch in the long flexor of the human thumb. J Physiol (Lond) 365: 285–296Google Scholar
  30. Martin JH, Ghez C (1985) Task-related coding of stimulus and response in cat motor cortex. Exp Brain Res 57: 427–442Google Scholar
  31. Marsden CD, Merton PA, Morton HB (1976) Servo action in the human thumb. J Physiol (Lond) 257: 1–44Google Scholar
  32. Marsden CD, Merton PA, Morton HB (1977) The sensory mechanisms of servoaction in human muscle. J Physiol (Lond) 265: 521–535Google Scholar
  33. Marsden CD, Merton PA, Morton HB (1985) New observations on the human stretch reflex. J Physiol (Lond) 360: 51PGoogle Scholar
  34. Marsden CD, Rothwell JC, Day BL (1983) Long-latency automatic responses to muscle stretch in man: origin and function. In: Desmedt JE (ed) Motor control mechanisms in health and disease. Raven Press, New York, pp 509–539Google Scholar
  35. Matthews PBC (1984a) Evidence from the use of vibration that the human long-latency stretch reflex depends upon spindle secondary afferents. J Physiol (Lond) 348: 383–415PubMedGoogle Scholar
  36. Matthews PBC (1984b) The contrasting stretch reflex responses of the long and short flexor muscles in the human thumb. J Physiol (Lond) 348: 545–558Google Scholar
  37. Nashner LM (1976) Adapting reflexes controlling the human posture. Exp Brain Res 26: 59–72Google Scholar
  38. Phillips JR, Johnson KO (1981) Tactile spatial resolution. III. A continuum mechanics model of skin predicting mechanoreceptor responses to bars, edges, and gratings. J Neurophysiol 46: 1204–1225Google Scholar
  39. Rood ON (1860) On contraction of the muscles induced by contact with bodies in vibration. Am J Sci Arts 24: 449Google Scholar
  40. Tatton WG, Bruce IC (1981) Comment: a schema for the interactions between motor programs and sensory input. Can J Physiol 59: 691–699Google Scholar
  41. Torebjörk HE, Hagbarth KE, Eklund G (1978) Tonic finger flexion reflex induced by vibratory activation of digital mechanoreceptors. In: Gordon G (ed) Active touch. Pergamon, Oxford, pp 197–203Google Scholar
  42. Westling G, Johansson RS (1983) Pinch reflexes. Neurosci Lett Suppl 14: 402Google Scholar
  43. Westling G, Johansson RS (1984a) Factors influencing the force control during precision grip. Exp Brain Res 53: 277–284Google Scholar
  44. Westling G, Johansson RS (1984b) Tactile afferent signals and sensori-motor memory influencing the force coordination during precision grip between tips of fingers and thumb. Neurosci Lett Suppl 18: 259Google Scholar
  45. Westling G, Johansson RS (1987) Responses in glabrous skin mechanoreceptors during precision grip in humans. Exp Brain Res 66: 128–140PubMedGoogle Scholar
  46. Young RR (1973) The clinical significance of exteroceptive reflexes. In: Desmedt JE (ed) New developments in electromyography and clinical neurophysiology, Vol 3. Karger, Basel, pp 697–712Google Scholar

Copyright information

© Springer-Verlag 1987

Authors and Affiliations

  • R. S. Johansson
    • 1
  • G. Westling
    • 1
  1. 1.Department of PhysiologyUniversity of UmeåUmeåSweden

Personalised recommendations