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Roles of glabrous skin receptors and sensorimotor memory in automatic control of precision grip when lifting rougher or more slippery objects

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Summary

To be successful, precision manipulation of small objects requires a refined coordination of forces excerted on the object by the tips of the fingers and thumb. The present paper deals quantitatively with the regulation of the coordination between the grip force and the vertical lifting force, denoted as the load force, while small objects were lifted, positioned in space and replaced by human subjects using the pinch grip. It was shown that the grip force changed in parallel with the load force generated by the subject to overcome various forces counteracting the intended manipulation. The balance between the two forces was adapted to the friction between the skin and the object providing a relatively small safety margin to prevent slips, i.e. the more slippery the object the higher the grip force at any given load force. Experiments with local anaesthesia indicated that this adaptation was dependent on cutaneous afferent input. Afferent information related to the frictional condition could influence the force coordination already about 0.1 s after the object was initially gripped, i.e. approximately at the time the grip and load forces began to increase in parallel. Further, “secondary”, adjustments of the force balance could occur later in response to small short-lasting slips, revealed as vibrations in the object. The new force balance following slips was maintained, indicating that the relationship between the two forces was set on the basis of a memory trace. Its updating was most likely accounted for by tactile afferent information entering intermittently at inappropriate force coordination, e.g. as during slips. The latencies between the onset of such slips and the appearance of the adjustments (0.06–0.08 s) clearly indicated that the underlying neural mechanisms operated highly automatically.

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References

  • Bowden FP, Tabor D (1973) Friction — an introduction to tribology. Anchor Press, Garden City, NY

    Google Scholar 

  • Brinkman J, Kuypers HGJM (1973) Cerebral control of contralateral and ipsilateral arm, hand and finger movements in the split-brain Rhesus monkey. Brain 96: 653–674

    CAS  PubMed  Google Scholar 

  • Brooks VB (1979) Motor programs revisited. In: Talbott RE, Humphrey DR (eds) Posture and movement. Raven, New York, pp 13–49

    Google Scholar 

  • Caccia MR, McComas AJ, Upton ARM, Blogg T (1973) Cutaneous reflexes in small muscles of the hand. J Neurol Neurosurg Psychiat 36: 960–977

    Google Scholar 

  • Comaish S, Bottoms E (1971) The skin and friction: Deviations from Amonton's law, and the effects of hydration and lubrication. Br J Dermatol 84: 37–43

    Google Scholar 

  • Crago PE, Houk JC, Hasan Z (1976) Regulatory actions of human stretch reflex. J Neurophysiol 39: 925–935

    CAS  PubMed  Google Scholar 

  • Evarts EV (1980) Brain mechanisms in voluntary movement. In: McFadden D (ed) Neural mechanisms in behavior. Springer, Berlin Heidelberg New York, pp 223–259

    Google Scholar 

  • Evarts EV, Vaughn WJ (1978) Intended arm movements in response to externally produced arm displacements in man. In: Desmedt JE (ed) Cerebral motor control in man: long loop mechanisms. Progress in clinical neurophysiology, vol 4. Karger, Basel, pp 178–192

    Google Scholar 

  • Gandevia SC, McCloskey DI (1977a) Effects of related sensory inputs on motor performance in man studied through changes in perceived heaviness. J Physiol (Lond) 272: 653–672

    Google Scholar 

  • Gandevia SC, McCloskey DI (1977b) Changes in motor commands, as shown by changes in perceived heaviness, during partial curarization and peripheral anaesthesia in man. J Physiol (Lond) 272: 673–689

    Google Scholar 

  • Garnett R, Stephens JA (1980) The reflex responses of single motor units in human first dorsal interosseus muscle following cutaneous afferent stimulation. J Physiol (Lond) 303: 351–364

    Google Scholar 

  • Garnett R, Stephens JA (1981) Changes in the recruitment threshold of motor units produced by cutaneous stimulation in man. J Physiol (Lond) 311: 463–473

    Google Scholar 

  • Gilbert PCF, Thach WT (1977) Purkinje cell activity during motor learning. Brain Res 128: 309–328

    Google Scholar 

  • Gonshor A, Melvill Jones G (1976a) Short-term adaptive changes in the human vestibulo-ocular reflex arc. J Physiol (Lond) 256: 361–379

    Google Scholar 

  • Gonshor A, Melvill Jones G (1976b) Extreme vestibulo-ocular adaption induced by prolonged optical reversal of vision. J Physiol (Lond) 256: 381–414

    Google Scholar 

  • Green DM, Swets JA (1966) Signal detection theory and psychophysics. John Wiley and Sons, Inc, New York

    Google Scholar 

  • Hepp-Reymond M-C, Wiesendanger M (1972) Unilateral pyramidotomy in monkeys: effect on force and speed of a conditioned precision grip. Brain Res 36: 117–131

    Google Scholar 

  • Houk JC (1978) Participation of reflex mechanisms and reaction time processes in the compensatory adjustments to mechanical disturbances. In: Desmedt JE (ed) Cerebral motor control in man: long loop mechanisms. Progress in clinical neurophysiology, vol 4. Karger, Basel, pp 193–215

    Google Scholar 

  • 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

    Google Scholar 

  • Ito M (1970) Neurophysiological aspects of the cerebellar motor control system. Int J Neurol 7: 162–176

    CAS  PubMed  Google Scholar 

  • Ito M (1976) Cerebellar learning control of vestibulo-ocular mechanisms. In: Desiraju T (ed) Mechanisms in transmission of signals for conscious behavior. Elsevier, Amsterdam

    Google Scholar 

  • Jenner JR, Stephens JA (1982) Cutaneous reflex responses and their central nervous pathways studied in man. J Physiol (Lond) 333: 405–419

    CAS  PubMed  Google Scholar 

  • Johansson RS, Vallbo ÅB (1983) Tactile sensory coding in the glabrous skin of the human hand. Trends Neurosci 6: 27–31

    Google Scholar 

  • Johansson RS, Westling G (1981) Coordination between grip force and vertical lifting force when lifting objects between index finger and thumb. Soc Neurosci Abstr 7: 247

    Google Scholar 

  • Johansson RS, Westling G (1984) Influences of cutaneous sensory input on the motor coordination during precision manipulation. In: Ottoson D, Franzen O (eds) Somatosensory mechanisms. In Press, MacMillan Press, London

    CAS  PubMed  Google Scholar 

  • Lawrence DG, Kuypers HGJM (1968) The functional organization of the motor system in the monkey. I. The effects of bilateral pyramidal lesions. Brain 91: 1–14

    Google Scholar 

  • Lemon RN (1981) Functional properties of monkey motor cortex neurones receiving afferent input from the hand and fingers. J Physiol (Lond) 311: 497–511

    Google Scholar 

  • Lemon RN, Porter R (1976) Afferent input to movement-related precentral neurones in conscious monkeys. Proc R Soc Lond B 194: 313–339

    Google Scholar 

  • Marsden CD, Merton PA, Morton HB (1977) The sensory mechanism of servoaction in human muscle. J Physiol (Lond) 265: 521–535

    Google Scholar 

  • Marsden CD, Rothwell JC, Traub MM (1979) The effects of thumb anaesthesia on weight perception, muscle activity and the stretch reflex in man. J Physiol (Lond) 294: 303–317

    Google Scholar 

  • Miles FA, Fuller JH (1974) Adaptive plasticity in the vestibuloocular responses of the rhesus monkey. Brain Res 80: 512–516

    Google Scholar 

  • Moberg E (1962) Criticism and study of methods for examining sensibility in the hand. Neurology 12: 8–19

    CAS  PubMed  Google Scholar 

  • Muir RB, Lemon RN (1983) Corticospinal neurones with a special role in precision grip. Brain Res 261: 312–316

    Google Scholar 

  • Nashner LM (1976) Adapting reflexes controlling the human posture. Exp Brain Res 26: 59–72

    Google Scholar 

  • Nashner LM (1981) Analysis of stance and posture in humans. In: Towe AL, Luschei ES (ed) Handbook of behavioral neurobiology, vol 5, motor coordination. Plenum, New York, pp 527–565

    Google Scholar 

  • Nashner LM, Grimm RJ (1978) Analysis of multiloop dyscontrols in standing cerebellar patients. In: Desmedt JE (ed) Cerebral motor control in man: long loop mechanisms. Progress in clinical neurophysiology, vol 4. Karger, Basel, pp 300–319

    Google Scholar 

  • Passingham R, Perry H, Wilkinsson F (1978) Failure to develop a precision grip in monkeys with unilateral neocortical lesions made in infancy. Brain Res 145: 410–415

    Google Scholar 

  • Phillips CG, Porter R (1977) Corticospinal neurones. Academic Press, London

    Google Scholar 

  • Poulton EC (1981) Human manual control. In: Brooks VB (ed) Handbook of physiology, sect 1, vol II, pp 1337–1339

  • Rack PMH (1981) Limitations of somatosensory feedback in control of posture and movement. In: Brooks VB (ed) Handbook of physiology: The nervous system, vol 2. Am Physiol Soc, Bethesda, MD

    Google Scholar 

  • Robinson DA (1976) Adaptive gain control of the vestibulo-ocular reflex by the cerebellum. J Neurophysiol 39: 954–969

    Article  CAS  Google Scholar 

  • Rosen I, Asanuma H (1972) Peripheral afferent input to the forelimb of the monkey motor cortex: Input-output relations. Exp Brain Res 14: 257–273

    Google Scholar 

  • Rothwell JC, Traub MM, Day BL, Obeso JA, Thomas PK, Marsden CD (1982) Manual motor performance in a deafferented man. Brain 105: 515–542

    Google Scholar 

  • Smith AM, Bourbonnais D (1981) Neuronal activity in cerebellar cortex related to control of prehensile force. J Neurophysiol 45: 286–303

    Google Scholar 

  • Smith AM, Bourbonnais D, Blanchette G (1981) Interaction between forced grasping and a learned precision grip after ablation of the supplementary motor area. Brain Res 222: 395–400

    Google Scholar 

  • Strick PL, Preston JB (1982) Two representations of the hand in area 4 of a primate. II. Somatosensory input organization. J Neurophysiol 48: 150–159

    Google Scholar 

  • Torebjörk HE, Hagbarth K-E, Eklund G (1978) Tonic finger flexion reflex induced by vibratory activation of digital mechanoreceptors. In: Gordon G (ed) Active touch. Pergamon, Oxford, pp 197–203

    Google Scholar 

  • Vierck CJ (1978) Interpretations of the sensory and motor consequences of dorsal column lesions. In: Gordon G (ed) Active touch. Pergamon, Oxford, pp 139–159

    Google Scholar 

  • Westling G, Johansson RS (1980) Factors setting the grip force when lifting an object with index and thumb. Neurosci Lett (Suppl) 5: p 113

    Google Scholar 

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

    Google Scholar 

  • Wong YC, Kwan H, MacKay WA, Murphy JT (1978) Spatial organization of precentral cortex in awake primates. I. Somatosensory inputs. J Neurophysiol 41: 1107–1120

    Google Scholar 

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Johansson, R.S., Westling, G. 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 (1984). https://doi.org/10.1007/BF00237997

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  • DOI: https://doi.org/10.1007/BF00237997

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