Neuronal activity in somatosensory cortex of monkeys using a precision grip. III. Responses to altered friction perturbations.

The purpose of this investigation was to examine the activity changes in single units of the somatosensory cortex in response to lubricating and adhesive coatings applied to a hand-held object. Three monkeys were trained to grasp an object between the thumb and index fingers and to lift and hold it stationary within a narrow position window for 1 s before release. Grip forces normal to the skin surface, load forces tangential to the skin surface, and the displacement of the object were measured on each trial. Adhesive (rosin) and lubricant (petroleum jelly) coatings were applied to the smooth metal surface of the object to alter the friction against the skin. In addition, neuronal activity evoked by force pulse-perturbations generating shear forces and slip on the skin were compared with the patterns of activity elicited by grasping and lifting the coated surfaces. Following changes in surface coatings, both monkeys modulated the rate at which grip forces normal to the skin surface and load forces tangential to the skin surface were applied during the lifting phase of the task. As a result, the ratio of the rates of change of the two forces was proportionately scaled to the surface coating properties with the more slippery surfaces, having higher ratios. This precise control of normal and tangential forces enabled the monkeys to generate adequate grip forces and prevent slip of the object. From a total of 386 single neurons recorded in the hand area of the somatosensory cortex, 92 were tested with at least 1 coating. Cell discharge changed significantly with changes in surface coating in 62 (67%) of these cells. Of these coating-related cells, 51 were tested with both an adhesive and lubricating coating, and 45 showed significant differences in activity between the untreated metal surface and either the lubricant or the adhesive coating. These cells were divided into three main groups on the basis of their response patterns. In the first group (group A), the peak discharge increased significantly when the grasped surface was covered with lubricant. These cells appeared to be selectively sensitive to slip of the object on the skin. The second group (group B) was less activated by the adhesive surface compared with either the untreated metal or the lubricated surface, and they responded mainly to variations in the force normal to the skin surface. These cells provide useful feedback for the control of grip force. The third group (group C) responded to both slips and to changes in forces tangential to the skin. Most of these cells responded with a biphasic pattern reflecting the bidirectional changes in load force as the object was first accelerated and then decelerated. One hundred sixty-eight of the 386 isolated neurons were tested with brief perturbations during the task. Of these, 147 (88%) responded to the perturbation with a significant change in activity. In most of the cells, the response to the perturbation was shorter than 100 ms with a mean latency of 44.1 +/- 16.3 (SD) ms. For each of the cell groups, the activity patterns triggered by the perturbations were consistent with the activity patterns generated during the grasping and lifting of the coated object.

[1]  M. Srinivasan,et al.  Tactile detection of slip: surface microgeometry and peripheral neural codes. , 1990, Journal of neurophysiology.

[2]  D. Pandya,et al.  Cortico‐cortical connections of somatic sensory cortex (areas 3, 1 and 2) in the rhesus monkey , 1978, The Journal of comparative neurology.

[3]  T Brochier,et al.  Neuronal activity in somatosensory cortex of monkeys using a precision grip. I. Receptive fields and discharge patterns. , 1999, Journal of neurophysiology.

[4]  Masahiro Sakamoto,et al.  Deficits in manipulative behaviors induced by local injections of muscimol in the first somatosensory cortex of the conscious monkey , 1985, Brain Research.

[5]  A. M. Smith,et al.  Comparison of the neuronal activity in the SMA and the ventral cingulate cortex during prehension in the monkey. , 1997, Journal of neurophysiology.

[6]  P. Strick,et al.  Input to primate motor cortex from posterior parietal cortex (area 5). I. Demonstration by retrograde transport , 1978, Brain Research.

[7]  A. M. Smith,et al.  Primary motor cortical responses to perturbations of prehension in the monkey. , 1992, Journal of neurophysiology.

[8]  Peter L. Strick,et al.  Multiple representation in the primate motor cortex , 1978, Brain Research.

[9]  A. M. Smith,et al.  Responses of cerebellar Purkinje cells to slip of a hand-held object. , 1992, Journal of neurophysiology.

[10]  M. Hepp-Reymond,et al.  Contrasting properties of monkey somatosensory and motor cortex neurons activated during the control of force in precision grip. , 1991, Journal of neurophysiology.

[11]  J. Pruett,et al.  Responses in primary somatosensory cortex of rhesus monkey to controlled application of embossed grating and bar patterns. , 1996, Somatosensory & motor research.

[12]  R. Johansson,et al.  Independent control of human finger‐tip forces at individual digits during precision lifting. , 1992, The Journal of physiology.

[13]  F. P. Bowden,et al.  Friction: An Introduction to Tribology , 1973 .

[14]  A. M. Smith,et al.  Friction, not texture, dictates grip forces used during object manipulation. , 1996, Journal of neurophysiology.

[15]  A. M. Smith,et al.  Scopolamine increases prehensile force during object manipulation by reducing palmar sweating and decreasing skin friction , 1997, Experimental Brain Research.

[16]  R. Johansson,et al.  Influences of Cutaneous Sensory Input on the Motor Coordination During Precision Manipulation , 1984 .

[17]  E. G. Jones,et al.  Intracortical connectivity of architectonic fields in the somatic sensory, motor and parietal cortex of monkeys , 1978, The Journal of comparative neurology.

[18]  H Burton,et al.  Neuronal activity in the primary somatosensory cortex in monkeys (Macaca mulatta) during active touch of textured surface gratings: responses to groove width, applied force, and velocity of motion. , 1991, Journal of neurophysiology.

[19]  T Brochier,et al.  Neuronal activity in somatosensory cortex of monkeys using a precision grip. II. Responses To object texture and weights. , 1999, Journal of neurophysiology.

[20]  C E Chapman,et al.  Cortical mechanisms underlying tactile discrimination in the monkey. I. Role of primary somatosensory cortex in passive texture discrimination. , 1996, Journal of neurophysiology.

[21]  G. Ekman,et al.  ROUGHNESS, SMOOTHNESS, AND PREFERENCE: A STUDY OF QUANTITATIVE RELATIONS IN INDIVIDUAL SUBJECTS. , 1965, Journal of experimental psychology.

[22]  C. G. Phillips,et al.  A quantitative study of the distribution of neurons projecting to the precentral motor cortex in the monkey (M. fascicularis) , 1987, The Journal of comparative neurology.

[23]  A. M. Smith,et al.  Primary motor cortical activity related to the weight and texture of grasped objects in the monkey. , 1992, Journal of neurophysiology.

[24]  S S Hsiao,et al.  Spatial pattern representation and transformation in monkey somatosensory cortex. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[25]  M. M. Taylor,et al.  Tactile roughness of grooved surfaces: A model and the effect of friction , 1975 .