Somatosensory control of precision grip during unpredictable pulling loads

SummaryDuring manipulation involving restraint of ‘active’ (mechanically unpredictable) objects, it is presumed that the control of the grip and other reaction forces more regularly relies on somatosensory input than during manipulation of ‘passive’ (mechanically predictable) objects. In companion studies we have shown that grip forces are automatically adjusted to the amplitude and the rate of distal pulling loads imposed through an ‘active’ object held in a precision grip. In this study anesthesia of either one or both digits holding the manipulandum was used to examine whether the grip force regulation was dependent on afferent signals from the digits. Five types of trapezoidal load force profiles of various rate and amplitude combinations were given in an unpredictable sequence while the subject was prevented from seeing the hand. Grip forces, load forces and position of the manipulandum in the pulling direction were recorded. With both digits anesthetized the load amplitude changes yielded considerably less grip force modulation and in many trials obvious grip force responses were absent. Moreover, the latencies between the onset of the load changes and the observed grip force responses were much prolonged. However, there was pronounced inter-individual variation. Subjects exhibiting a lower stiffness in the pulling direction, probably due to more flexed fingers when holding the manipulandum, showed a higher force modulation, higher responsiveness to the load ramps and shorter latencies. Hence, under certain conditions afferent input from receptors proximal to the digits could be utilized to provide some grip regulation. The evoked grip force responses showed an initial response similar to the normally occurring ‘catch-up’ response, but it was not graded by the load force rate. Also, there was no ‘tracking’ response, suggesting that the latter was contingent upon a momentto-moment control using afferent input from the digits. With only one digit anesthetized (thumb) the handicap was less severe. Thus, the grip force regulation was impaired under any condition of digital anesthesia, i.e., afferent input from both index finger and thumb was required for the adequate operation of the grip force regulation.

[1]  R. Johansson,et al.  Tactile sensibility in the human hand: relative and absolute densities of four types of mechanoreceptive units in glabrous skin. , 1979, The Journal of physiology.

[2]  R. Johansson,et al.  Somatosensory control of precision grip during unpredictable pulling loads , 2004, Experimental Brain Research.

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

[4]  R. Johansson,et al.  Somatosensory control of precision grip during unpredictable pulling loads , 1992, Experimental Brain Research.

[5]  C. Wilson,et al.  Anatomical and physiological properties of the cortical and thalamic innervations of neostriatal tissue grafts. , 1990, Progress in brain research.

[6]  M. Jeannerod Intersegmental coordination during reaching at natural visual objects , 1981 .

[7]  J. Jenner,et al.  Cutaneous reflex responses and their central nervous pathways studied in man , 1982, The Journal of physiology.

[8]  D. Burke,et al.  Responses to passive movement of receptors in joint, skin and muscle of the human hand. , 1988, The Journal of physiology.

[9]  D. McCloskey,et al.  Effects of prior instruction and anaesthesia on long‐latency responses to stretch in the long flexor of the human thumb. , 1985, The Journal of physiology.

[10]  M. Jeannerod The formation of finger grip during prehension. A cortically mediated visuomotor pattern , 1986, Behavioural Brain Research.

[11]  J. Stephens,et al.  Changes in the recruitment threshold of motor units produced by cutaneous stimulation in man. , 1981, The Journal of physiology.

[12]  J. Abbs,et al.  Finger movement responses of cutaneous mechanoreceptors in the dorsal skin of the human hand. , 1991, Journal of neurophysiology.

[13]  O. Lippold,et al.  Long-latency spinal reflexes in humans. , 1985, Journal of neurophysiology.

[14]  L. Nashner Analysis of Stance Posture in Humans , 1981 .

[15]  R. Johansson,et al.  Factors influencing the force control during precision grip , 2004, Experimental Brain Research.

[16]  J. Stephens,et al.  Task‐dependent changes in cutaneous reflexes recorded from various muscles controlling finger movement in man. , 1989, The Journal of physiology.

[17]  M. McClean,et al.  The reflex responses of single motor units in human lower lip muscles to mechanical stimulation , 1982, Brain Research.

[18]  M. Flanders,et al.  Interaction between visually and kinesthetically triggered voluntary responses. , 1986, Journal of motor behavior.

[19]  Bernice W. Polemis Nonparametric Statistics for the Behavioral Sciences , 1959 .

[20]  R. Johansson,et al.  Responses in glabrous skin mechanoreceptors during precision grip in humans , 2004, Experimental Brain Research.

[21]  B. B. Edin,et al.  Finger joint movement sensitivity of non-cutaneous mechanoreceptor afferents in the human radial nerve , 2004, Experimental Brain Research.

[22]  J E Desmedt,et al.  Cutaneous facilitation of large motor units and motor control of human fingers in precision grip. , 1983, Advances in neurology.

[23]  Y. Lamarre,et al.  Fast ballistic arm movements triggered by visual, auditory, and somesthetic stimuli in the monkey. I. Activity of precentral cortical neurons. , 1983, Journal of neurophysiology.

[24]  R S Nickerson,et al.  Intersensory facilitation of reaction time: energy summation or preparation enhancement? , 1973, Psychological review.

[25]  J. Stephens,et al.  The reflex responses of single motor units in human first dorsal interosseous muscle following cutaneous afferent stimulation. , 1980, The Journal of physiology.

[26]  R. S. Johansson,et al.  Roles of glabrous skin receptors and sensorimotor memory in automatic control of precision grip when lifting rougher or more slippery objects , 2004, Experimental Brain Research.

[27]  K. J. Cole,et al.  Grip force adjustments evoked by load force perturbations of a grasped object. , 1988, Journal of neurophysiology.

[28]  R. Johansson,et al.  Coordinated isometric muscle commands adequately and erroneously programmed for the weight during lifting task with precision grip , 2004, Experimental Brain Research.

[29]  D. McCloskey,et al.  Effects of related sensory inputs on motor performances in man studied through changes in perceived heaviness , 1977, The Journal of physiology.

[30]  P. Matthews Long‐latency stretch reflexes of two intrinsic muscles of the human hand analysed by cooling the arm. , 1989, The Journal of physiology.

[31]  C. Marsden,et al.  The sensory mechanism of servo action in human muscle. , 1977, The Journal of physiology.

[32]  R. Johansson,et al.  Signals in tactile afferents from the fingers eliciting adaptive motor responses during precision grip , 2004, Experimental Brain Research.