G. Westling

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

SummaryTo 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.

Factors influencing the force control during precision grip

SummaryA small object was gripped between the tips of the index finger and thumb and held stationary in space. Its weight and surface structure could be changed between consecutive lifting trials, without changing its visual appearance. The grip force and the vertical lifting force acting on the object, as well as the vertical position of the object were continuously recorded. Likewise, the minimal grip force necessary to prevent slipping, was measured. The difference between this minimal force and the employed grip force, was defined as the safety margin to prevent slipping.It was found that the applied grip force was critically balanced to optimize the motor behaviour so that slipping between the skin and the gripped object did not occur and the grip force did not reach exeedingly high values. To achieve this motor control, the nervous system relied on a mechanism that measured the frictional condition between the surface structure of the object and the fingers. Experiments with local anaesthesia indicated that this mechanism used information from receptors in the fingers, most likely skin mechanoreceptors. In addition to friction, the control of the grip force was heavily influenced by the weight of the object and by a safety margin factor related to the individual subject. The frictional conditions during the previous trial could also, to some extent, influence the grip force.

Coordinated isometric muscle commands adequately and erroneously programmed for the weight during lifting task with precision grip

SummarySmall objects were lifted from a table, held in the air, and replaced using the precision grip between the index finger and thumb. The adaptation of motor commands to variations in the objects weight and sensori-motor mechanisms responsible for optimum performance of the transition between the various phases of the task were examined. The lifting movement involved mainly a flexion of the elbow joint. The grip force, the load force (vertical lifting force) and the vertical position were measured. Electromyographic activity (e.m.g.) was recorded from four antagonist pairs of hand/arm muscles primarily influencing the grip force or the load force. In the lifting series with constant weight, the force development was adequately programmed for the current weight during the loading phase (i.e. the phase of parallel increase in the load and grip forces during isometric conditions before the lift-off). The grip and load force rate trajectories were mainly single-peaked, bell-shaped and roughly proportional to the final force. In the lifting series with unexpected weight changes between lifts, it was established that these force rate profiles were programmed on the basis of the previous weight. Consequently, with lifts programmed for a lighter weight the object did not move at the end of the continuous force increase. Then the forces increased in a discontinous fashion until the force of gravity was overcome. With lifts programmed for a heavier weight, the high load and grip force rates at the moment the load force overcame the force of gravity caused a pronounced positional overshoot and a high grip force peak, respectively. In these conditions the erroneous programmed commands were automatically terminated by somatosensory signals elicited by the start of the movement. A similar triggering by somatosensory information applied to the release of programmed motor commands accounting for the unloading phase (i.e. the parallel decrease in the grip and load forces after the object contacted the table following its replacement). These commands were always adequately programmed for the weight.

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

SummaryWhile 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.

Eye–Hand Coordination in Object Manipulation

We analyzed the coordination between gaze behavior, fingertip movements, and movements of the manipulated object when subjects reached for and grasped a bar and moved it to press a target-switch. Subjects almost exclusively fixated certain landmarks critical for the control of the task. Landmarks at which contact events took place were obligatory gaze targets. These included the grasp site on the bar, the target, and the support surface where the bar was returned after target contact. Any obstacle in the direct movement path and the tip of the bar were optional landmarks. Subjects never fixated the hand or the moving bar. Gaze and hand/bar movements were linked concerning landmarks, with gaze leading. The instant that gaze exited a given landmark coincided with a kinematic event at that landmark in a manner suggesting that subjects monitored critical kinematic events for phasic verification of task progress and subgoal completion. For both the obstacle and target, subjects directed saccades and fixations to sites that were offset from the physical extension of the objects. Fixations related to an obstacle appeared to specify a location around which the extending tip of the bar should travel. We conclude that gaze supports hand movement planning by marking key positions to which the fingertips or grasped object are subsequently directed. The salience of gaze targets arises from the functional sensorimotor requirements of the task. We further suggest that gaze control contributes to the development and maintenance of sensorimotor correlation matrices that support predictive motor control in manipulation.

Responses in glabrous skin mechanoreceptors during precision grip in humans.

SummaryImpulses in single tactile units innervating the human glabrous skin were recorded percutaneously from the median nerve using tungsten electrodes. The units were classified as belonging to one of the four categories: fast adapting with small receptive fields (FA I), fast adapting with large receptive fields (FA II), slowly adapting with small fields (SA I), and slowly adapting with large fields (SA II). A small test object was lifted, positioned in space and replaced using the precision grip between fingers and thumb. The grip force, the load force (vertical lifting force), the vertical movements of the object and vibrations (accelerations) in the object were recorded. After being virtually silent between lifts, the FA I units whose fields contacted the object became highly active during the initial period of grip force increase (initial response). This was also true for most SA I units. Accordingly, most of the skin deformation changes took place at low grip forces (below ca. 1 N). Later, while the load and grip forces increased in parallel during isometric conditions, the FA I and SA I units continued firing but generally at declining impulse rates. As long as the object was held in the air, the SA I units generally maintained firing with a tendency to adaptation. A minority of the FA I unit also discharged, especially during periods of pronounced physiological muscle tremor. The SA I units usually became silent when the grip and load forces in parallel declined to zero during isometric conditions after the object had contacted the table. However, during the very release of the grip the FA I units and some SA I units showed brief burst discharges (release response). The FA II units responded distinctly to the mechanical transients associated with the start of the vertical movement and especially with the sudden cessation of movement at the terminal table contact. FA II units whose end organs were remotely located in relation to the skin areas in contact with the object also responded. Most FA II units also discharged at the initial touch and at the release of the object, albeit less reliably than the type I units. In addition to weak dynamic responses during the phase of isometric force increase, the SA II units showed comparatively strong tonic responses while the object was held during static conditions. High firing rates also were maintained during long-lasting lifts. Moreover, it was established that the signals in SA II afferents were related to the three dimensional force profile in the grip. The results are discussed with regard to the possible implications for the control of precise manipulative movements.

Visual size cues in the programming of manipulative forces during precision grip

SummaryA size-weight illusion was used to examine the role of visual cues in the programming of manipulative forces during the lifting of test objects utilizing the preci sion grip. Three different boxes of equal weight and unequal size were lifted. These were equipped with an instrumented grip handle to measure the employed grip force, load force (vertical lifting force), force rates and vertical movement. All fifteen subjects participating in the study reported that the smallest box was the heaviest which is consistent with size-weight illusion predictions. However, the rate of increase of the isometric grip and load forces initially during the lift, the peaks of the grip and load force and the vertical acceleration were all found to increase with the box size. Thus, despite the conscious perception indicating a heavier weight for the small object, the motor program was scaled for a lighter weight. Yet, no differences were found in grip force during the static phase of the lift, where weight related information was apparently available via sensory feed back. Previous studies have reported that the program ming of the precision grip is based on somatosensory information gained during previous lifts (Johansson and Westling 1984, 1988a, b). The present study suggests that visual cues are integrated in the programming of manipu lative forces during precision grip.

Programmed and triggered actions to rapid load changes during precision grip

SummaryA test object (grip apparatus) was held at its upper part using a precision grip. Small balls were dropped into a target cup at the bottom of the apparatus. The grip force, the load force (vertical lifting force) and the vertical movement were measured. Electromyographic activity (e.m.g.) was recorded from four antagonist pairs of hand/arm muscles primarily influencing the grip force or the load force. The balls were dropped either by the subject during a bimanual task, or unexpectedly by the experimenter. When the subject dropped the ball, preparatory actions occurred before the rapid increase in the vertical load caused by the impact. These actions appeared ca. 150 ms prior to the impact and involved a grip force increase and a lifting movement of the grip apparatus. The e.m.g. activity increased in all eight of the hand and arm muscles, indicating a general stiffening of the hand/arm system prior to the impact. Furthermore, the preparatory actions were programmed adequately for the size of the load force step at the impact, i.e. an adequate safety margin to prevent slips was preserved during the critical period of the impact. Thus, variations in this step caused by changes in (i) the weight of ball, (ii) the weight of the grip apparatus and (iii) the length of the drop were adequately taken into account during the programming of these actions. In addition, the frictional condition between the skin and the grip surface was also taken into account. The relevant sensory information apparently was obtained during the handling of the ball and the grip apparatus prior to the drop. There were also task-related automatic muscle responses triggered by the impact. These responses, which also served to stiffen the hand/arm system, were most pronounced during unexpected load changes, but they appeared too late to prevent slips. However, if no overall slip occurred, the triggered responses were functional in the sense that they helped to quickly restore the safety margin and the vertical position of the object.

Independent control of human finger-tip forces at individual digits during precision lifting.

1. Subjects lifted an object with two parallel vertical grip surfaces and a low centre of gravity using the precision grip between the tips of the thumb and index finger. The friction between the object and the digits was varied independently at each digit by changing the contact surfaces between lifts. 2. With equal frictional conditions at the two grip surfaces, the finger‐tip forces were about equal at the two digits, i.e. similar vertical lifting forces and grip forces were used. With different frictions, the digit touching the most slippery surface exerted less vertical lifting force than the digit in contact with the rougher surface. Thus, the safety margins against slips were similar at the two digits whether they made contact with surfaces of similar or different friction. 3. During digital nerve block, large and variable safety margins were employed, i.e. the finger‐tip forces did not reflect the surface conditions. Slips occurred more frequently than under normal conditions (14% of all trials with nerve block, <5% during normal conditions), and they only occasionally elicited compensatory adjustments of the finger‐tip forces and then at prolonged latencies. 4. The partitioning of the vertical lifting force between the digits was thus dependent on digital afferent inputs and resulted from active automatic regulation and not just from the mechanics of the task. 5. The safety margin employed at a particular digit was mainly determined by the frictional conditions encountered by the digit, and to a lesser degree by the surface condition at the same digit in the previous lift (anticipatory control), but was barely influenced by the surface condition at the other digit. 6. It was concluded that the finger‐tip forces were independently controlled for each digit according to a ‘non‐slip strategy’. The findings suggest that the force distribution among the digits represents a digit‐specific lower‐level neural control establishing a stable grasp. This control relies on digit‐specific afferent inputs and somatosensory memory information. It is apparently subordinated to a higher‐level control that is related to the total vertical lifting and normal forces required by the lifting task and the relevant physical properties of the manipulated object.

Thresholds of mechanosensitive afferents in the human hand as measured with von Frey hairs

Abstract Afferent activity in low threshold mechanoreceptive units innervating the glabrous skin area of the hand was recorded from the median nerve of human subjects, using tungsten needle electrodes. The units were classified as RA, PC, SA I and SA II units mainly on the basis of their adaptation and receptive field properties Thresholds of the units were determined by two methods, the force threshold was determined with von Frey hairs and the indentation threshold with triangular indentations of controlled amplitudes. The characteristics of the force developed by the von Frey hairs as a function of movement parameters was analyzed when the hairs were prodded against a force transducer. The rise time was 10–20 msec and the variability of the peak force was within-20% of the steady-state force during repetitive prodding with various repetition rates. The von Frey thresholds were determined for 284 units and the indentation threshold for 116 of them. The RA and PC units were the most sensitive unit types with median thresholds of 0.58 mN and 0.54 mN. The medians of the slowly adapting SA I and SA II units, were 1.3 mN and 7.5 mN. The threshold distributions for all unit types were positively skewed. No regional differences were found but the thresholds were identical in skin areas where the psychophysical thresholds have been shown to be diverse. The relation between force threshold and indentation threshold was analyzed for 116 units. There was a positive correlation between the two thresholds, although the relation appeared not to be identical for the four types of units and the scatter was considerable.