Heather E. Wheat

Human ability to scale and discriminate forces typical of those occurring during grasp and manipulation

When humans manipulate objects, the sensorimotor system coordinates three-dimensional forces to optimize and maintain grasp stability. To do this, the CNS requires precise information about the magnitude and direction of load force (tangential to skin surface) plus feedback about grip force (normal to skin). Previous studies have shown that there is rapid, precise coordination between grip and load forces that deteriorates with digital nerve block. Obviously, mechanoreceptive afferents innervating fingerpad skin contribute essential information. We quantify human capacity to scale tangential and normal forces using only cutaneous information. Our paradigm simulated natural manipulations (a force tangential to the skin superimposed on an indenting force normal to the skin). Precisely controlled forces were applied by a custom-built stimulator to an immobilized fingerpad. Using magnitude estimation, subjects (n = 8) scaled the magnitude of tangential force (0.25–2.8 N) in two experiments (normal force, 2.5 and 4 N, respectively). Performance was unaffected by normal force magnitude and tangential force direction. Moreover, when both normal (2–4 N) and tangential forces were varied in a randomized-block factorial design, the relationship between applied and perceived tangential force remained near linear, with a minor but statistically significant nonlinearity. Our subjects could also discriminate small differences in tangential force, and this was the case for two different reference stimuli. In both cases, the Weber fraction was 0.16. Finally, scaling functions for magnitude estimates of normal force (1–5 N) were also approximately linear. These data show that the cutaneous afferents provide a wealth of precise information about both normal and tangential force.

Encoding of tangential torque in responses of tactile afferent fibres innervating the fingerpad of the monkey

Torsional loads are ubiquitous during everyday dextrous manipulations. We examined how information about torque is provided to the sensorimotor control system by populations of tactile afferents. Torsional loads of different magnitudes were applied in clockwise and anticlockwise directions to a standard central site on the fingertip. Three different background levels of contact (grip) force were used. The median nerve was exposed in anaesthetized monkeys and single unit responses recorded from 66 slowly adapting type‐I (SA‐I) and 31 fast adapting type‐I (FA‐I) afferents innervating the distal segments of the fingertips. Most afferents were excited by torque but some were suppressed. Responses of the majority of both afferent types were scaled by torque magnitude applied in one or other direction, with the majority of FA‐I afferent responses and about half of SA‐I afferent responses scaled in both directions. Torque direction affected responses in both afferent types, but more so for the SA‐I afferents. Latencies of the first spike in FA‐I afferent responses depended on the parameters of the torque. We used a Parzen window classifier to assess the capacity of the SA‐I and FA‐I afferent populations to discriminate, concurrently and in real‐time, the three stimulus parameters, namely background normal force, torque magnitude and direction. Despite the potentially confounding interactions between stimulus parameters, both the SA‐I and the FA‐I populations could extract torque magnitude accurately. The FA‐I afferents signalled torque magnitude earlier than did the SA‐I afferents, but torque direction was extracted more rapidly and more accurately by the SA‐I afferent population.

Cutaneous Afferents From the Monkeys Fingers: Responses to Tangential and Normal Forces

Control of tangential force plays a key role in everyday manipulations. In anesthetized monkeys, forces tangential to the skin were applied at a range of magnitudes comparable to those used in routine manipulations and in eight different directions. The paradigm used enabled separation of responses to tangential force from responses to the background normal force. For slowly adapting type I (SAI) afferents, tangential force responses ranged from excitatory through no response to suppression, with both a static and dynamic component. For fast adapting type I (FAI) afferents, responses were dynamic and excitatory only. Responses of both afferent types were scaled by tangential force magnitude, elucidating the neural basis for previous human psychophysical scaling data. Most afferents were direction selective with a range of preferred directions and a range in sharpness of tuning. Both the preferred direction and the degree of tuning were independent of the background normal force. Preferred directions were distributed uniformly over 360 degrees for SAI afferents, but for FAI afferents they were biased toward the proximo-ulnar direction. Afferents from all over the glabrous skin of the distal segment of the finger responded; there was no evident relationship between the position of an afferents receptive field on the finger and its preferred direction or its degree of tuning. Nor were preferred directions biased either toward or away from the receptive field center. In response to the relatively large normal forces, some afferents saturated and others did not, regardless of the positions of their receptive fields. Total afferent response matched human psychophysical scaling functions for normal force.

Physiological mechanisms of the receptor system

When we manipulate objects in our environment, a vast array of receptors in the skin, joints and muscles is activated. This information is relayed to the central nervous system and underlies two distinct but complementary aspects of hand function. Most obviously, these neural signals lead to haptic perception. We may sense how rough or smooth a surface is, or how curved an object is, whether it is soft or hard, whether the surface is slippery or sticky, how heavy it is and so on. Less obvious, but equally important, is the use the motor control system makes of these sensory signals in order to ensure appropriate hand movements resulting in stable grasps and effective complex manipulations. Some examples of common manipulations in our daily lives are: lifting a cup of coffee, opening a door, getting dressed, typing a manuscript, threading a needle.

Representation of the shape and contact force of handled objects in populations of cutaneous afferents

Everyday, humans grasp and manipulate objects with precision. In order to achieve this, the neural mechanisms controlling movements of the fingers must have continuous information about the relationships of the fingers to the object being handled. In particular, successful manipulations depend on a knowledge of the local shape of the object, its position on the fingers and the contact forces. Some of this information is relayed by receptors in the joints and in the muscles (Burgess et al., 1982), and joint angle is also signalled by cutaneous receptors around the joints and in the hairy skin of the hand (Edin and Abbs, 1991). The fingerpads are densely innervated with low threshold mechanoreceptors which signal a variety of precise information about grasp (Johansson and Vallbo, 1979). They are the only source of information about the region of contact with the fingers, an important consideration from the point of view of the dynamics of grasp (Fearing and Hollerbach, 1985). Receptors in the extrinsic and intrinsic hand muscles signal forces used by the fingers but information about contact forces between the fingers and the object is also signalled by the cutaneous receptors in the fingerpads (Cohen and Vierck, 1993)