How Tactile Afferents in the Human Fingerpad Encode Tangential Torques Associated with Manipulation: Are Monkeys Better than Us?

Dexterous object manipulation depends critically on information about forces normal and tangential to the fingerpads, and also on torque associated with object orientation at grip surfaces. We investigated how torque information is encoded by human tactile afferents in the fingerpads and compared them to 97 afferents recorded in monkeys (n = 3; 2 females) in our previous study. Human data included slowly-adapting Type-II (SA-II) afferents, which are absent in the glabrous skin of monkeys. Torques of different magnitudes (3.5-7.5 mNm) were applied in clockwise and anticlockwise directions to a standard central site on the fingerpads of 34 human subjects (19 females). Torques were superimposed on a 2, 3, or 4 N background normal force. Unitary recordings were made from fast-adapting Type-I (FA-I, n = 39), and slowly-adapting Type-I (SA-I, n = 31) and Type-II (SA-II, n = 13) afferents supplying the fingerpads via microelectrodes inserted into the median nerve. All three afferent types encoded torque magnitude and direction, with torque sensitivity being higher with smaller normal forces. SA-I afferent responses to static torque were inferior to dynamic stimuli in humans, while in monkeys the opposite was true. In humans this might be compensated by the addition of sustained SA-II afferent input, and their capacity to increase or decrease firing rates with direction of rotation. We conclude that the discrimination capacity of individual afferents of each type was inferior in humans than monkeys which could be because of differences in fingertip tissue compliance and skin friction.SIGNIFICANCE STATEMENT We investigated how individual human tactile nerve fibers encode rotational forces (torques) and compared them to their monkey counterparts. Human hands, but not monkey hands, are innervated by a tactile neuron type (SA-II afferents) specialized to encode directional skin strain yet, so far, torque encoding has only been studied in monkeys. We find that human SA-I afferents were generally less sensitive and less able to discriminate torque magnitude and direction than their monkey counterparts, especially during the static phase of torque loading. However, this shortfall in humans could be compensated by SA-II afferent input. This indicates that variation in afferent types might complement each other signaling different stimulus features possibly providing computational advantage to discriminate stimuli.

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.

Sensory signals in neural populations underlying tactile perception and manipulation.

For humans to manipulate an object successfully, the motor control system must have accurate information about parameters such as the shape of the stimulus, its position of contact on the skin, and the magnitude and direction of contact force. The same information is required for perception during haptic exploration of an object. Much of these data are relayed by the mechanoreceptive afferents innervating the glabrous skin of the digits. Single afferent responses are modulated by all the relevant stimulus parameters. Thus, only in complete population reconstructions is it clear how each of the parameters can be signaled to the brain independently when many are changing simultaneously, as occurs in most normal movements or haptic exploration. Modeling population responses reveals how resolution is affected by neural noise and intrinsic properties of the population such as the pattern and density of innervation and the covariance of response variability.

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.