How tactile afferents in the human fingerpad encode tangential torques associated with manipulation: are we better than monkeys?

Abstract

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. In this study we investigated how torque information is encoded by human tactile afferents, including slowly adapting type-II (SA-II) afferents, in the fingerpads. SA-II afferent properties seemed perfectly suited for torque encoding but could not be previously investigated as they 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 participants. Torques were superimposed on a 2 N, 3 N, or 4 N background normal force. Unitary microneurography recordings were made from fast adapting type-I (FA-I, n=39), slowly adapting type-I (SA-I, n=31), and type-II (SA-II, n=13) afferents supplying the fingerpads. All three afferent types encoded torque magnitude and direction, with SA-II afferents showing excitatory and inhibitory modulation depending on torque direction. Most afferents of all three types had higher torque sensitivity with smaller normal force. FA-I afferents showed the best torque magnitude and worst directional discrimination abilities in both species. Human SA-I afferent response to static torque was inferior to dynamic stimuli, while in monkeys the opposite was true. In humans this might be compensated by the addition of a sustained SA-II afferent input. In comparison to monkeys the performance of each afferent type was inferior in humans, likely due to differences in fingertip tissue compliance and skin friction. [currently 246 words; 250 words max] Significance StatementWe investigate how individual human tactile nerve fibres encode rotational forces (torques) and compare them to their monkey counterparts. Human hands, but not monkey hands, are innervated by a tactile neuron type (SA-II afferents) specialised 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 the addition of SA-II afferent input. This indicates that variation in afferent types might compliment their specialisation for stimulus features, by slight differences between encoding in the two species.