Mechanoreceptive Aβ primary afferents discriminate naturalistic social touch inputs at a functionally relevant time scale

Abstract

AbstractInterpersonal touch is an important part of our social and emotional interactions. How these physical, skin-to-skin touch expressions are processed in the peripheral nervous system is not well understood. From single-unit microneurography recordings in humans, we evaluated the capacity of six subtypes of cutaneous afferents to differentiate perceptually distinct social touch expressions. By leveraging conventional statistical analyses and classification analyses using convolutional neural networks and support vector machines, we found that single units of multiple Aβ subtypes, especially slowly adapting type II (SA-II) and fast adapting hair follicle afferents (HFA), can reliably differentiate the skin contact of those expressions at accuracies similar to those perceptually. Rapidly adapting field (Field) afferents exhibit lower accuracies, whereas C-tactile (CT), fast adapting Pacinian corpuscles (FA-II), and muscle spindle (MS) afferents can barely differentiate the expressions, despite responding to the stimuli. We then identified the most informative firing patterns of SA-II and HFA afferents’ spike trains, which indicate that an average duration of 3-4 s of firing provides sufficient discriminative information. Those two subtypes also exhibit robust tolerance to shifts in spike-timing of up to 10 ms. A greater shift in spike-timing, however, drastically compromises an afferent’s discrimination capacity, and can change a firing pattern’s envelope to resemble that of another expression. Altogether, the findings indicate that SA-II and HFA afferents differentiate the skin contact of social touch at time scales relevant for such interactions, which is 1-2 orders of magnitude longer than those relevant for discriminating non-social touch inputs.