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

Interpersonal touch is an important channel of social emotional interaction. How these physical skin-to-skin touch expressions are processed in the peripheral nervous system is not well understood. From microneurography recordings in humans, we evaluated the capacity of six subtypes of cutaneous mechanoreceptive afferents to differentiate human-delivered social touch expressions. Leveraging statistical and classification analyses, we found that single units of multiple mechanoreceptive Aβ subtypes, especially slowly adapting type II (SA-II) and fast adapting hair follicle afferents (HFA), can reliably differentiate social touch expressions at accuracies similar to human recognition. We then identified the most informative firing patterns of SA-II and HFA afferents, which indicate that average durations of 3-4 s of firing provide sufficient discriminative information. Those two subtypes also exhibit robust tolerance to spike-timing shifts of up to 10-20 ms, varying with touch expressions due to their specific firing properties. Greater shifts in spike-timing, however, can change a firing pattern's envelope to resemble that of another expression and drastically compromise an afferent's discrimination capacity. 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 are 1-2 orders of magnitude longer than those for non-social touch.