Club-like Receptors Respond to Light Touch but not to Whisking

Rodents acquire environmental information through their whiskers by employing active whisking and touch. Each whisker extends from a highly complex follicle containing hundreds of mechanoreceptors (MRs) of various types, positioned in different locations and surrounded by diverse tissue structures. Previous studies have shown that individual primary sensory afferents from these follicles respond selectively either to whisking (W) or touch (T), or non-selectively to both (WT). Given that MRs are sensitive to tiny, sub-micron deformations, the mechanisms enabling such selectivity were enigmatic. In this study, using artificial whisking, intra-axonal recordings and single-cell morphological analysis, we identify one class of MRs, the club-like endings, as T cells - all responding selectively to active touch and not to active whisking. The other MR types examined here, Merkel and lanceolate endings, exhibited various selectivity patterns. Club-like endings are arranged as a one-layer circular array around the whisker shaft near its center of mass, within the neck of a specialized structure called ringwulst (Rw). Using scanning electron microscopy (SEM), we found that individual club-like endings were directly attached to the glassy membrane covering the epithelial sheath attached to the whisker shaft, while being anchored to a specialized network of collagen fibers. This morphology minimizes deformations during whisking in air while allowing high sensitivity to whisker deformations induced by touch. We hypothesize that these specific morphological adaptations evolved to enable the detection of light touch, which is crucial for precise object localization during active whisking and show that cats, which do not use active whisking, lack several of these adaptations.