Whisker-based pre-neuronal and peripheral encoding of surface stickiness

Texture is a multidimensional perceptual feature of touch, with coarseness, stickiness, and compliance as its major axes of variability. Of these, coarseness is the best understood in the rodent whisker system. However, variation in surface stickiness is also a common feature of natural scenes, and is likely to alter the mechanical interactions between whiskers and surfaces that drive neuronal responses and are the basis for perceptual experience. In this study, we asked whether and how stickiness information could be extracted from whisker–surface interactions and represented in the activity of whisker follicle innervating mechanosensory neurons. We developed a 3D whisker tracking system applicable to texture sensing, and used it to characterize the whisker–surface interactions occurring during whisking against surfaces of jointly varying stickiness, coarseness, and position, as well as the responses of whisker follicle innervating neurons in the trigeminal ganglion. The bending, twisting, and roll of the whisker shaft, the rates and amplitudes of stick-slip events at the whisker tip, and the firing rates of a subset of mechanosensory neurons could all be used to distinguish between surfaces of high and low stickiness. These results demonstrate that stickiness information is available to the whisker system.