Computationally Modeling the Impact of Measured Variance in Skin Mechanics on Neural Responses to Touch Stimuli

Abstract

We rely on our sense of touch to obtain information from the external environment with which we interact. Upon touching an object, the distal mechanical stimulus propagates through the skin's layers toward the end organs of cutaneous afferents that initiate neural responses. While the encoding of various stimuli has been thoroughly investigated in prior studies, the impact of the skin's mechanics remains vastly understudied. In particular, while we know that the skin undergoes natural cycles of remodeling, we do not know how remodeling impacts the skin's thickness and elasticity and what impacts those might have on the neural response and neural sensitivity between afferents. In the first aim, we performed uniaxial compression tests to measure the viscoelastic properties of 139 mouse skin specimens while also varying stretch level and rate. This is the first effort to do such a detailed characterization at different stages of the hair cycle. Over the population measured, we observed the skin's thickness and viscoelasticity to be highly variable, yet found systematic correlations between the viscoelastic parameters and skin thickness and applied stretch. Specifically, residual stress ratio positively correlates with skin thickness and stretch, and relaxation time constants negative correlates with strain rates. In the second aim, we used the population of measurements to build finite element models to closely examine the effect of thickness-dependent viscoelasticity on the propagation of internal deformation toward the end orangs of slowly adapting type I (SAI) afferents. In simulating the observed changes to the skin's mechanics, we find that there can be large variance in stresses and strains near the locations of end organs, which might lead to large variance in firing sensitivity. However, variance in internal deformation is significantly reduced when the stimulus tip is controlled by surface pressure and compressive stress is measured near the end organs. The combined results of the two aims indicate that the skin can reliably convey surface stimulus information to locations of tactile receptors even amidst changes in skin's structure. During such 2 changes, stimulus control by surface pressure may be more naturalistic and optimal and underlie how animals actively explore the tactile environment.