Decoupling kinematics and mechanics reveals coding properties of trigeminal ganglion neurons in the rat vibrissal system

Abstract

Tactile information available to the rat vibrissal system begins as external forces that cause whisker deformations, which in turn excite mechanoreceptors in the follicle. Despite the fundamental mechanical origin of tactile information, primary sensory neurons in the trigeminal ganglion (Vg) have often been described as encoding the kinematics (geometry) of object contact. Here we aimed to determine the extent to which Vg neurons encode the kinematics vs. mechanics of contact. We used models of whisker bending to quantify mechanical signals (forces and moments) at the whisker base while simultaneously monitoring whisker kinematics and recording single Vg units in both anesthetized rats and awake, body restrained rats. We employed a novel manual stimulation technique to deflect whiskers in a way that decouples kinematics from mechanics, and used Generalized Linear Models (GLMs) to show that Vg neurons more directly encode mechanical signals when the whisker is deflected in this decoupled stimulus space.DOI: http://dx.doi.org/10.7554/eLife.13969.001

Active Touch and Self-Motion Encoding by Merkel Cell-Associated Afferents

“…First, our results are based in significant part on recordings from identified Merkel afferents (17 of 53 recordings). Second, while our results support the notion that afferent spiking is closely associated with whisker bending moment (Bush et al, 2016; Campagner et al, 2016), we show that, in addition to bending moment ( M 0 ), its rate of change ( $M_0^{\prime }$) must also be considered in order to explain spiking during touch. Third, we offer a simple mechanical model that explains these sensitivities in terms of contact forces and tissue viscoelasticity.…”

“…Despite the popularity of the whisker system, only a very small number of studies have recorded from whisker afferents in behaving animals (Bush et al, 2016; Campagner et al, 2016; Khatri et al, 2009; Leiser and Moxon, 2007; Pais-Vieira et al, 2013; Yang et al., 2016). Only two of these studies measured the whisker bending necessary to estimate the forces and moments that drive spiking (Bush et al., 2016; Campagner et al, 2016). Our work supports these two studies, which both used statistical models to correlate the spiking of unidentified whisker afferents with mechanical variables estimated from high-speed video, and extends them in multiple ways.…”

WHISKiT Physics: A three-dimensional mechanical model of the rat vibrissal array

“…Mechanical responses of isolated whiskers have been quantified in various contexts (33,40,43,(47)(48)(49)(50)(51)(52)(53), but models of the vibrissal system have typically been quasi-static, two-dimensional (2D), and limited to a single whisker (32,34,38,42,44,(54)(55)(56)(57)(58)(59)(60). These are significant limitations when studying neural circuitry that has evolved with multiple sensors interacting with a three-dimensional complex world.…”

“…This choice allowed us to avoid any forced motion induced by the deflecting probe. Following the conventions of previous studies (43,44), the horizontal direction was defined to be parallel to the plane of the intrinsic curvature of the whisker and the vertical direction was perpendicular to that plane.…”

Dye-enhanced visualization of rat whiskers for behavioral studies

“…In particular, one can exploit the mechanical analogy between a whisker and a tapered beam (Quist and Hartmann, 2012; Williams and Kramer, 2010; Hires et al, 2013; Bush et al, 2016). A truncated conical beam model can predict rat whiskers’ natural resonant frequencies (Yan et al, 2013), the so-called normal modes.…”