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

Many rodents tactually sense the world through active motions of their vibrissae (whiskers), which are regularly arranged in rows and columns (arcs) on the face. The present study quantifies several geometric parameters of rat whiskers that determine the tactile information acquired. Findings include the following. ) A meta-analysis of seven studies shows that whisker base diameter varies with arc length with a surprisingly strong dependence on the whisker's row position within the array.) The length of the whisker medulla varies linearly with whisker length, and the medulla's base diameter varies linearly with whisker base diameter. ) Two parameters are required to characterize whisker "taper": radius ratio (base radius divided by tip radius) and radius slope (the difference between base and tip radius, divided by arc length). A meta-analysis of five studies shows that radius ratio exhibits large variability due to variations in tip radius, while radius slope varies systematically across the array.) Within the resolution of the present study, radius slope does not differ between the proximal and distal segments of the whisker, where "proximal" is defined by the presence of the medulla. ) Radius slope of the medulla is offset by a constant value from radius slope of the proximal portion of the whisker. We conclude with equations for all geometric parameters as functions of row and column position. Rats tactually explore their world by brushing and tapping their whiskers against objects. Each whisker's geometry will have a large influence on its mechanics and thus on the tactile signals the rat obtains. We performed a meta-analysis of seven studies to generate equations that describe systematic variations in whisker geometry across the rat's face. We also quantified the geometry of the whisker medulla. A database provides access to geometric parameters of over 500 rat whiskers.

Highlights d Intra-axon recordings from four different mechanoreceptor types in whisker follicle d Types have different response magnitudes, latencies, and adaptation properties d Angular tuning explained by both mechanoreceptor location and mechanics d Electron microscopy shows unique geometry for Merkel endings near ring sinus

During active tactile exploration with their whiskers (vibrissae), rodents can rapidly orient to an object even though there are very few proprioceptors in the whisker muscles. Thus a long-standing question in the study of the vibrissal system is how the rat can localize an object in head-centered coordinates without muscle-based proprioception. We used a three-dimensional model of whisker bending to simulate whisking motions against a peg to investigate the possibility that the 3D mechanics of contact from a single whisker are sufficient for localization in head-centered coordinates. Results show that for nearly all whiskers in the array, purely tactile signals at the whisker base – as would be measured by mechanoreceptors, in whisker-centered coordinates – could be used to determine the location of a vertical peg in head-centered coordinates. Both the “roll” and the “elevation” components of whisking kinematics contribute to the uniqueness and resolution of the localization. These results offer an explanation for a behavioral study showing that rats can more accurately determine the horizontal angle of an object if one column, rather than one row, of whiskers is spared.

Recent work has quantified the geometric parameters of individual rat vibrissae (whiskers) and developed equations that describe how these parameters vary as a function of row and column position across the array. This characterization included a detailed quantification of whisker base diameter and arc length as well as the geometry of the whisker medulla. The present study now uses these equations for whisker geometry to quantify several properties of the whisker that govern its mechanical behavior. We first show that the average density of a whisker is lower in its proximal region than in its distal region. This density variation appears to be largely attributable to the presence of the whisker cuticle rather than the medulla. The density variation has very little effect on the center of mass of the whisker. We next show that the presence of the medulla decreases the deflection of the whisker under its own weight and also decreases its mass moment of inertia while sacrificing <1% stiffness at the whisker base compared with a solid whisker. Finally, we quantify two dimensionless parameters across the array. First, the deflection-to-length ratio decreases from caudal to rostral: caudal whiskers are longer but deflect more under their own weight. Second, the nondimensionalized radius of gyration is approximately constant across the array, which may simplify control of whisking by the intrinsic muscles. We anticipate that future work will exploit the mechanical properties computed in the present study to improve simulations of the mechanosensory signals associated with vibrissotactile exploratory behavior. NEW & NOTEWORTHY The mechanical signals transmitted by a whisker depend critically on its geometry. We used measurements of whisker geometry and mass to quantify the center of mass, mass moment of inertia, radius of gyration, and deflection under gravity of the whisker. We describe how variations in these quantities across the array could enhance sensing behaviors while reducing energy costs and simplifying whisking control. Most importantly, we provide derivations for these quantities for use in future simulation work.