Whisking Kinematics Enables Object Localization in Head-Centered Coordinates Based on Tactile Information from a Single Vibrissa

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.