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Abstract
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.
Highlights
Many rodents, including rats, exhibit 5 – 12 Hz “whisking” motions of the large facial vibrissa as they tactually explore the environment
How does the rat know the angular position of the whisker at the instant of whisker-object contact? Several possible answers to this question have been proposed by three behavioral studies that have quantified the degree to which rodents can localize an object in the horizontal plane (Knutsen et al, 2006; Mehta et al, 2007; O’Connor et al, 2010)
Given that the kinematic equations for 3D whisker motion were obtained from the head-fixed animal (Knutsen et al, 2008), the present work simulates whisking in the head-fixed rat
Summary
Many rodents, including rats, exhibit 5 – 12 Hz “whisking” motions of the large facial vibrissa as they tactually explore the environment. A large open question, is how the rat might localize an object in head-centered coordinates without muscle-based proprioception. How does the rat know the angular position of the whisker (and the object) at the instant of whisker-object contact? Several possible answers to this question have been proposed by three behavioral studies that have quantified the degree to which rodents can localize an object in the horizontal plane (Knutsen et al, 2006; Mehta et al, 2007; O’Connor et al, 2010). Mehta et al (2007) propose that the rat integrates a binary touch signal with kinesthetic information about the angular position of the vibrissa at the time of contact. The authors suggest that the kinesthetic signal could be generated either in the periphery, via “whisking” neurons of the trigeminal ganglion (Zucker and Welker, 1969; Szwed et al, 2003, 2006; Leiser and Moxon, 2007; Khatri et al, 2009; Wallach et al, 2016) or from a cortical reafferent signal
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