Behavioral Properties of the Trigeminal Somatosensory System in Rats Performing Whisker-Dependent Tactile Discriminations

Abstract

To address several fundamental questions regarding how multiwhisker tactile stimuli are integrated and processed by the trigeminal somatosensory system, a novel behavioral task was developed that required rats to discriminate the width of either a wide or narrow aperture using only their large mystacial vibrissae. Rats quickly acquired this task and could accurately discriminate between apertures of very similar width. Accurate discriminations required a large number of intact facial whiskers. Systematic removal of individual whiskers caused a decrease in performance that was directly proportional to the number of whiskers removed, indicating that tactile information from multiple whiskers is integrated as rats gauge aperture width. In different groups of rats, different sets of whiskers were removed in patterns that preferentially left whisker rows or whisker arcs intact. These different whisker removals caused similar decreases in performance, indicating that individual whiskers within the vibrissal array are functionally equivalent during performance of this task. Lesions of the barrel cortex abolished the ability of rats to discriminate, demonstrating that this region is critically involved in this tactile behavior. Interestingly, sectioning the facial nerve, which abolished whisker movements, did not affect the ability to perform accurate discriminations, indicating that active whisker movements are not necessary for accurate performance of the task. Collectively, these results indicate that the trigeminal somatosensory system forms internal representations of external stimuli (in this case, aperture width) by integrating tactile input from many functionally equivalent facial whiskers and that the vibrissal array can function as a fine-grained distance detector without active whisker movements.

Vibrissa-Based Object Localization in Head-Fixed Mice

“…Freely moving rodents can discriminate the roughness of textures (Guić-Robles et al, 1989;Carvell and Simons, 1990;von Heimendahl et al, 2007) and the widths of apertures (Krupa et al, 2001). Rodents also accurately judge the distances to platforms ("gap crossing") (Hutson and Masterton, 1986;Celikel and Sakmann, 2007) and the relative distance of two objects (Knutsen et al, 2006).…”

“…Rats also exhibit asymmetric whisking (Mitchinson et al, 2007;Towal and Hartmann, 2008) and irregular whisker movements during a horizontal object localization task (Knutsen et al, 2006). Active whisking is not required to solve all spatial tasks: rats can determine the width of an aperture after sectioning of the facial nerve (Krupa et al, 2001). The whisking strategies used by rodents to solve spatial localization problems are incompletely understood.…”

Two Psychophysical Channels of Whisker Deflection in Rats Align with Two Neuronal Classes of Primary Afferents

“…Psychophysical properties of whisker stimulation in rats have been assessed early on (Vincent, 1912;Schiffman et al, 1970). It has been shown that rats are capable of amazingly fine discriminations of surfaces (GuicRobles et al, 1989;Carvell and Simons, 1990) and apertures (Krupa et al, 2001), and that discrimination of textures and object forms are optimized by active scanning movements (Carvell and Simons, 1995;Harvey et al, 2001;Prigg et al, 2002). Finally, the detectability of 1-3°whisker deflections applied by a sinusoidally modulated air stream (at 0.1-32 Hz) in mobile rats was demonstrated in the only study so far that attempted to use parameterized whisker deflections (Hutson and Masterton, 1986).…”

“…Designing such tasks is challenging because of the difficulty of applying spatiotemporally precise stimuli to awake behaving rats while precluding nonvibrissal stimulus sources (such as cutaneous receptors or the small perioral sinus hairs) under conditions which allow for the assessment of psychophysical parameters. Psychophysical studies conducted so far mostly used nonrestrained, freely moving rats sampling stimuli by using their own body and whisker movements Simons, 1990, 1995;Harvey et al, 2001;Krupa et al, 2001). Hutson and Masterton (1986) are the only investigators so far who attempted to quantify psychophysical detection thresholds with varying kinematic deflection parameters; however, rats in that study were free to move their head, and control of whisker deflection generated by air streams did not reach the level of stimulus control deemed necessary: micrometer precision at a millisecond time scale.…”

Processing of tactile information by the hippocampus

“…Such navigation is heavily dependent on the use of facial vibrissae, which are extremely sensitive tactile organs used as both highresolution tactile discriminators (2,3) and distance detectors (4,5). During exploration, the vibrissae are bilaterally swept against objects and obstacles to gather accurate information about the animal's close surroundings (2)(3)(4)(5).…”