Texture Coding in the Rat Whisker System: Slip-Stick Versus Differential Resonance

Top Cited Papers
Open Access
Publisher Website
Google Scholar
Abstract
Rats discriminate surface textures using their whiskers (vibrissae), but how whiskers extract texture information, and how this information is encoded by the brain, are not known. In the resonance model, whisker motion across different textures excites mechanical resonance in distinct subsets of whiskers, due to variation across whiskers in resonance frequency, which varies with whisker length. Texture information is therefore encoded by the spatial pattern of activated whiskers. In the competing kinetic signature model, different textures excite resonance equally across whiskers, and instead, texture is encoded by characteristic, nonuniform temporal patterns of whisker motion. We tested these models by measuring whisker motion in awake, behaving rats whisking in air and onto sandpaper surfaces. Resonant motion was prominent during whisking in air, with fundamental frequencies ranging from approximately 35 Hz for the long Delta whisker to approximately 110 Hz for the shorter D3 whisker. Resonant vibrations also occurred while whisking against textures, but the amplitude of resonance within single whiskers was independent of texture, contradicting the resonance model. Rather, whiskers resonated transiently during discrete, high-velocity, and high-acceleration slip-stick events, which occurred prominently during whisking on surfaces. The rate and magnitude of slip-stick events varied systematically with texture. These results suggest that texture is encoded not by differential resonant motion across whiskers, but by the magnitude and temporal pattern of slip-stick motion. These findings predict a temporal code for texture in neural spike trains. A fundamental problem in neuroscience is understanding how behaviorally relevant information is collected by a sensory organ and subsequently encoded by the brain. By actively moving their whiskers, rats can discriminate fine differences in textures. Little is known, however, about how whisker dynamics reflect texture properties or how the nervous system encodes this information. In one hypothesis, whisker motion over a texture produces a unique, texture-specific temporal profile of velocity, which is encoded in the temporal pattern of neural activity. In a second, alternative hypothesis, textures excite a specific subset of whiskers due to intrinsic, whisker-specific mechanical resonance frequencies. Information is then encoded by the spatial distribution of neural activity in whisker-related columns in cortex. Here, we assess these hypotheses by measuring whisker motion as animals whisk across sandpapers of varying roughness. We found that whiskers resonate in air and on surfaces, but that these resonance vibrations do not vary with, and therefore do not encode, texture. Instead, whisker motion over a textured surface produces fast, transient slip-stick events whose dynamics are dependent on texture roughness. Texture is likely to be encoded in the temporal pattern of spikes evoked by these slip-stick events.