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

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.

Cortical control of adaptation and sensory relay mode in the thalamus

“…Thalamic Adaptation Is Reduced by L6 Activation. Behaviorally relevant inputs for mice and rats are sequences of whisker stimuli that occur when a mouse rhythmically moves its whiskers during exploration and when the whiskers are swept along objects with uneven surfaces (32). As in other sensory thalamo-cortical systems, VPM neurons exhibit characteristic rapid adaptation to sensory inputs (6,33,34).…”

Long-term In Vivo Calcium Imaging of Astrocytes Reveals Distinct Cellular Compartment Responses to Sensory Stimulation

“…Mice use their whiskers for vibrotactile perception mediated by high frequency changes in whisker position (Wolfe et al 2008;Jadhav et al 2009;Mayrhofer et al 2015). Recently, our group characterized the neuronal population response to increasing frequencies of whisker deflection and found that while many neurons respond weakly to stimulation, a subset of highly-responding neurons (~3%) reliably discriminate different stimuli (Mayrhofer et al 2015).…”

“…In order to study the local astrocyte response to somatosensory activation, we used two different stimulation paradigms: electrical hindpaw stimulation (400 µA at 4 Hz for 5 s, Movie 1) and single whisker deflection (1 s duration) at different frequencies known to mimic "stick-slip" events from whisking on textured surfaces (Movie 2; (Wolfe et al 2008;Jadhav et al 2009;Mayrhofer et al 2015)). …”

Correlated physiological and perceptual effects of noise in a tactile stimulus

“…2B), the sensory system may record whisking motion equally well, no matter whether it is periodic or irregular 24). On the other hand, during object contact, whisker motion can be characterized as an irregular vibration containing frequencies up to a few hundred Hz (25)(26)(27)(28)(29)(30)(31)(32). The "noisiness" of such kinetic profiles would evoke a particularly robust and temporally precise cortical response.…”