Neuronal Activity in Rat Barrel Cortex Underlying Texture Discrimination

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Abstract
Rats and mice palpate objects with their whiskers to generate tactile sensations. This form of active sensing endows the animals with the capacity for fast and accurate texture discrimination. The present work is aimed at understanding the nature of the underlying cortical signals. We recorded neuronal activity from barrel cortex while rats used their whiskers to discriminate between rough and smooth textures. On whisker contact with either texture, firing rate increased by a factor of two to ten. Average firing rate was significantly higher for rough than for smooth textures, and we therefore propose firing rate as the fundamental coding mechanism. The rat, however, cannot take an average across trials, but must make an immediate decision using the signals generated on each trial. To estimate single-trial signals, we calculated the mutual information between stimulus and firing rate in the time window leading to the rat's observed choice. Activity during the last 75 ms before choice transmitted the most informative signal; in this window, neuronal clusters carried, on average, 0.03 bits of information about the stimulus on trials in which the rat's behavioral response was correct. To understand how cortical activity guides behavior, we examined responses in incorrect trials and found that, in contrast to correct trials, neuronal firing rate was higher for smooth than for rough textures. Analysis of high-speed films suggested that the inappropriate signal on incorrect trials was due, at least in part, to nonoptimal whisker contact. In conclusion, these data suggest that barrel cortex firing rate on each trial leads directly to the animal's judgment of texture. How cortical activity contributes to sensation is among biology's oldest problems. We studied the nature of the cortical representations underlying judgments of texture in rats. The rodent whisker sensory system is particularly intriguing because it is “active”: the animal generates sensory signals by palpating objects through self-controlled whisker motion (just as we move our fingertips along surfaces to measure their tactile features). Rats touched rough or smooth textures with their whiskers and turned left or right for a reward according to the texture identity. Monitoring behavior with high-speed videography, we have found that on trials when the rat correctly identified the stimulus, the firing rate of cortical neurons varies during a window of a few hundred milliseconds before making a decision according to the contacted texture: high for rough and lower for smooth. This firing-rate code is reversed on error trials (lower for rough than smooth). So when cortical neurons report the wrong stimulus, the rat, “feeling” the signals of its cortical neurons, fails to identify the stimulus. We conclude that barrel cortex firing rate on each trial predicts the animal's judgment of texture. This experiment begins to elucidate which features of cortical activity underlie the animal's capacity for tactile sensory discrimination.