Neuronal Activity in Rat Barrel Cortex Underlying Texture Discrimination

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.

Integration of Vibrotactile Signals for Whisker-Related Perception in Rats Is Governed by Short Time Constants: Comparison of Neurometric and Psychometric Detection Performance

“…This response pattern may be tuned to the timing of chunks of vibrotactile signals [e.g., stick-slip events, instances of high acceleration in the vibrotactile signal brought about by interplay of surface and whisker mechanics (Arabzadeh et al, 2005;Wolfe et al, 2008;Ritt et al, 2008)] coming in at the rhythm of sequential whisker strokes. One study reported that, indeed, rats use repetitive whisking against a texture to reach a decision, mostly 1-3 consecutive whisks (von Heimendahl et al, 2007). Assuming a whisking frequency of ϳ7 Hz and touch times of 50 ms per single whisk (von Heimendahl et al, 2007) these strips of data would be integrated using the short time constant found in the present study and then separated by ϳ100 ms to the next touch time by suppression of signal flow in barrel cortex.…”

“…One study reported that, indeed, rats use repetitive whisking against a texture to reach a decision, mostly 1-3 consecutive whisks (von Heimendahl et al, 2007). Assuming a whisking frequency of ϳ7 Hz and touch times of 50 ms per single whisk (von Heimendahl et al, 2007) these strips of data would be integrated using the short time constant found in the present study and then separated by ϳ100 ms to the next touch time by suppression of signal flow in barrel cortex. In future studies it has to be worked out whether neuronal activity generated by active whisking (Fanselow and Nicolelis, 1999;Hentschke et al, 2006) may recruit memory systems, not available to our passively detecting rats, that in addition integrates information acquired across repetitive whisker strokes.…”

“…Behavioral observation of whisking rats has revealed that tactile information is accumulated for rather short periods of time before committing to a choice. Individual touch durations are mostly Ͻ50 ms, reaching a maximum of 100 ms (von Heimendahl et al, 2007), with total palpation time (i.e., consecutive whisks) ranging from ϳ100 -700 ms, being highly task-dependent (Carvell and Simons, 1995). It is intriguing to learn that during typical touch times as found in the study of von Heimendahl et al (2007), temporal frequencies of Ͻ10 -20 Hz cannot at all be represented in the vibrotactile signal entering the ascending tactile pathway.…”

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).…”

Long-Term Plasticity in Mouse Sensorimotor Circuits after Rhythmic Whisker Stimulation

“…This form of active sensation has been compared with digital palpation and microsaccadic eye movements in primates Kleinfeld et al, 2002). A consequence of the rhythmical nature of whisking is that neuronal activity in the primary somatosensory (barrel) cortex varies rhythmically in synchrony with whisker movement and contact against obstacles (Fee et al, 1997;Crochet and Petersen, 2006;von Heimendahl et al, 2007). The vibrissal motor cortex, which controls whisker movement (Brecht et al, 2004), is interconnected with both cortical and subcortical somatosensory structures (Miyashita et al, 1994), and activity in the motor cortex is also modulated synchronously with whisker movement (Kleinfeld et al, 2002;Chakrabarti et al, 2008).…”