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. 2007 Nov;5(11):e305.
doi: 10.1371/journal.pbio.0050305.

Neuronal activity in rat barrel cortex underlying texture discrimination

Moritz von Heimendahl  1 , Pavel M Itskov, Ehsan Arabzadeh, Mathew E Diamond
Affiliations

Neuronal activity in rat barrel cortex underlying texture discrimination

Moritz von Heimendahl et al. PLoS Biol. 2007 Nov.

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.

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Conflict of interest statement

Competing interests. The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Texture Discrimination Tasks
Trials sketched from camera images. (A) The 1-arm task. (i) The rat perched on the edge of the platform and extended to touch the rough texture (gray rectangle) with its whiskers. (ii) Having identified the texture, the rat turned to the right drinking spout and received a water reward. (B) The 3-arm task. (i) The rat began by crossing from the start arm to the central platform, (ii) touched the smooth-textured discriminandum with its whiskers, (iii) rejected the first texture and proceeded to touch the rough-textured discriminandum, and (iv) crossed the gap to collect a water reward at the distant part of the arm.
Figure 2
Figure 2. Behavior and Neuronal Activity in a Typical Trial
(A) Spatial arrangement of the two high-speed cameras. (B) Images from high-speed films taken from two different views (top row—top view, bottom row—side view, see [A] for positions; frame pairs of the upper and lower rows are synchronous). Whisker C2 is traced. Although in the side view, the rat's snout seemed to touch the texture, the corresponding top view frames show that this was not the case. Although on a small proportion of trials, rats were close enough that microvibrissae contact could not be excluded, this happened too rarely to explain the animals' high performance. (C) Spikes fired by a neuronal cluster whose receptive field was centered on whisker C2. Estimated moment of choice is given by gray vertical line at 0 ms. Contacts of the selected whisker before decision are marked as red frames. Note the increase in firing rate during contact. Contacts after choice are not highlighted, and the corresponding spikes were not considered in the analysis. Shown: rat 16, session 2006-07-23, cluster #58, trial 20, smooth texture.
Figure 3
Figure 3. Activity of the Same Neuronal Cluster in the Course of a Session
Trial 20, depicted in Figure 2, is highlighted by a green box. Spike times are relative to moment of choice (gray line). Contacts of whisker C2 occurring before choice are marked by red frames. Note the increase in firing rate during contact. On missing trial numbers, whisker contact times could not be defined.
Figure 4
Figure 4. Whisker Touch Statistics
For the whiskers of interest, contact onset and offset times were measured for all touches ending prior to the moment of choice. (A) Number of touches per trial per whisker (red—rough texture; blue—smooth texture) (B) Individual touch durations. (C) Summated duration of all touches of a single whisker per trial. (D) Time from first contact of the whisker of interest to the rat's choice. Values are consistent with a reported range of 150 to 500 ms in a different texture discrimination task [34].
Figure 5
Figure 5. Contact and Texture Indices on Whisker Touch
(A) Distribution of the contact index, C. All clusters have C > 1, equivalent to an increase in firing rate on contact. (B) Distribution of texture index, T. Most clusters have T > 0, equivalent to a higher firing rate for rough than for smooth contact. (C) Correlation between contact index and texture index across clusters. The green points are single neurons.
Figure 6
Figure 6. Dynamics of Neuronal Response During Whisker Contact
Spike times were aligned to the onset of each whisker contact; onset time was set to 0 ms. Touches had a wide range of durations (see Figures 3 and 4) so that response values at progressively later times were gathered from progressively fewer contacts; only 30% lasted longer than 80 ms. (A) Quartile plot of firing rates. The interquartile range (25% to 75% of neuronal clusters) is shaded gray; the black line is the mean. All clusters were normalized by dividing by their average rates across the whole session. (B) Magnified view of mean response onset. (C) Response dynamics separated by texture.
Figure 7
Figure 7. Average Normalized Firing Rate as a Function of Texture
Firing rates were aligned to the moment of choice (0 ms) and binned in a sliding 250-ms window, centered on each data point. Each cluster's firing rates were divided by the recording session mean rate (note the value of 1.0 before whisker contact, at −600 ms), then the average was calculated across all clusters. The unmasked area, from −200 to 0 ms, shows the strongest texture coding before the rat's choice. Texture-related differences after the rat's choice were a consequence of the different actions rats performed in correspondence with each texture (e.g., turn left or turn right) and were not further analyzed.
Figure 8
Figure 8. Texture Coding Before Choice
(A) Upper panel: texture index T calculated for backwards-growing windows from 0 ms (moment of choice) to −t, averaged across correct trials only; Black trace: average across all clusters; green trace: single neurons only; Lower panel: significance of T > 0 for all clusters. The dashed line shows the 5% limit. (B) Texture index T on correct trials only (black trace, carried over from [A]) versus random trials (gray trace); Lower panel: significance of the difference between correct and random trials.
Figure 9
Figure 9. Texture Coding in Local Field Potential (LFP)
(A) LFP curves aligned on moment of choice and averaged across trials. (B) LFP curves aligned on moment of first touch of any whisker. (C) Upper panel: LFP Texture Index TLFP on correct trials only compared to random trials, integrated across backwards-growing windows from the moment of choice to −t. Lower panel: significance of TLFP being greater than chance on correct trials (black trace) and significance of TLFP being greater on correct trials compared to random trials (gray trace). For both, p < 0.05 for t = −75 ms.
Figure 10
Figure 10. Texture Information Carried by Firing Rate
Upper panel: information about the two stimuli transmitted by firing rate, averaged across clusters, using backwards-growing windows as in Figure 8A, for correct only and random trials. Lower panel: significance of the information on correct trials being greater than chance (black trace) and significance of the information on correct trials being greater than on random trials (gray trace); p < 0.05 for time windows from −75 to 0 ms. The dashed line shows the 5% limit.
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