Detection of tactile inputs in the rat vibrissa pathway

Abstract

The rapid detection of sensory inputs is crucial for survival. Sensory detection explicitly requires the integration of incoming sensory information and the ability to distinguish between relevant information and ongoing neural activity. In this study, head-fixed rats were trained to detect the presence of a brief deflection of their whiskers resulting from a focused puff of air. The animals showed a monotonic increase in response probability and a decrease in reaction time with increased stimulus strength. High-speed video analysis of whisker motion revealed that animals were more likely to detect the stimulus during periods of reduced self-induced motion of the whiskers, thereby allowing the stimulus-induced whisker motion to exceed the ongoing noise. In parallel, we used voltage-sensitive dye (VSD) imaging of barrel cortex in anesthetized rats receiving the same stimulus set as those in the behavioral portion of this study to assess candidate codes that make use of the full spatiotemporal representation and to compare variability in the trial-by-trial nature of the cortical response and the corresponding variability in the behavioral response. By application of an accumulating evidence framework to the population cortical activity measured in separate animals, a strong correspondence was made between the behavioral output and the neural signaling, in terms of both the response probabilities and the reaction times. Taken together, the results here provide evidence for detection performance that is strongly reliant on the relative strength of signal versus noise, with strong correspondence between behavior and parallel electrophysiological findings.

Fig. 1.

A go/no-go behavioral detection task was used to probe the sensitivity of head-fixed rats to brief whisker deflections. A: schematic of the behavioral apparatus. Head-fixed animals were trained to respond to air puff stimuli delivered to their whiskers by licking a response spout. B: timeline of the behavioral task. After a tone, the tactile stimulus was presented at a random time, where the duration between the tone and the stimulus was drawn from a uniform distribution on 1.5–5.5 ms. To discourage guessing, a “no-lick period” was imposed in which any licks within 1 s prior to the forthcoming stimulus resulted in an additional delay of the stimulus. Animals had a 500-ms window in which to respond by licking the spout after the delivery of a stimulus. Responses to air puff (S+) trials were rewarded with a 70- to 100-μl drop of water. Catch (S−) trials were interleaved on 10% of trials, where a distracter nozzle (positioned near the air nozzle but not aimed at the vibrissae) was activated to test for chance response probability. Responses on S− trials were penalized with a 5- to 10-s time-out in which the stimulus light was activated. Failure to respond on S+ trials was not penalized, and correctly withholding on S− trials was not rewarded. C: to quantify the strength of the air puff stimulus, high-speed video was recorded while the stimulus was delivered to an anesthetized animal with only a single row of whiskers remaining. Shown are 4 frames from a representative video with a tracking polynomial overlaid on the C2 whisker, which was the whisker that was deflected maximally by the air puff. Although multiple whiskers were deflected, only the maximally deflected whisker was considered for tracking purposes. The polynomial fit to the whisker is designated by the solid white line, while the dashed white line indicates the initial position of the whisker. The coordinate system used in the tracking algorithm is shown in the 1st frame.

Fig. 2.

Response probability increased and reaction time decreased with increasing stimulus strength. A: lick response rasters for a single animal for 3 deflection velocities. The light gray region indicates the enforced no-lick period, and the dark gray region indicates the 500-ms response window. Each tick mark in the lick raster indicates the contact of the tongue with the water spout, with all first licks falling within the response window highlighted in black (rewarded lick). The responses are divided into 50-ms bins in the accompanying histograms, with first licks again highlighted in black. B: psychometric curves for each of the 5 individual animals. Solid lines represent sigmoidal fits to the response probabilities at each of the 11 tested deflection velocities (see methods). Individual mean response probabilities are shown for each of the 5 animals. C: psychometric curve for all 5 animals combined. Each data point represents the response probability at a particular deflection velocity with data pooled across all 5 animals. The solid line is the sigmoidal fit to the data, and the dashed horizontal line represents the response probability on catch trials, which is the experimentally derived measure of chance performance. The average detection threshold, which is defined as the deflection strength at which the animals detect the stimulus 50% of the time, was ∼125°/s. D: mean reaction times for all 5 animals for the 5 highest deflection velocities. There is a 52-ms decrease in the reaction time from the fifth-highest deflection velocity to the highest (P < 0.005, 2-sample t-test).

Fig. 3.

Self-motion of whiskers degrades detection performance. In a subset of behavioral trials, the whiskers were trimmed, leaving only the C row to facilitate imaging. High-speed video was collected during presentation of the 121°/s stimulus, which corresponded to the velocity at which the animals responded correctly on 45% of the trials with the full vibrissa array intact. A: whisker angle at the base was measured with custom tracking software, and trials were categorized based on the total power in the 0–15 Hz frequency band. Shown are representative examples of both a nonwhisking and a whisking trial. B: average power for all of the whisking (solid line) and nonwhisking (dashed line) trials in the 150 ms prior to stimulus onset, with the shaded region representing 1 standard deviation about the mean. Inset shows all of the whisking trials (top) and all of the nonwhisking trials (bottom). Behaviorally correct and incorrect trials are black and gray, respectively. C: the response probability was significantly higher during periods of reduced self-motion prior to the arrival of the stimulus. Response probabilities for the 2 conditions were 0.55 and 0.24, respectively. Error bars represent 95% confidence intervals. *Statistical significance between the response probabilities under the 2 conditions (P = 0.0313, Wilcoxon rank sum test).

Fig. 4.

Voltage-sensitive dye (VSD) imaging was used to characterize the layer 2/3 cortical population response to the air puff stimuli. A: schematic of the VSD system. After a craniotomy was performed over the barrel cortex, VSD RH1691 was allowed to diffuse into the cortex. A high-speed camera was subsequently focused 300 μm below the cortical surface, and images of cortical surface were captured every 5 ms. B: image frames showing the spatiotemporal evolution of the signal during the 55 ms after stimulus onset for 5 stimulus strengths. Frames representing the initial 15 ms are not shown. Background image shows the region of cortex being imaged. Responses were smoothed with a 3 × 3 boxcar filter, and any response <10% of the maximum value was excluded for visualization purposes. ΔF/F₀, differential fluorescence normalized to background fluorescence.

Fig. 5.

Neurometric performance based on an accumulating evidence model of the VSD signal predicts psychometric performance. A: a circular area with a radius of 1 mm centered at the center of mass of the peak signal, designated with a white X, was treated as the input to the accumulating evidence model. Shown are the averaged responses to the strongest air puff stimulus from 15 to 100 ms, with only the signal inside the region of interest shown. Below is the spatial average of these frames for each of the individual trials. B: the neurometric signal is generated from leaky integration of the VSD signal from A. Specifically, the VSD signal was convolved with an exponential window with a time constant of 20 ms. Shown are the mean and standard deviation of the integrated response for the strongest (335°/s, shown in purple) and the fifth-strongest (154°/s, shown in cyan) velocities. For a given detection threshold, the probability of crossing that threshold was calculated for each of the 11 deflection strengths. The value of the threshold was chosen to minimize the mean squared error between the calculated response probabilities and those measured behaviorally (Fig 2C). C: the neurometric-psychometric match using the optimized threshold values. The neurometric data points represent the average across 2 animals. D: the neurometric latencies were measured as the time that each integrated population response crossed the optimized threshold. Note that responses that fail to reach the threshold are not included in the measured neurometric latency. E: comparison of both the total change in latencies and the % change in latencies from the strongest presented stimulus to the threshold-level stimulus. Black bars represent the values measured from the behaving animals, and red bars represent the output of the accumulating evidence model. The absolute change in neurometric latency is not reflective of the absolute change in the animals' reaction times, but the relative change provides much closer correspondence.