Behavioral study of whisker-mediated vibration sensation in rats

Abstract

Rats use their vibrissal sensory system to collect information about the nearby environment. They can accurately and rapidly identify object location, shape, and surface texture. Which features of whisker motion does the sensory system extract to construct sensations? We addressed this question by training rats to make discriminations between sinusoidal vibrations simultaneously presented to the left and right whiskers. One set of rats learned to reliably identify which of two vibrations had higher frequency (f(1) vs. f(2)) when amplitudes were equal. Another set of rats learned to reliably identify which of two vibrations had higher amplitude (A(1) vs. A(2)) when frequencies were equal. Although these results indicate that both elemental features contribute to the rats' sensation, a further test found that the capacity to discriminate A and f was reduced to chance when the difference in one feature was counterbalanced by the difference in the other feature: Rats could not discriminate amplitude or frequency whenever A(1)f(1) = A(2)f(2). Thus, vibrations were sensed as the product Af rather than as separable elemental features, A and f. The product Af is proportional to a physical entity, the mean speed. Analysis of performance revealed that rats extracted more information about differences in Af than predicted by the sum of the information in elemental differences. These behavioral experiments support the predictions of earlier physiological studies by demonstrating that rats are "blind" to the elemental features present in a sinusoidal whisker vibration; instead, they perceive a composite feature, the speed of whisker motion.

Fig. 1.

Schematic representation of the stimuli and the behavioral paradigm. (A) (Left) Stimulus space. Each circle represents the frequency–amplitude combination of one stimulus. In every experiment, specific stimuli were defined as either S+ or S−. In this example, stimuli with amplitude of 2A were S+ whereas those with amplitude A were S−. (Right) Brief (50 ms) segments of the same stimuli. (B) The rat initiated a trial by a nose poke into the aperture while touching the two mesh plates with its whiskers (Left). After a random delay period during which the rat maintained its position in the nose poke, it received two simultaneous vibrations on its left and right whisker pads (Center). In each trial, one of the two vibrations was S+ and the other was S−. Having identified the S+ vibration, the rat expressed its choice by turning toward the corresponding drinking spout, e.g., to the right in this example. Correct judgments were rewarded by sucrose water (Right).

Fig. 2.

Experiment 1a: Discrimination of stimuli by frequency difference. (A) Phase 1. (Left) Two frequencies (f = 37.5 Hz and 2f = 75 Hz) and two amplitudes (A = 13 μm and 2A = 26 μm) were combined to generate four vibrations. Stimuli that were presented together and had to be discriminated (paired stimuli) are connected by a shaded line (d₁ and d₂). S+ stimuli were defined by 2A. (Right) Performance is plotted for individual rats across all trials collected over 7 sessions. Error bars in A–C are the 95% confidence interval (Wilson score). (B) Phase 2. (Left) Stimuli were identical to those in phase 1, but paired differently. The solid line indicates the pair in which both amplitude and frequency differed with the same sign (delta-Af) whereas the shaded line indicates the pair in which amplitude and frequency differed with opposite signs (iso-Af). (Right) Performance is plotted for individual rats across all trials collected over 11 sessions. (C) Phase 3. (Left) All stimulus pairs from phases 1 and 2 were intermixed. (Right) Performance is plotted for individual rats across all trials collected over 10 sessions.

Fig. 3.

Experiment 1b: Discrimination of stimuli by amplitude difference. (A) Phase 1. (Left) Two frequencies (f = 37.5 Hz and 2f = 75 Hz) and two amplitudes (A = 13 μm and 2A = 26 μm) were combined to generate four vibrations. Stimuli that were presented together and had to be discriminated (paired stimuli) are connected by a shaded line (d₁ and d₂). S+ stimuli were defined by 2A. (Right) Performance is plotted for individual rats across all trials collected over 6 sessions. (B) Phase 2. (Left) Stimuli were identical to those in phase 1, but paired differently. The solid line indicates the pair in which both amplitude and frequency differed with the same sign (delta-Af) whereas the shaded line indicates the pair in which amplitude and frequency differed with opposite signs (iso-Af). (Right) Performance is plotted for individual rats across all trials collected over 10 sessions. Error bars indicate the 95% confidence interval (Wilson Score).

Fig. 4.

Experiment 2: Stimulus dimensions underlying the percept. (A) (Left) Group 1. Three frequencies (1/2 f = 40 Hz, f = 80 Hz and 2f = 160 Hz) and two amplitudes (A = 16 μm and 2A = 32 μm) were used to generate five vibrations. (Right) Group 2. Two frequencies (f = 80 Hz and 2f = 160 Hz) and three amplitudes (1/2 A = 8 μm, A = 16 μm, and 2A = 32 μm) were combined to generate five vibrations. Stimuli that were presented together and had to be discriminated (paired stimuli) are connected by lines: The dotted and solid lines indicate discriminations along delta-Af contours. The lines with dark shading indicate discriminations along elemental features [A (Left) and f (Right)]. The lines with light shading indicate discriminations along iso-Af counters. (B) The average discrimination performances across four rats. Each bar represents a specific stimulus pair, using the same color key as in A. The x axis shows the net difference between stimuli in elemental features. E denotes a unit (100%) change in any elemental feature A or f. (C) Same data as in B, replotted here as a function of the Af difference. Error bars indicate the SEM.