Changes in S1 neural responses during tactile discrimination learning

Abstract

In freely moving rats that are actively performing a discrimination task, single-unit responses in primary somatosensory cortex (S1) are strikingly different from responses to comparable tactile stimuli in immobile rats. For example, in the active discrimination context prestimulus response modulations are common, responses are longer in duration and more likely to be inhibited. To determine whether these differences emerge as rats learned a whisker-dependent discrimination task, we recorded single-unit S1 activity while rats learned to discriminate aperture-widths using their whiskers. Even before discrimination training began, S1 responses in freely moving rats showed many of the signatures of active responses, such as increased duration of response and prestimulus response modulations. As rats subsequently learned the discrimination task, single unit responses changed: more cortical units responded to the stimuli, neuronal sensory responses grew in duration, and individual neurons better predicted aperture-width. In summary, the operant behavioral context changes S1 tactile responses even in the absence of tactile discrimination, whereas subsequent width discrimination learning refines the S1 representation of aperture-width.

Fig. 1.

Schematic of the aperture-width discrimination task. On each correct trial, the distance between 2 retractable bars is set to a narrow or wide value, the main door opens, the rat enters the stimulus chamber, and samples the aperture with its facial whiskers and retreats to the left reward port if the aperture was narrow or the right reward port if the aperture was wide.

Fig. 2.

Typical single unit responses. Colored bars beneath each response histogram indicate periods of significantly increased (red) or decreased firing (blue). A: single-unit responses recorded in anesthetized rats in response to moving aperture that reproduces the stimulus in awake behaving rats. The dual peaks reflect onset and offset responses. B: responses recorded before discrimination training, with no aperture stimulus presented (the no stimulus case). Robust, diverse response modulations persist in somatosensory cortex (S1) despite the absence of whisker stimulation around t = 0. C: responses during 2nd phase of training, when a stimulus is present in the box but the rats are not required to discriminate aperture width. D: responses during phase 3 in a rat that successfully performed the aperture-width discrimination task. E: mean poststimulus time histograms (PSTHs) ± SE in anesthetized animals (black curve), in the absence of the aperture stimulus during phase 2 of training (green curve), before discrimination training, phase 2 (blue curve), and during discrimination training, phase 3 (red curve). The relatively flat average during the active task conditions (green, blue, red curves) reflects the diversity of active responses and contrasts with the stereotyped, stimulus-locked phasic passive responses recorded in anesthetized animals (black curve). Note the difference in y-axis limits. F: examples of changes in PSTHs of individual neurons. Top row: single-unit PSTHs from 3 different units recorded during phase 2 of training. Second row: PSTHs from the same units as in the 1st row, with the units recorded during phase 3 [P3(N) indicates the PSTH is from day N of phase 3 training]. Third row: mean ± SE of the action potential for the units in phase 2 (red trace) and phase 3 (green trace). The amplitude of the waveforms is smaller on later days of training, but we were able to trace this change in waveform shape over the course of training the animals.

Fig. 3.

S1 response latency and duration distributions before discrimination training (P2, blue curves), at an intermediate stage of learning (P3 < 75%, green curves), and after reaching a criterion of 75% correctly discriminated trials (P3 > 75%, red curves). A: distribution of response durations for excited (left) and inhibited (right) response modulations. B: distribution of latencies (relative to the aperture beam break at t = 0) of excited (left) and inhibited (right) response modulations.

Fig. 4.

Distributions of whisker contact durations. Comparison of relative frequency of time of contact between whiskers and discriminanda in phase 2 (blue: n = 4 rats; 346 total trials) and phase 3 (red: n = 4 rats; n = 374 total trials) animals. Phase 3 rats were above criterion in performance (i.e., >75% correct).

Fig. 5.

S1 single-unit aperture-width tuning curves from behaving rats get steeper with discrimination training. A: average tuning curve ± SE for phase 2 (blue) and phase 3 (red) animals. The difference between the 2 responses is greater in phase 3. B: frequency histogram of tuning-differences for all neurons recorded in phase 2 (blue) and phase 3 (red). The abscissa is proportional to the slope of the tuning curve for aperture-width. The median response-difference over all cells is indicated by the filled circles on the abscissa. C: same histogram as in B, with the analysis restricted to wide-preferring neurons. The median response-difference changes very little between phase 2 and phase 3. D: when the analysis is restricted to narrow-preferring neurons, the change in the slope of the tuning curves is significantly different in phase 2 (blue) vs. phase 3 (red).

Fig. 6.

S1 single-unit single-trial stimulus predictions improve with learning. The average percent of trials correctly classified as narrow or wide stimulus trials is plotted as a function of time relative to the stimulus beam-break at t = 0, for all prediscrimination units (phase 2, solid blue curve), for all units during discrimination training sessions (phase 3, dashed black curve), and for phase 3 units from sessions with 75% or greater correct behavioral performance (P3 > 75%, solid red curve). The classification algorithm attempts to predict the stimulus on each trial based on each neuron's firing during a 0.5-s window. Performance is plotted at the start of each window, so better than chance performance can begin ≤500 ms before t = 0. Error bars denote SE based on the average over units. Asterisks indicate result of statistical comparison between the population of learning vector quantization (LVQ) results from neurons in P3 > 75% sessions and phase 2 sessions (*P < 0.005, **P < 0.0005; two-sided t-test).

Fig. 7.

Quantifying rat behavior during learning. A: image from the discrimination chamber as the rat approaches the center nose poke (CNP) at the back of the chamber. B: the same image as in A, with the 5 behavioral variables shown. C and D: the mean behavioral trajectory before (red) and after (blue) learning. The filled circle in the center of the ring is the mean position of the rat's head, the line connecting a circle's center and edge represents the mean orientation of the rat's head, and the left and right lines represent the mean angle of the left and right whiskers, respectively, with respect to the rat's face. C: the mean trajectory for the rat with the most significant change in trajectory over learning (P < 0.001), whereas D shows the trajectories for the rat with the least significant trajectory change (P = 0.05).