Rapid spectrotemporal plasticity in primary auditory cortex during behavior

Abstract

Complex natural and environmental sounds, such as speech and music, convey information along both spectral and temporal dimensions. The cortical representation of such stimuli rapidly adapts when animals become actively engaged in discriminating them. In this study, we examine the nature of these changes using simplified spectrotemporal versions (upward vs downward shifting tone sequences) with domestic ferrets (Mustela putorius). Cortical processing rapidly adapted to enhance the contrast between the two discriminated stimulus categories, by changing spectrotemporal receptive field properties to encode both the spectral and temporal structure of the tone sequences. Furthermore, the valence of the changes was closely linked to the task reward structure: stimuli associated with negative reward became enhanced relative to those associated with positive reward. These task- and-stimulus-related spectrotemporal receptive field changes occurred only in trained animals during, and immediately following, behavior. This plasticity was independently confirmed by parallel changes in a directionality function measured from the responses to the transition of tone sequences during task performance. The results demonstrate that induced patterns of rapid plasticity reflect closely the spectrotemporal structure of the task stimuli, thus extending the functional relevance of rapid task-related plasticity to the perception and learning of natural sounds such speech and animal vocalizations.

Keywords: ferrets; primary auditory cortex; tone sequence.

Figure 1.

Structure of the behavioral tasks in two animals. A, Structure of the trials in ferret FerUP. The animal was trained to listen to acoustic stimuli and to withhold licking during a sequence of tone pairs with downward shifts (reference stimuli: random number of 1–5 repeats). The animal learned to approach the waterspout upon hearing an upward shifting tone pair (target) to receive a water reward. The frequencies of the tone pairs were variable, both within and between trials, and randomly shifted in frequency. In some experiments, only the tone pairs were presented (with silence between them). In others, additional spectrotemporally modulated sounds (such as TORCs or amplitude-modulated rippled noise; see Materials and Methods) were inserted between all tone pairs, and the animals learned to ignore the TORCs and continued to perform the task based on the tone pairs. B, Structure of the trials in ferret FerDN. This animal learned the same task as FerUP, except for attending to the opposite tone-pair shifts. All other details were the same. C, Behavioral performance in head-holder. The bar plot represented the average DI when the animal performed the task with its head restrained. The dashed horizontal lines indicate the threshold level defined as the mean + 2 SD of the shuffled DIs (for more details, see Yin et al., 2010). There was no difference in performance between the experimental conditions with and without the TORCs. Although both ferrets displayed significant performance, FerUP had overall a better performance in the head-holder than FerDN (Wilcoxon rank sum test, p < 0.01).

Figure 2.

The matched filter hypothesis and polar Fourier representation. A, Schematic of the predictions of the matched filter hypothesis. Rapid receptive field plasticity during behavior is predicted to reflect the difference between the discriminated reference and target sounds: Δ(reference, target). Animals attended to a spectrotemporal difference: the direction of pitch shift in tone pairs that have random absolute frequencies. Consequently, plasticity is predicted to reflect the change in pitch direction via ΔSTRF of the responding neurons. B, The 2D polar Fourier transforms of the two-tone sequences. The stimuli, STRFs, and ΔSTRFs can be better visualized through their Fourier transforms, which specifically highlight the directional information in the stimuli through their asymmetry around the midline. In general, directionally shifting stimuli or tilted STRFs exhibit an asymmetric Fourier transforms. For the tone pairs, the asymmetry is reversed in the LD and HD regions, which are separated by the white horizontal line in the panels. Because of the “aversive” nature of the reference stimuli (compared with the “appetitive” target), the asymmetry of the Fourier transforms of ΔSTRF (denoted by F(ΔSTRF)) is predicted to match the asymmetry pattern of the Fourier transform of the difference of the reference and target stimuli: F (Ref) − F (Tar). The example shown represents the case when the reference (target) stimulus is the up-shifting (down-shifting) tone sequence. C, All Fourier transforms shown are plotted on a polar grid, which spreads them out more evenly and clearly. The sinusoidal spectra (called “ripples”) are the basis functions of the Fourier transform of the spectrotemporal stimulus and STRF patterns. Left panels, Normal distribution of ripple coefficients in the Fourier domain, with positive rates (ω) and spectral densities (Ω) corresponding to downward-moving ripples, and negative rates to upward-moving ripples. In the polar Fourier transform, the coefficients of the ripples are simply rearranged on a grid such that all ripples in a given column have the same orientation (π) and are organized from 0 to π orientations. They are arranged with increasing density up the ordinate.

Figure 3.

The 2D polar Fourier transforms of STRFs and ΔSTRF. A, B, Two examples of polar Fourier transforms of STRFs of A1 neurons. The directional selectivity of the STRFs is the reverse of their STRF tilts. Thus, the slightly downward tilting STRF (in A) indeed responds more selectively to upward moving ripples, whereas the slightly upward tilting STRF (in B) is more selective for downward moving ripples. To match the directional selectivity, it is necessary to reverse the STRFs before the transformation. So, the F (STRF) and F (ΔSTRF) in all figures and text denote the reversed polar Fourier transformation. C, The procedures for computing F (ΔSTRF). The STRFs were computed from the neuronal responses to the TORCs before (STRF_Pre) and during (STRF_Dur) performance of the task. Changes in STRFs (ΔSTRF_Dur-Pre) were calculated by the subtraction of STRF_Dur − STRF_Pre. The reversed polar Fourier transformation was then applied on the STRF changes (F (ΔSTRF_Dur-Pre)), and the magnitude of this transformation is represented in the rightmost plot.

Figure 4.

Examples of STRF changes in A1 neurons during task performance. A, Examples of rapid changes in two single units from FerUP. For each unit, we illustrate the original STRF (left panels), the STRF during performing task (second panels from left), and the magnitudes of reversed-polar Fourier transform of the STRF (F (STRF)) (third panels from left) and the changes of STRF (F (ΔSTRF)) during performance of the task relative to the prior passive state (right panels). The STRFs adapted so as to enhance their sensitivity to the pitch shifts of the reference tone sequence (e.g., the downward sequence in FerUP). The asymmetry indices for LD and HD region of the reversed-polar transform are shown on the bottom and top right of each panel, respectively. As predicted in Figure 2B, both neurons show an enhancement of the asymmetry at low density toward the DN selectivity, which is highlighted by the dashed circles for (LD < 0). They also show an enhancement of the asymmetry toward the UP region (HD > 0) as predicted. B, Examples of rapid changes in two single units from FerDN. All figure conventions are the same as in 4A above. As predicted in Figure 2B, the STRFs adapted so as to enhance their sensitivity to the upward pitch shifts of the tone sequence on FerDN. Both neurons show an enhancement of the asymmetry at low and high densities, which is highlighted by the dashed circles for (LD > 0; HD < 0).

Figure 5.

Population STRF changes in different behavioral states. A, Averaged changes in the behaving animals. Top, Population averages of F (ΔSTRF_Dur-pre) from 112 units in FerUP (left) and 65 units in FerDN (right). The average is strongly asymmetric, reflecting enhanced sensitivity to DOWN shifts in FerUP, and UP shifts in FerDN, as highlighted by the dashed circles. Note the opposite asymmetry at LD and HD regions (the white dashed lines at 7 cycles/octave.s indicate the border line that divides the two regions) in both FerUP and FerDN. The asymmetry indices LD and HD are computed and are given in the bottom right and top right corners of all panels. LD versus HD asymmetry indices from all cells are shown in the scatter plot (bottom). Consistent with the matched filter hypothesis, the points tended to lie above the midline (LD − HD < 0) for FerUP (paired Wilcoxon signed rank test, p = 0.0389), and the opposite for FerDN (paired Wilcoxon signed rank test, p = 0.0004), as confirmed by the overlaid histograms of the differences. B, Averaged changes in passive post-behavior. The asymmetry of the average F (ΔSTRF_Post-pre) at both LD and HD region persisted in FerUP (left), but not in FerDN (right) after the behavior. C, Averaged changes in the naive animals. Responses to the same sequence of tone sequence sounds in a behaviorally naive animal demonstrate that presenting the stimuli passively induces very weak changes, with no significant asymmetry in the population average (F (ΔSTRF)).

Figure 6.

Two examples of directionality functions of A1 neurons. A, Frequency response curves. Neuron's frequency response curves are computed from the onset responses at different T1 frequency, which are normalized to each neuron's spontaneous activity. The BF is defined as the frequency inducing the maximum responses as indicate by the dashed vertical line. B, Raster and poststimulus time histogram representation of the response to the tone sequence. The responses to UP-step (the red) and DOWN-step (the blue) tone sequences are first aligned relative to the T2 frequency and then superimposed. The frequencies of the T1 (red and blue) and T2 tones (black) of the sequence are indicated inside each panel. *The panel in which the T2 frequency was at the neuron's BF. The vertical line in each panel indicates the onset or offset of the T1 and T2 tones. Top, Horizontal bars represent the duration of T1 (filled with gray) and T2 (filled with black). C, Directionality function of the neurons. The directional selectivity (Δ_DIR) of the response to the tone sequence was computed from the onset responses (25–75 ms onset time windows, shaded areas in B) to T2 at different T2 frequencies (see Materials and Methods). Neurons are not sensitive to the step direction in the sequence when the T2 is at the neuron's BF (Δ_DIR is near zero); however, they are sensitive to UP (DOWN) shift sequence when T2 frequency is below (above) the BF within the receptive field. D, Population directionality functions of A1 neurons. The averaged directionality function from a neuronal population (N = 143) in A1 of two naive ferrets confirms a general tendency observed around the neuron's BF in the two examples in C. *p < 0.05, significant bias in directional selectivity (t test). **p < 0.01, significant bias in directional selectivity (t test).

Figure 7.

Evidence of spectrotemporal plasticity in directionality functions. Rapid plasticity in responses to the tone pairs led to similar conclusions as those derived from analysis of STRF changes (based on responses to TORCs). A, Left, Middle, The directionality index function Δ_DIR (ordinate) reports the directional selectivity of unit responses to upward or downward tone-pair shifts. The index varies with the frequency of the second tone (T2) relative to the BF of the cell (abscissa) (e.g., for T2 at 6 to −6 semitones [st] relative to the BF of each cell). During behavior, the average indices from all FerUP cells shift significantly toward negative values (red curve and arrow), indicating an enhanced preference to DN shifts. The opposite occurs in FerDN responses (red curve and arrow). Measurements from the same cells after behavior (green curves and arrows) indicate that the enhancement weakly persists in FerUP after conclusion of the task, but not in FerDN, as indicated by the green arrows in each panel. Right, Summary of average index changes in the two behaving animals. The red bars represent significant changes during behavior relative to measurements in the prepassive state. In all, these shifts are toward negative indices in FerUP and toward positive indices in FerDN (i.e., in the same direction of enhancements as those found in the STRF changes). *Statistical significance for the change of directional index during versus before task by Wilcoxon signed rank test, or of the difference of the changes between the animals (FerUP vs FerDN) by Wilcoxon rank sum test. B, Left, Middle, In the naive animal, there were no significant shifts during the three conditions. Right, The average index changes in the naive animal showed no significant changes in the indices across the population.