Article Figures & Data
Figures
- Figure 1.
Experimental design: stimulus sequence for discrimination task. Two types of stimuli were used: broadband noise-like stimuli known as TORCs and pure tones. Reference and target sounds consisted of TORC-tone combinations in which the reference or target tones were of relatively short duration (250 ms) and occurred at the end of each 1 s TORC. On a given trial during a behavioral session, a random number of reference TORC tones (1-6 reference signals) was followed by a target TORC tone (except on control “catch” trials in which 7 reference TORC tones were presented with no target). The panels illustrate spectrograms of three such reference TORC tones (blue stripe denotes the reference tone) and of the following target TORC tone (red stripe denotes target tone). Responses to the TORC portions of each reference stimulus were collected in peristimulus time histograms (PSTH) that were cross-correlated with the TORC spectrograms to estimate the STRF (see Materials and Methods).
- Figure 2.
STRFs from five single units (a-e) in A1 illustrate receptive field changes observed during performance of the frequency discrimination task. a, Comparison of a prebehavior passive STRF (left) and a behavioral STRF (middle). Each panel depicts an STRF with a “rainbow” color scale ranging from red to green to blue, representing increased-to-suppressed firing about the (green) mean. The STRF in each panel was normalized, and all STRFs were then depicted on the same color scale for each unit. The contours in a demarcate the excitatory (red) and inhibitory (blue) regions with statistically significant fluctuations (level of 2.5σ) from the mean (as explained in Materials and Methods). We do not draw these contours in subsequent STRFs to avoid cluttering the figures. However, all excitatory and inhibitory features of the STRF or STRFdiff discussed subsequently are statistically significant by this criterion. The blue arrows indicate the frequency of the reference tone; the red arrows indicate the frequency of the target tone during the discrimination task. The difference between the normalized passive and behavior STRF is shown in the right (STRFdiff). An asterisk marks the location of maximal change near fR (within ±0.125 octaves from the reference) (ΔAref = -95%). No significant changes occurred at target in this unit. b, Same as in a, except that both ΔAref (-57%) and ΔAtar (61%) are significant in this unit. A square marks the maximal change near target as defined in Results. c, d, Examples of STRF depression induced at the reference tone frequencies (ΔAref = -69 and -55%; blue arrows), with small or insignificant effects at the target tone (red arrows). Postbehavior STRFs reverted to their original prebehavior shapes. e, Example of STRF depression near fR (ΔAref = -63%; blue arrow) and facilitation near fT (ΔAtar = 61%; red arrow). In this case, the postbehavior STRF did not revert to its original shape but showed a persistent enhancement at the target tone frequency (e.g., an additional decrease in the lower inhibitory sideband) and a rebound to higher than original levels of the excitatory region at reference tone frequency.
- Figure 3.
Overall summary scatter plot and smoothed distribution of local STRF changes (ΔAref vs ΔAtar) from a population of 74 single units recorded in the naive control and also from all 127 neurons recorded during discrimination behavioral sessions (including a comparison of STRF changes in high and low performance behavioral sessions). a, Scatter plot and superimposed distribution from neurons recorded in the behaving animals. The smoothed distribution is computed by first replacing each point with a 2-D Gaussian with unit area and the variances of the ΔA estimates. All Gaussians are then summed to produce the total smoothed gray-color surface shown (gray bar range on the right). Contour plots at 10% steps are also shown. Note that the distribution is skewed toward the top left quadrant, indicating tendency toward negative ΔAref and positive ΔAtar STRF changes. The side graphs indicate the corresponding 1-D histograms of ΔAref and ΔAtar. The smooth plots are the marginal distributions obtained from the contours in the middle panel. The red asterisk indicates the overall mean of each distribution, with a mean value of -18% for ΔAref and +13% for ΔAtar. The red arrows indicate the mean value of the distribution of negative ΔAref values (mean of -65%) and positive ΔAtar values (mean of +53%). b, Scatter plot and superimposed distribution from the naive animal. All other details are as in a. The distribution of changes from neurons recorded in the naive ferret appears approximately circular as would be expected from random variations in the STRF. c, Establishing the significance of the difference between the distributions of STRF changes in a and b above. The light gray points are difference vectors between randomly selected behaving and naive distributions (for details, see Results). The red vector is the net vectorial sum of all points in the behaving distribution in a. The green vector is the vectorial sum of all points in the naive distribution in b; it is relatively small because of the smaller and more highly random direction of STRF changes in this distribution. The black vector is the difference between the gray and green vectors above; its tip is represented by the large black circle that lies at the edge of the random distribution, indicating a highly significant difference between the behaving and naive distributions of STRF changes. d, The distribution of gain changes (percentage change in spike rate) between passive and active state for all 127 single units. The histogram indicates that fluctuations in gain are variable and mostly symmetric around 0. e, Graphs of three distributions of ΔAref derived from populations of neurons in the naive (green line), poor performance (LRD <2; black dashed line), and good performance (LRD >2; red line) conditions (see Materials and Methods). This figure demonstrates a negative correlation between behavioral performance and amplitude of adaptive change at reference frequency (ΔAref). f, Similar set of graphs showing a positive correlation between behavioral performance and amplitude of adaptive change at target frequency (ΔAtar).
- Figure 4.
Average change in the STRF for all frequency discrimination experiments. a, The left panel illustrates the average plastic change in STRF as a function of log frequency away from the reference frequency (centered at 0 and marked by the blue arrow). The plot is generated by summing the STRFdiff from all cells with any significant change. A relatively strong (blue) suppressed area emerges at the frequency of the reference tone, surrounded by two facilitated (red) sidebands. The right panel is the average plastic change in STRF as a function of log frequency away from the target frequency (centered at 0 and marked by the red arrow). Note that the disparity in unit numbers (127 vs 158) between the two panels, which reflects those cases (n = 19) in which multiple target tones were used. b, Distribution of target tone frequencies relative to the reference tone frequency (marked as 0 on the x-axis) used in all experiments with only a single target tone frequency (108 neurons). In this distribution, there were twice as many tests with targets below reference frequency than with targets above reference frequency. c, Left, Average STRF changes around the reference tone in experiments in which reference and target tones were far apart (fR - fT >= 1 octave). Right, Average STRF changes around reference tone frequency from experiments in which reference and target tone frequencies were relatively close (fR - fT < 1 octave). The depression around the reference tone frequency is significantly wider when the target frequency is farther away. The dashed lines are positioned 0.5 octaves above and below the reference frequency. d, Left, Average STRF changes around the reference tone frequency in experiments in which the reference tone frequency was below the target frequency. The excitatory sideband below the depression vanishes. Right, Average STRF changes from experiments in which target frequency was below reference frequency. In this case, as predicted, there is now an excitatory sideband below the depression centered at the reference frequency. This sideband now is stronger than the excitatory sideband above the reference frequency, which has decreased in amplitude but has not vanished.
- Figure 5.
STRF plasticity in a sequence of multiple tasks and behavioral contexts. a, A passive prebehavior STRF (first panel), followed by a discrimination STRF (second panel) in which changes at both target and reference frequencies occurred (ΔAref = -90%; ΔAtar = 62%). The STRF immediately recovered afterward (third panel). Another discrimination test (fourth panel) caused depressive and facilitative STRF changes (ΔAref = -68%; ΔAtar = 69%), which again reverted to the original passive STRF shape afterward. b, Three passive STRFs (first, third, fifth panels) interleaved with discrimination and detection tasks (second, fourth panels). In the two behavioral tasks, the 1 kHz tone played the role of reference tone (in the discrimination task) and target tone (in the detection task). The effect on the STRF was different depending on the behavioral context (as seen in the STRFdiff panels below). As a reference tone, the 1 kHz tone (blue arrow) induced a strong depression in the STRF (second panel). As a target tone (red arrow), it facilitated the STRF at 1 kHz (weakening inhibition at 1 kHz). c, Summary of results from performance of the detection task after a frequency discrimination task. Left, The average STRF facilitation induced by target tones during detection tasks, which followed discrimination tasks with the same tone as reference. Note that facilitation for the target frequency in a detection task with a previous discrimination task may be broader than in a single detection task because of the influence of persistent STRF plasticity to the target of the previous discrimination task. Right, The average STRF facilitation at target during a detection task, computed from our previously published single-unit data.
- Figure 6.
Plasticity and single-unit variability in multiunit STRFs. a, Example of plasticity in a behavioral STRF constructed from multiunit records. The three single units in the panels below were components of the multiunit cluster. The single-unit mean waveforms here (and in b) are clearly distinct, as shown by the nonoverlapping variance bars around each waveform (see Materials and Methods). Multiunit STRFs, The passive STRF (left) changed significantly during frequency discrimination behavior (ΔAref = -128%; ΔAtar = 69%; middle), and the change persisted afterward (right). Single-unit STRFs, STRF changes in three units. In each pair, the passive and behavior STRFs are shown, as well as the locations and type of significant plasticity that occurred in each. Details are the same as in Figure 2. Note that unit 2 in this figure was shown previously in Figure 2a. b, Same as in a above except that there were four single-unit STRFs that were isolated from the multiunit cluster. Multiunit STRFs, A strong depression was induced at the reference tone frequency during the discrimination task, but no significant effects were observed at the target tone frequency (middle). The multiunit STRF reverted to the original shape afterward (see postbehavior passive STRF in the right). Single-unit STRFs, STRF changes in four units that constitute the multiunit cluster. All details are as in a above. Note that the STRF changes are different in each of the four cells. In the first, no significant changes occurred. In unit 2, only facilitation at target frequency was seen. In the units 3 and 4, only depression at reference frequency occurred.
- Figure 7.
Summary of STRF changes from populations of single units and multiunit clusters. a, A comparison between STRF changes ΔAref in multiunit clusters versus single units. Each cluster may contain one to four isolated single units. Most points lie near the midline (solid line), indicating that the two changes are reasonably well matched [regression (dashed) line is also shown]. b, The average plasticity effects from all multiunit clusters during discrimination tasks is compared with the average multiunit plasticity effects observed in detection, from a behavioral sequence in which the tone detection task followed the frequency discrimination task. During performance of the discrimination task, a strong depression was induced relative to the reference frequency (left), whereas the opposite effect (facilitation) was seen relative to the target frequency (middle). In detection tasks after frequency discrimination tasks, the multiunit STRFs display a similar pattern of facilitation relative to the target frequency (right). Thus, the facilitatory effects at target frequency are consistent for both detect and discrimination tasks and also consistent for single-unit and multiunit averages (b) (see also Fig. 5c).
- Figure 8.
Examples of buildup in STRF plasticity and its relation to responses to reference tone. a, Snapshot sequence of STRFs for a multiunit cluster before (passive STRF) and during the behavior. STRF changes were already evident by the end of the second repetition of the stimulus set (4 min) and were essentially complete by the end of the fourth repetition (8 min). b, Reference tone response of the multiunit cluster decreased, reflecting the fading and downward shift of the excitatory region away from 3.2 kHz in the multiunit behavioral STRFs. The single-unit STRF shown previously (in Fig. 2b) was isolated from the multiunit cluster in this figure, and a marked inhibition at the reference frequency can be seen in its STRFdiff. c, Responses to the reference tones throughout the behavior. Data are accumulated from 12 multiunit clusters that exhibited the strongest suppressive STRF changes at reference tone frequencies. Progression of tone responses is indicated by the dashed lines.
