Neural and behavioral discrimination of sound duration by cats

Abstract

Sound duration is important for distinguishing auditory object. Previous studies on the neural representation of duration have usually lacked psychophysical data obtained from the same species; hence, the correspondence between neural and behavioral discrimination of duration remains obscure. We addressed this issue in cats by using the signal detection theory to investigate both neural activities in the primary auditory cortex (A1) and the cat's behavioral performance. We found that 320 ms duration can be well discriminated from 10 ms duration by some A1 neurons with specific response patterns: sustained response extended proportionally with the increase of stimulus duration and the On-Off response synchronizing stimulus onset and offset. Neurons with only On response cannot discriminate duration. The discrimination performance of both sustained and On-Off responses deteriorated as the target duration decreased from 320 to 20 ms and the percentage of discriminative neurons (correct rate >0.75) decreased from 40 to 2%. Compared with the psychophysical results, we found that the psychometric functions of cats well matched the neurometric functions of most sustained-response neurons and a small number of On-Off-response neurons. Pooling the spikes of multiple units improved neural discrimination, which may be attributable to the salience (noise reduction) of the responses in pooled data. Our results suggest that the sustained and Off responses of A1 neurons underlie the duration discrimination behavior of cats.

Figure 1.

Discharge patterns and duration tuning functions of the three representative units. A–C, Raster plots and mean PSTHs of 20 trials in response to tone bursts of different durations (10, 20, 40, 80, 160, and 320 ms). Shaded areas indicate stimulus duration. D–F, Mean driven rate as a function of stimulus duration. Dotted line shows the level of 2 SDs of the background firing rate.

Figure 2.

Results of ROC analysis in three representative units. A–C, ROC curves constructed from the two distributions of ED: the ED between two single-trial PSTHs, both from the standard duration (10 ms) group and the ED between two PSTHs of the standard and target duration (20, 40, 80, 160, or 320 ms), respectively. D–F, Neurometric functions constructed by plotting the area under the ROC curves shown in A–C against the target duration. Dotted line shows the level of 0.75. Time window used in ROC analysis is 0–400 ms after stimulus onset. G–I, Neurometric functions obtained from the time window of 0–50 ms. J–L, Neurometric functions obtained from the time window of 50–400 ms.

Figure 3.

Population properties of the three groups of A1 neurons. A–C, Mean PSTHs of sustained-, On–Off-, and On-response units, respectively. PSTHs of 10, 20, 40, 80, 160, and 320 ms are superimposed to show the effect of stimulus duration on each unit group. Shaded area shows SE. D–F, Mean duration tuning function averaged over each group. Shaded area shows SE. Dotted line is the mean level of 2 SDs of background firing. G–I, Mean neurometric function averaged over each group. Dots show SD. Horizontal line is the level of 0.75.

Figure 4.

Histograms showing the percentage of units achieving a discrimination performance higher than 0.75, when spike activities are used to discriminate 10 ms tones from 20, 40, 80, 160, and 320 ms tones, respectively.

Figure 5.

Behavioral performance of three cats during training sessions to discriminate 20–320 ms tones from 10 ms tones. Different marks represent different target durations. Horizontal line shows the criterion (d′ = 2) of behavioral performance. Vertical lines mark the session when the tone frequency was changed.

Figure 6.

Comparison of psychometric and neurometric functions. A–C, Area under the ROC was plotted against the duration of target tone, constructing the neurometric and psychometric functions. Gray lines show the individual neurometrics of sustained-response units. Circles and bars show the mean and SD of the psychometrics, respectively. D–F, Neurometrics of On–Off-response units are presented with the psychometrics. G–I, Neurometrics of On-response units are presented with the psychometrics.

Figure 7.

Effect of pooling sustained-response units. A, B, Raster plots and PSTHs of the spike data pooled by the 10 worst and best units, respectively. Same format as Figure 1. C, D, Asterisks represent the neurometric function obtained from the pooled data of the 10 worst and best units, respectively. Gray lines show the individual neurometrics of each unit. Circles represent the mean psychometric function.

Figure 8.

Effect of pooling On–Off-response units. Same format as Figure 7.

Figure 9.

Effect of pooling On-response units. Same format as Figure 7.