Enhanced temporal response properties of anteroventral cochlear nucleus neurons to broadband noise

Abstract

Compared with auditory nerve (AN) fibers, trapezoid body (TB) fibers of the cat show enhanced synchronization to low-frequency tones. This phenomenon probably contributes to the high temporal resolution of binaural processing. We examined whether enhanced synchronization also occurs to sustained broadband noise. We recorded responses to a reference Gaussian noise and its polarity-inverted version in the TB of barbiturate-anesthetized cats. From these we constructed shuffled autocorrelograms (SACs) and quantified spike timing by measuring the amplitude and width of their central peak. Many TB fibers with low characteristic frequency (CF) showed SACs with higher and narrower central peaks than ever observed in the AN, indicating better consistency and precision of temporal coding. Larger peaks were also observed in TB fibers with high CF, but this was mostly caused by higher average firing rates, resulting in a larger number of coincident spikes across stimulus repetitions. The results document monaural preprocessing of the temporal information delivered to binaural nuclei in the olivary complex, which likely contributes to the high sensitivity to interaural time differences.

Figure 1.

Dot rasters of responses to pure tones at the CF (A, C) and to broadband noise (B, D) for a PHL trapezoid body fiber (top) and an AN fiber (bottom). CF, threshold, and SR were 350 Hz, 23 dB SPL, and 90 spikes/s (top) and 379 Hz, 39 dB SPL, and 57 spikes/s (bottom). Sound levels (dB SPL) were 40 (A), 60 (B), 60 (C), and 80 (D).

Figure 2.

Dot rasters of broadband noise responses from a PL_N (top row) and an AN (bottom row) fiber. CFs and SR were 7600 Hz and 27 spikes/s for the PL_N fiber and 7300 Hz and 10 spikes/s for the AN fiber. The sound level was 50 dB SPL in both cases.

Figure 3.

Examples of SACs of responses to broadband noise from four AN fibers (left column) and 12 TB fibers. All abscissas have the same scale. For each row, ordinate scales in the left column apply to all other columns. In all cases, the stimulus level was ∼50 dB SPL. The CF, fiber type, SR, average firing rate (in spikes/s), and CR_max (coincidences/s) are indicated in the left top corner of each panel.

Figure 4.

Effects of SPL on normalized SACs obtained from responses to broadband noise of six TB fibers. Top row shows low-CF, and the bottom row shows high-CF fibers. The abscissas of all panels are on the same scale. For each row, the ordinate scale in the left column applies to all other columns, but note that it differs between the top and bottom rows. CF, fiber type, SR, and SPL are indicated in each panel.

Figure 5.

Influence of SPL on correlation index (top row) and halfwidth (bottom row) of the central peak of SACs, for low-CF PHL fibers (left column) and high-CF PL_N fibers (right column). Each line represents a single fiber. In each column, the corresponding symbols of the top and bottom rows represent the same fiber. CFs (in Hertz) are indicated in the top right corners of the top panels.

Figure 7.

CF dependence of halfwidth of SACs to noise obtained from a population of low-CF TB and AN fibers. Data from single fibers at multiple SPLs are connected by a vertical line. The thick solid lines indicate the range of halfwidth values obtained from 99 AN fibers. Symbols are the same as those shown for Figure 6.

Figure 12.

Halfwidths (A) and modulation depths (B) of SACs from envelope-dominated responses obtained at 40-60 dB SPL. The dashed lines indicate the extreme values obtained for AN fibers.

Figure 6.

CR_max (A), correlation index (B), and maximal average firing rate (C) for responses to noise, plotted versus CF for a population of 340 TB fibers pooled from 16 cats. Each vertical line connecting two or more data points represents data from a single fiber at multiple SPLs. The thick solid line in each panel indicates the top limit of values from a population of 360 AN fibers.

Figure 8.

A-C, Amplitude spectra (10.log₁₀) of SACs of a low-, mid-, and high-CF TB fiber. The asterisk indicates the DF or spectral maximum. D, DF of SACs versus CF. The oblique solid line graphs equality. Each vertical line connects data from single fibers at multiple SPLs.

Figure 9.

A-C, G-I, Examples of SACs (thick lines) and normalized XACs (thin lines) for two AN fibers (left column) and four TB fibers (middle and right column). D-F, J-L, Difcors obtained by subtraction of XACs from SACs. The abscissas of all panels are on the same scale. Ordinate scales in the left column apply to all other columns, but differ between rows. The stimulus level for all fibers was ∼50 dB SPL. CF, fiber type, and SR are as indicated.

Figure 10.

CF dependence of difcor peak heights for TB and AN fibers. The broadband noise was presented at 50-90 dB SPL for both TB and AN fibers. The thick solid lines illustrate the range of values for a population of AN fibers.

Figure 11.

Ratio of the value at delay 0 of XAC and SAC for a population of 238 TB fibers. The thick solid lines show the range of values for a population of AN fibers. The dashed horizontal line at 0.9 indicates our criterion for responses dominated by envelope. Symbols are the same as those shown for Figure 6.

Figure 13.

A, CI obtained from responses to broadband noise versus vector strength (R) obtained from responses to short tone bursts at CF. When responses were obtained at more than one SPL, we chose the maximum CI and R. Each data point represents the two metrics from a single AN or TB fiber. B, CI from responses to broadband noise versus SR. C, CR_max obtained from the same responses as in A. D, CR_max from responses to broadband noise versus SR. Each asterisk represents a PHL fiber for which responses to CF tones were available. When the tonal responses yielded a vector strength (R) of >0.9, the asterisk is encircled.

Figure 14.

Halfwidth of SACs obtained from responses of PHL fibers to broadband noise. The solid lines indicate the range of values of halfwidths obtained from 99 AN fibers.