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. 2009 Mar;10(1):5-22.
doi: 10.1007/s10162-008-0142-y. Epub 2008 Oct 15.

Encoding intensity in ventral cochlear nucleus following acoustic trauma: implications for loudness recruitment

Shanqing Cai  1 , Wei-Li D Ma, Eric D Young
Affiliations

Encoding intensity in ventral cochlear nucleus following acoustic trauma: implications for loudness recruitment

Shanqing Cai et al. J Assoc Res Otolaryngol. 2009 Mar.

Abstract

Loudness recruitment, an abnormally rapid growth of perceived loudness with sound level, is a common symptom of sensorineural hearing loss. Following acoustic trauma, auditory-nerve rate responses are reduced, and rate grows more slowly with sound level, which seems inconsistent with recruitment (Heinz et al., J. Assoc. Res. Otolaryngol. 6:91-105, 2005). However, rate-level functions (RLFs) in the central nervous system may increase in either slope or saturation value following trauma (e.g., Salvi et al., Hear. Res. 147:261-274, 2000), suggesting that recruitment may arise from central changes. In this paper, we studied RLFs of neurons in ventral cochlear nucleus (VCN) of the cat after acoustic trauma. Trauma did not change the general properties of VCN neurons, and the usual VCN functional classifications remained valid (chopper, primary-like, onset, etc.). After trauma, non-primary-like neurons, most noticeably choppers, exhibited elevated maximum discharge rates and steeper RLFs for frequencies at and near best frequency (BF). Primary-like neurons showed the opposite changes. To relate the neurons' responses to recruitment, rate-balance functions were computed; these show the sound level required to give equal rates in a normal and a traumatized ear and are analogous to loudness balance functions that show the sound levels giving equal perceptual loudness in the two ears of a monaurally hearing-impaired person. The rate-balance functions showed recruitment-like steepening of their slopes in non-primary-like neurons in all conditions. However, primary-like neurons showed recruitment-like behavior only when rates were summated across neurons of all BFs. These results suggest that the non-primary-like, especially chopper, neurons may be the most peripheral site of the physiological changes in the brain that underlie recruitment.

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Figures

FIG. 1
FIG. 1
CAP audiograms in the normal and noise-exposed experiments. A The light lines show CAP audiograms from individual experiments, and the heavy lines are averages for the normal (dashed lines) and exposed (solid lines) animals. The vertical bar shows the frequency of the noise exposure. B CAP audiograms from individual experiments shifted to align their edge frequencies with the geometric mean value (11.3 kHz). Audiograms from normal animals are also aligned at 11.3 kHz.
FIG. 2
FIG. 2
Thresholds at BF of neurons of various response types plotted against BF relative to the edge of the CAP audiogram. The thresholds are presented as dB relative to the thresholds in the average CAP audiogram of the normal group (Fig. 1). Symbols identify neuron types; these are the same as in subsequent figures. Filled symbols are from exposed animals, and unfilled symbols are from normal animals.
FIG. 3
FIG. 3
Q10 values of VCN neurons are similar to those of AN fibers in both normal and noise-exposed ears. A A summary of tuning-curve Q10s of neurons in the normal (unfilled symbols) and noise-exposed (filled symbols) populations. The gray bar indicates the frequency of the exposure noise. The upper and lower limits (5% and 95% quantiles) of Q10s of normal AN fibers from Miller et al. (1997) and Ji (2000) are overlaid for comparison (dashed lines). The solid line shows the moving average of Q10 versus BF for the control group. B Relative Q10 (normalized by the average Q10 at the same BF in the normal-hearing population) versus threshold relative to the average normal CAP audiogram (Fig. 1). The horizontal dashed line indicates the average normal Q10 values. The horizontal dash-dotted line (at 0.55) is the boundary between sharp and broad tuning used by Heinz and Young (2004), chosen to be the fifth percentile of Q10s in normal AN fibers. The ellipse shows the region occupied by AN fibers with moderate to severe loss from Figure 5 of Heinz and Young for comparison. The ellipse was shifted along the abscissa by 28 dB to account for the difference between the mean CAP threshold at 2 kHz (23.5 dB SPL) and the threshold reference used by Heinz and Young at 2 kHz (−4.5 dB SPL).
FIG. 4
FIG. 4
Primary-like neurons show a decrease in rate responses following AT. RLFs from Pri and PriN neurons are shown. Data in normal and exposed animals are identified by line style, defined in the caption. A BF-tone RLFs as driven rate (rate–SR). B Average firing rate versus level re threshold. The individual RLFs in A were aligned at their thresholds (vertical line) and averaged. The circles and error bars show mean ± 1 SE of rates at 30 dB re threshold.
FIG. 5
FIG. 5
Chopper neurons show an increase in rate response after AT. RLFs for BF tones in chopper neurons arranged as in Figure 4.
FIG. 6
FIG. 6
Spread of excitation is larger following AT. A Equal-level rate contours for the tonal pseudopopulation in normal animals. The rates are average normalized driven firing rates of all VCN response types, computed in 0.4 octave frequency bins, as described in the text. The numbers show sound levels in dBP. The heavy gray line shows the 60 dB SPL contour for AN fibers from Heinz et al. (2005), Figure 4, normalized in the same way. This level was chosen for comparison because it shows a clear shift in the BF at which the peak rate occurs. B Same for the exposed preparations. The heavy gray lines show 80 and 90 dB contours for AN fibers in preparations with “mild” and “moderate” hearing loss, as defined in Heinz et al. (2005). Locker neurons are not included in this figure because their BFs are far from those of other neuron types.
FIG. 7
FIG. 7
Rate-balance functions from Ch, but not PL neurons resemble perceptual loudness-balance functions. In each section, the left plot shows the average rate for normal (dashed lines) and exposed (solid lines) pseudopopulations consisting of (1) neurons with BFs within ±0.2 octaves of the tone frequency (On-BF), shown with shaded bootstrap confidence limits (±1 SD), and (2) neurons of all BFs, shown as the average rate lines only. The circles on the on-BF functions show the thresholds (3 spikes/s). The right plots show the sound levels that give the same rates in the normal and exposed populations. Matches are shown for the on-BF and all-BF populations, identified by line shading, as in the legend in A. The numbers are the slopes of best-fitting lines for the rate matches over the range of sound levels shown. The dashed lines show predictions for typical recruitment functions in human observers (see text). A AN data from Heinz et al. (2005), reanalyzed with the pseudopopulation method. Rate-matching lines and slopes are shown for both pseudopopulation analysis (slopes, 0.54 and 1.46) and from the previous real-population analysis done by Heinz and colleagues (slopes, 0.56 and 1.20). B, C Average RLFs and the corresponding rate-matching curves for PL and chopper neurons.
FIG. 8
FIG. 8
The slopes of rate-matching functions change with the averaging bandwidth for AN fibers and PL neurons, but not Ch neurons. Slopes of rate-matching functions are shown for tonal pseudopopulations as a function of the range of BFs (relative to the tone frequency) averaged together. Results are given as mean ± 1 SD of 500 bootstrap repetitions of the calculation for the same three populations as in Figure 7, identified in the legends. The shaded band shows the range of slopes of loudness-matching curves in human subjects (publications cited in the text) with hearing losses comparable to those of the exposed cats. The AN fiber data are from a reanalysis using pseudopopulations of the data of Heinz et al. (2005).
FIG. 9
FIG. 9
Rate-matching slopes for responses to BBN; these differ between PL and non-PL neurons as for the tone responses. The figure is drawn as in Figure 7, except that the recruitment prediction line is not shown because of uncertainty as to how recruitment should behave for BBN. Neurons are grouped into PL and non-PL pseudopopulations, and the plots show average RLFs (left) and rate-matching curves (right).
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