Relationship between auditory thresholds, central spontaneous activity, and hair cell loss after acoustic trauma

Abstract

Acoustic trauma caused by exposure to a very loud sound increases spontaneous activity in central auditory structures such as the inferior colliculus. This hyperactivity has been suggested as a neural substrate for tinnitus, a phantom hearing sensation. In previous studies we have described a tentative link between the frequency region of hearing impairment and the corresponding tonotopic regions in the inferior colliculus showing hyperactivity. In this study we further investigated the relationship between cochlear compound action potential threshold loss, cochlear outer and inner hair cell loss, and central hyperactivity in inferior colliculus of guinea pigs. Two weeks after a 10-kHz pure tone acoustic trauma, a tight relationship was demonstrated between the frequency region of compound action potential threshold loss and frequency regions in the inferior colliculus showing hyperactivity. Extending the duration of the acoustic trauma from 1 to 2 hours did not result in significant increases in final cochlear threshold loss, but did result in a further increase of spontaneous firing rates in the inferior colliculus. Interestingly, hair cell loss was not present in the frequency regions where elevated cochlear thresholds and central hyperactivity were measured, suggesting that subtle changes in hair cell or primary afferent neural function are sufficient for central hyperactivity to be triggered and maintained.

Figure 1

Illustration of effects of conversion from audiovisually estimated CF into nominal CF. A: scatterplot of the relationship between depth from cortical surface and audiovisual CF of all neurons from one control animal and the fitted polynomial function. B: scatterplot of relationship between depth from cortical surface and audiovisual CF of all neurons from a 2 week acoustic trauma animal and the fitted polynomial function based on neurons with an audiovisual CF in the normal hearing regions (according to CAP). C: illustration of the effect of transforming audiovisual CF into nominal CF. of the animal shown in B. Line indicates 1:1 ratio.

Figure 2

A,B: CAP thresholds at different frequencies recorded from the left cochlea before acoustic trauma (black circles), immediately after acoustic trauma (open triangles) and after a 2 week recovery period after acoustic trauma (black triangles), as well as from the right cochlea after recovery (open circles). A, 1 h acoustic trauma. B, 2 h acoustic trauma. C: CAP threshold losses recorded from the left cochlea at different frequencies two weeks after 1 h (black circles) and 2 h (open circles) of acoustic trauma. D: CAP thresholds at different frequencies recorded from the left cochlea of sham animals during initial surgery (black circles) and after a 2 week recovery period (black triangles), as well as from the right cochlea after recovery (open circles). Data points ± SEM. n=4 for all groups. * p<0.05; ** p<0.01; # p<0.001 statistical significance as compared to before trauma data. Grey line in A–C indicates exposure frequency.

Figure 3

Mean spontaneous firing rate of all CNIC neurons recorded in each group. Asterisks without bar indicate significance from shams. ** p<0.01; *** p<0.001.

Figure 4

Mean spontaneous activity of single neurons in different frequency regions in the CNIC in sham animals (grey bars) and animals after 2 weeks recovery from 1 (white bars) or 2 h acoustic trauma (black bars). The number of recorded neurons in each frequency region is indicated above the bars. Bars show mean spontaneous firing rates ± SEM. * P < 0.05; ** p<0.01; # p<0.001.

Figure 5

Illustration of relationship between CF and spontaneous firing rates of CNIC neurons in all 2 hr acoustic trauma animals and the CAP threshold loss at different frequencies. A: scatterplot of individual neurons and CAP threshold loss (mean ± SEM). B: Mean spontaneous activity of single neurons in different frequency regions (2 kHz bins) in CNIC. Bars show mean spontaneous firing rates ± SEM. C and D: 11 (C) and 31 (D) point running average of spontaneous firing rate and CAP threshold loss (mean ± SEM).

Figure 6

Relationship between the distribution of spontaneous firing rates of CNIC neurons and CAP threshold loss according to frequency. A, 1 h acoustic trauma group, acute threshold loss. B, 2 h acoustic trauma group, acute threshold loss. C, 1 h acoustic trauma group, permanent threshold loss. B, 2 h acoustic trauma group, permanent threshold loss. n = 4 in all panels. CAP threshold loss shown ± SEM. Spontaneous firing rate shown a 28 point running average. Grey line indicates exposure frequency.

Figure 7

cochleograms showing missing inner (dark line) and outer hair cells (dotted, medium and thin black lines) along the tonotopic axis of the cochlea after 1 h (A) and 2 h (B) of acoustic trauma in combination with the mean CAP threshold loss in both groups. All data n=4. Grey line indicates exposure frequency.