Correlations between cochlear pathophysiology and behavioral measures of temporal and spatial processing in noise exposed macaques

Abstract

Noise-induced hearing loss (NIHL) is known to have significant consequences for temporal, spectral, and spatial resolution. However, much remains to be discovered about their underlying pathophysiology. This report extends the recent development of a nonhuman primate model of NIHL to explore its consequences for hearing in noisy environments, and its correlations with the underlying cochlear pathology. Ten macaques (seven with normal-hearing, three with NIHL) were used in studies of masked tone detection in which the temporal or spatial properties of the masker were varied to assess metrics of temporal and spatial processing. Normal-hearing (NH) macaques showed lower tone detection thresholds for sinusoidally amplitude modulated (SAM) broadband noise maskers relative to unmodulated maskers (modulation masking release, MMR). Tone detection thresholds were lowest at low noise modulation frequencies, and increased as modulation frequency increased, until they matched threshold in unmodulated noise. NH macaques also showed lower tone detection thresholds for spatially separated tone and noise relative to co-localized tone and noise (spatial release from masking, SRM). Noise exposure caused permanent threshold shifts that were verified behaviorally and audiologically. In hearing-impaired (HI) macaques, MMR was reduced at tone frequencies above that of the noise exposure. HI macaques also showed degraded SRM, with no SRM observed across all tested tone frequencies. Deficits in MMR correlated with audiometric threshold changes, outer hair cell loss, and synapse loss, while the differences in SRM did not correlate with audiometric changes, or any measure of cochlear pathophysiology. This difference in anatomical-behavioral correlations suggests that while many behavioral deficits may arise from cochlear pathology, only some are predictable from the frequency place of damage in the cochlea.

Keywords: Modulation masking release; Noise exposure; Nonhuman primate; Sensorineural hearing loss; Spatial release from masking.

FIGURE 1 –

Modulation masking release (MMR) in normal-hearing macaques (Color available online). A. Exemplar psychometric functions showing probability correct as a function of tone level for Monkey D, detecting 1 kHz tones embedded in noise that was unmodulated (triangles), or amplitude modulated at 10 (◊), 40 (○) or 150 Hz (□). B. An example of detection threshold (pc=0.76) as a function of noise modulation frequency, fit with a Weibull function to extract metrics of MMR: MMR threshold (arrow) and amplitude (solid vertical line). C. MMR thresholds of each monkey, at each tone frequency tested. D. MMR amplitudes for each monkey, at each tone frequency tested. MMR previously published in Dylla et al. (2013), estimated by threshold shift in 10 Hz AM noise relative to unmodulated noise shown inset, in grey.

FIGURE 2 –

Spatial release of masking (SRM) in normal-hearing macaques (Color available online). A. Exemplar psychometric functions showing SRM, the difference between thresholds (pc=0.76) when the noise masker was at 45° (◊) or 90° (∆) and 0° (○) along the azimuthal plane. B. SRM at 45° for each monkey at each tone frequency measured. C. SRM at 90° for each monkey at each tone frequency measured.

FIGURE 3 –

Audiometric shift after noise exposure. (Color available online). Audiograms for monkeys L (□), E (○), and G (∆) pre-exposure (black) and post-noise exposure (red). A. Initial audiometric shift measured at 5 weeks post noise exposure for each monkey. B. Secondary audiometric shift measured at time-points after MMR and SRM data collection for Monkeys L and E, but near MMR collection for Monkey G.

FIGURE 4 –

MMR in noise-exposed macaques (Color available online). A. Exemplar psychometric functions showing probability correct as a function of tone level for Monkey L, detecting 4 kHz tones embedded in noise, amplitude modulated at 10 (◊), 40 (○) or 150 Hz (□). B. Examples of the lack of MMR at any noise modulation frequency at frequencies showing pronounced cochlear damage in monkey E (○) and monkey L (□), where MMR threshold was taken to be 10 Hz, the lowest modulation frequency tested, and MMR amplitude was zero. C. MMR threshold in noise exposed macaques, compared to a group of non-noise-exposed monkeys (◊). D. MMR amplitude in noise-exposed macaques, compared to unexposed monkeys. MMR previously published in Dylla et al. (2013), estimated by threshold shift in 10 Hz AM noise relative to unmodulated noise shown inset, in grey. Conventions follow legend in part C. The format is similar to Figure 1.

FIGURE 5 –

Spatial release of masking in noise-exposed macaques (Color available online.) A. Exemplar psychometric functions showing lack of SRM when the noise masker was at 45° (◊) or 90° (∆) and 0° (○) along the azimuthal plane. B, C. SRM at 45° and 90° for each monkey at each tone frequency measured, compared to unexposed monkeys (◊).

FIGURE 6 –

Correlation of MMR and SRM with audiometric shift. A. Between group difference in MMR threshold as a function of change in audiometric threshold for the noise exposed monkeys G (∆), E (○), and L (□). The dashed line represents the best fitting exponential function, with significance determined by non-linear regression. B. Modulation masking release amplitude as a function of audiometric shift. Symbols and lines follow the conventions in panel A. C. Maximum spatial release from masking as a function of audiometric shift. The dashed line represents the best fitting line. Symbols follow conventions in A.

FIGURE 7 –

Histopathological effects of noise exposure (Color available online). A. Inner hair cell survival as a function of frequency place in the cochlea for monkeys L (□), E (○) and G (∆). The grey box represents the frequency band of the noise exposure. B and C are similar to panel A, but for outer hair cells (B) and cochlear ribbon synapses (C).

FIGURE 8 –

Correlation of modulation masking release with histological changes. (Color available online). A. Between group differences in MMR threshold as a function of outer hair cell survival. B. Between group differences in MMR threshold as a function of ribbons synapse survival. C. MMR amplitude as a function of OHC survival. D. MMR amplitude as a function of ribbon synapse survival. The dashed lines represent the best fitting line as assessed by linear or non-linear regression. Symbols follow conventions in Figure 7. The percentage survival exceeded 100 in some cases due to variability in the mean numbers of ribbon synapses per inner hair cell in control animals.

FIGURE 9 –

Correlation of spatial release of masking with histological changes. (Color available online). A. Maximal SRM (90°) as a function of outer hair cell survival for the three noise-exposed monkeys. B. Maximal SRM as a function of ribbon synapse survival. Symbols and lines follow conventions in Figures 7 and 8.