Echolocating Bats Have Evolved Decreased Susceptibility to Noise-Induced Temporary Hearing Losses

Abstract

Glenis Long championed the application of quantitative psychophysical methods to understand comparative hearing abilities across species. She contributed the first psychophysical studies of absolute and masked hearing sensitivities in an auditory specialist, the echolocating horseshoe bat. Her data demonstrated that this bat has hyperacute frequency discrimination in the 83-kHz range of its echolocation broadcast. This specialization facilitates the bat's use of Doppler shift compensation to separate echoes of fluttering insects from concurrent echoes of non-moving objects. In this review, we discuss another specialization for hearing in a species of echolocating bat that contributes to perception of echoes within a complex auditory scene. Psychophysical and behavioral studies with big brown bats show that exposures to long duration, intense wideband or narrowband ultrasonic noise do not induce significant increases in their thresholds to echoes and do not impair their ability to orient through a naturalistic sonar scene containing multiple distracting echoes. Thresholds of auditory brainstem responses also remain low after intense noise exposures. These data indicate that big brown bats are not susceptible to temporary threshold shifts as measured in comparable paradigms used with other mammals, at least within the range of stimulus parameters that have been tested so far. We hypothesize that echolocating bats have evolved a decreased susceptibility to noise-induced hearing losses as a specialization for echolocation in noisy environments.

Keywords: Animal psychophysics; Auditory brainstem response; Bats; Echolocation; Hearing loss; Temporary threshold shifts.

Fig. 1

The masked audiogram for the horseshoe bat (red curve, data from two bats) plots detection thresholds in dB SPL (re 20 µPa) for tones against wideband noise in the frequency range around the CF reference frequency (72–89 kHz). The sharp decrease in threshold around 83 kHz indicates a more acute ability to discriminate CF tones against noise within this narrow frequency range compared to lower or higher frequencies. The critical ratio function (blue curve, bandwidth derived from the dB difference between the spectral level of the noise and the masked threshold) parallels the masked audiogram. Smaller critical ratios around 83 kHz indicate greater frequency resolving power at the CF reference frequency. Replotted from [11, 16]

Fig. 2

Psychometric functions from one big brown bat tested before and after noise exposure. The x-axis shows successive trials (three days of testing in baseline, one day of testing in each of the exposure conditions). Thresholds were estimated using a two-alternative forced choice procedure with food reinforcement. The virtual echo was a FM sweep with the spectrum of the first harmonic of an echolocation broadcast. Its level (dB SPL rms, y-axis) decreased by 3 dB after successful detection, then increased by 1 dB after unsuccessful detection. In all plots, the green circles indicate correct detection and the gray triangles indicate incorrect detection. In the baseline condition (left plot), thresholds were tested against ambient noise. Shown are data from the last three days of testing. The bat’s threshold (dashed line) is estimated as 18 dB SPL, midway between correct and incorrect choices, averaged over three reversal points. Estimated thresholds in a sham exposure condition (middle plot, dashed lines) were 19 dB SPL at both 5 min and 24 h post-sham. In the noise exposure condition (right plot), bats were exposed to 60 min of NB noise (49–20 kHz) at a level of 116–119 dB SPL. At both 5 min and 24 h post-exposure, the bat’s threshold was about 16 dB SPL, a 3 dB decrease from baseline and sham exposure conditions (dashed lines). Bats sometimes declined to continue performing after a certain number of incorrect trials, so there are unequal numbers of reversal points in each psychometric function. Data replotted from [41]. We wish to acknowledge here Glenis’s repeated admonitions to us and to others of the importance of showing psychometric functions

Fig. 3

Summary of threshold data from six bats tested in six noise exposure conditions. Some bats were tested in more than one condition. Threshold shift from baseline is plotted along the y-axis. Positive values depict increases in threshold after noise exposure, and negative values depict decreases in threshold after noise exposure. The exposure condition is shown on the x-axis. Dark blue circles: NB2 = narrow band noise, measured 2 min post-exposure. Dark red triangles: NB5 = narrow band noise, measured 5 min post-exposure. NB noise spanned the frequency range of 10–50 kHz, 20–50 kHz, or 25–50 kHz in different experiments. Gray inverted triangles: WB20 = wide band noise, measured 20 min post-exposure. Brown squares: S2 = sham exposure, 2 min post-sham. Dark pink diamonds: S5 = sham exposure, 5 min post-sham. Green dotted hexs: S20 = sham exposure, 20 min post-sham. All threshold values are within 6 dB of baseline, indicating no significant effect of noise exposure. Data replotted from [40, 41]

Fig. 4

Left plot: Performance of four big brown bats (Bats A, B, C, and D) tested in a flight task in baseline conditions and after (20 min, 24 h) 60 min exposures to wideband (WB; 10–90 kHz) noise at 116 dB SPL. Performance is quantified as the proportion of unsuccessful flights in which the bat did not reach the end goal. Right plot: Performance after exposure to NB noise at a level of 123 dB SPL, assessed 2 min post-exposure, 24 h post-exposure, and after sham exposures. Data show mean proportion of unsuccessful flights after exposures to noise bandwidths of 5, 10, or 25 kHz (colored bars: 1, 2, or 3 exposures for each bat). Bats A, B, and C are the same as those whose data are shown in the left plot; Bat E was not tested previously. Bats overall showed poorer performance when tested 2 min compared to 20 min post-exposure, but with considerable individual variability between bats. Data replotted from [44, 45]