Abstract
BackgroundMammalian and avian auditory hair cells display tonotopic mapping of frequency along the length of the cochlea and basilar papilla. It is not known whether the auditory hair cells of fishes possess a similar tonotopic organization in the saccule, which is thought to be the primary auditory receptor in teleosts. To investigate this question, we determined the location of hair cell damage in the saccules of goldfish (Carassius auratus) following exposure to specific frequencies. Subjects were divided into six groups of six fish each (five treatment groups plus control). The treatment groups were each exposed to one of five tones: 100, 400, 800, 2000, and 4000 Hz at 176 dB re 1 μPa root mean squared (RMS) for 48 hours. The saccules of each fish were dissected and labeled with phalloidin in order to visualize hair cell bundles. The hair cell bundles were counted at 19 specific locations in each saccule to determine the extent and location of hair cell damage. In addition to quantification of anatomical injury, hearing tests (using auditory evoked potentials) were performed on each fish immediately following sound exposure. Threshold shifts were calculated by subtracting control thresholds from post-sound exposure thresholds.ResultsAll sound-exposed fish exhibited significant hair cell and hearing loss following sound exposure. The location of hair cell loss varied along the length of the saccule in a graded manner with the frequency of sound exposure, with lower and higher frequencies damaging the more caudal and rostral regions of the saccule, respectively. Similarly, fish exposed to lower frequency tones exhibited greater threshold shifts at lower frequencies, while high-frequency tone exposure led to hearing loss at higher frequencies. In general, both hair cell and hearing loss declined as a function of increasing frequency of exposure tone, and there was a significant linear relationship between hair cell loss and hearing loss.ConclusionsThe pattern of hair cell loss as a function of exposure tone frequency and saccular rostral-caudal location is similar to the pattern of hearing loss as a function of exposure tone frequency and hearing threshold frequency. This data suggest that the frequency analysis ability of goldfish is at least partially driven by peripheral tonotopy in the saccule.
Highlights
Mammalian and avian auditory hair cells display tonotopic mapping of frequency along the length of the cochlea and basilar papilla
The temporal theory argues that the perception of pitch depends upon the temporal patterns with which auditory neurons respond to sound, since waveforms of stimuli are well represented by patterns of phase-locking in the auditory nerve [5]
In order to better understand the role of peripheral processes involved in frequency discrimination in fishes, we examined the tonotopic pattern of saccular hair cell damage in response to tone exposures in goldfish (Carassius auratus)
Summary
Mammalian and avian auditory hair cells display tonotopic mapping of frequency along the length of the cochlea and basilar papilla. Frequency discrimination in fishes has been established from pyschophysical studies of a limited number of species [1], but has been of great theoretical interest since the early fish hearing experiments of von Frisch [2] The reason for this interest is that the otolith organs of fishes lack obvious macromechanical frequency selective processes such as those found in the basilar membrane of the mammalian cochlea [3]. The temporal theory argues that the perception of pitch depends upon the temporal patterns with which auditory neurons respond to sound, since waveforms of stimuli are well represented by patterns of phase-locking in the auditory nerve [5] In reality, both place and temporal cues may be processed differentially at various levels of the auditory system as the information passes from the sensory epithelia of the ear to the auditory nuclei of the brainstem, and on to the midand forebrain. It is currently unknown whether frequency discrimination in fishes is largely due to peripheral processes (hair cells and their associated primary afferent neurons) or central processes (e.g., brainstem and midbrain auditory nuclei)
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