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The plainfin midshipman, Porichthys notatus, is a seasonally breeding vocal fish that relies on acoustic communication to mediate nocturnal reproductive behaviors. Reproductive females use their auditory senses to detect and localize “singing” males that produce multiharmonic advertisement (mate) calls during the breeding season. Previous work showed that the midshipman saccule, which is considered the primary end organ used for hearing in midshipman and most other fishes, exhibits reproductive state and hormone-dependent changes that enhance saccular auditory sensitivity. In contrast, the utricle was previously posited to serve primarily a vestibular function, but recent evidence in midshipman and related toadfish suggests that it may also serve an auditory function and aid in the detection of behaviorally relevant acoustic stimuli. Here, we characterized the auditory-evoked potentials recorded from utricular hair cells in reproductive and nonreproductive female midshipman in response to underwater sound to test the hypothesis that variation in reproductive state affects utricular auditory sensitivity. We show that utricular hair cells in reproductive females exhibit up to a sixfold increase in the utricular potential magnitude and have thresholds based on measures of particle acceleration (re: 1 ms −2 ) that are 7–10 dB lower than nonreproductive females across a broad range of frequencies, which include the dominant harmonics of male advertisement calls. This enhanced auditory sensitivity of the utricle likely plays an essential role in facilitating midshipman social and reproductive acoustic communication. NEW & NOTEWORTHY In many animals, vocal-acoustic communication is fundamental for facilitating social behaviors. For the vocal plainfin midshipman fish, the detection and localization of social acoustic signals are critical to the species’ reproductive success. Here, we show that the utricle, an inner ear end organ often thought to primarily serve a vestibular function, serves an auditory function that is seasonally plastic and modulated by the animal’s reproductive state effectively enhancing auditory sensitivity to courting male advertisement calls.
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This content will become publicly available on March 15, 2026
Reproductive state-dependent cell turnover in the inner ear of the plainfin midshipman fish ( Porichthys notatus )
ABSTRACT Plainfin midshipman fish (Porichthys notatus) exhibit seasonal auditory plasticity that enhances their reproductive success. During the summer, type I male midshipman acoustically court females and both the males and females exhibit increased auditory sensitivity during this period. The enhanced auditory sensitivity is associated with increased density of sensory hair cells in the saccule but not the utricle, suggesting that different mechanisms underlie physiological plasticity in distinct inner ear regions. To better understand how shifts in hair cell number occur within auditory tissues, we examined cell turnover across breeding states and sexes in midshipman fish. We found that reproductive type I males exhibited less saccular cell proliferation than non-reproductive males without a change in cell death, indicating a net loss of saccular cells during the breeding season. By contrast, saccular cell proliferation increased in summer females, with no seasonal changes in other inner ear epithelia. Collectively, our data reveal that multiple mechanisms are likely to contribute to seasonal auditory plasticity within a single species, potentially within the ear of an individual animal.
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- Award ID(s):
- 1933166
- PAR ID:
- 10590455
- Publisher / Repository:
- Company of Biologists
- Date Published:
- Journal Name:
- Journal of Experimental Biology
- Volume:
- 228
- Issue:
- 6
- ISSN:
- 0022-0949
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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