Seasonal plasticity of auditory saccular sensitivity in the vocal plainfin midshipman fish, Porichthys notatus

Abstract

The plainfin midshipman fish, Porichthys notatus, is a seasonally breeding species of marine teleost fish that generates acoustic signals for intraspecific social and reproductive-related communication. Female midshipman use the inner ear saccule as the main acoustic endorgan for hearing to detect and locate vocalizing males that produce multiharmonic advertisement calls during the breeding season. Previous work showed that the frequency sensitivity of midshipman auditory saccular afferents changed seasonally with female reproductive state such that summer reproductive females became better suited than winter nonreproductive females to encode the dominant higher harmonics of the male advertisement calls. The focus of this study was to test the hypothesis that seasonal reproductive-dependent changes in saccular afferent tuning is paralleled by similar changes in saccular sensitivity at the level of the hair-cell receptor. Here, I examined the evoked response properties of midshipman saccular hair cells from winter nonreproductive and summer reproductive females to determine if reproductive state affects the frequency response and threshold of the saccule to behaviorally relevant single tone stimuli. Saccular potentials were recorded from populations of hair cells in vivo while sound was presented by an underwater speaker. Results indicate that saccular hair cells from reproductive females had thresholds that were approximately 8 to 13 dB lower than nonreproductive females across a broad range of frequencies that included the dominant higher harmonic components and the fundamental frequency of the male's advertisement call. These seasonal-reproductive-dependent changes in thresholds varied differentially across the three (rostral, middle, and caudal) regions of the saccule. Such reproductive-dependent changes in saccule sensitivity may represent an adaptive plasticity of the midshipman auditory sense to enhance mate detection, recognition, and localization during the breeding season.