For seasonally breeding vertebrates, reproductive cycling is often coupled with changes in vocalizations that function in courtship and territoriality. Less is known about changes in auditory sensitivity to those vocalizations. Here, we show that nonreproductive female midshipman fish treated with either testosterone or 17beta-estradiol exhibit an increase in the degree of temporal encoding of the frequency content of male vocalizations by the inner ear that mimics the reproductive female's auditory phenotype. This sensory plasticity provides an adaptable mechanism that enhances coupling between sender and receiver in vocal communication.

Female midshipman fish (Porichthys notatus) use the auditory sense to detect and locate vocalizing males during the breeding season. Detection of conspecific vocal signals is essential to their reproductive success and can evoke strong phonotactic responses in gravid females but not in spent females that have released all of their eggs. Here, we test the hypothesis that seasonal variation in reproductive state affects the neurophysiological response properties of the peripheral auditory system in female midshipman fish. Iso-intensity responses of eighth nerve afferents from the sacculus, the main auditory end organ of the inner ear, to individual tones were measured for spike rate and vector strength (VS) of synchronization. Most auditory saccular units in reproductive, summer females showed robust temporal encoding up to 340 Hz, whereas nonreproductive winter females showed comparable encoding only up to 100 Hz. The dramatic upward shift in temporal encoding among summer fish was paralleled by increases in best frequency (BF), maximum evoked spike rate at BF, VS values at BF, and the percentage of units that showed significant VS to iso-intensity tones Ͼ140 Hz. Reproductive summer females were best suited to encode the higher harmonic components of male advertisement calls. This first demonstration of a natural cyclicity in peripheral auditory frequency sensitivity among vertebrates may represent, in this case, an adaptive plasticity of the female midshipman's auditory system to enhance the acquisition of auditory information needed for mate identification and localization during the breeding season.

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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.

This study examined the response properties of skate electrosensory primary afferent neurons of pre-hatch embryo (8-11 weeks), post-hatch juvenile (1-8 months), and adult (> 2 year) clearnose skates (Raja eglanteria) to determine whether encoding of electrosensory information changes with age, and if the electrosense is adapted to encode natural bioelectric stimuli across life history stages. During ontogeny, electrosensory primary afferents increase resting discharge rate, spike regularity, and sensitivity at best frequency. Best frequency was at 1-2 Hz for embryos, showed an upwards shift to 5 Hz in juveniles, and a downward shift to 2-3 HZ in adults. Encapsulated embryos exhibit ventilatory movements that are interrupted by a "freeze response" when presented with weak uniform fields at 0.5 and 1 Hz. This phasic electric stimulus contains spectral information found in potentials produced by natural fish predators, and therefore indicates that the embryo electrosense can efficiently mediate predator detection and avoidance. In contrast, reproductively active adult clearnose skates discharge their electric organs at rates near the peak frequency sensitivity of the adult electrosensory system, which; facilitates electric communication during social behavior. We suggest that life-history-dependent functions such as these may shape the evolution of the low-frequency response properties for the elasmobranch electrosensory system.