Seasonal Plasticity of Peripheral Auditory Frequency Sensitivity

Abstract

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.

Seasonal plasticity of auditory saccular sensitivity in “sneaker” type II male plainfin midshipman fish, Porichthys notatus

“…This SPL level was chosen for calibration because 130 dB SPL is well above the noise floor for our measurement devices, and it is consistent with sound levels for type I male midshipman calls within and near their nests in the field and therefore within the range of stimulus amplitudes tested here (Bass and Clark 2003). The frequency stimuli used in this study were based on that used in previous studies (Sisneros and Bass 2003;Sisneros 2007Sisneros , 2009bRohmann and Bass 2011). The intentional of this study was to compare the saccular sensitivity of type II male P. notatus across season (non-reproductive vs. reproductive state) and compare the saccular sensitivity with that of females (Sisneros 2009b) and type I males (Rohmann and Bass 2011) under similar experimental conditions.…”

“…This increase in type II A. A. Bhandiwad and E. A. Whitchurch contributed equally. Previous studies have shown that both the female and type I male auditory systems are seasonally adapted to detect the broadband agonistic calls and the dominant harmonic components of the advertisement calls produced by type I males during the breeding season (Sisneros and Bass 2003;Rohmann and Bass 2011). These adaptations are potentially important for conspecific detection and localization, mate choice decisions and intraspecific male competition (Sisneros 2009a, b).…”

“…Instead, type II males, which have neuroendocrine traits similar to that of females, engage in satellite or sneak-spawning to steal fertilizations from type I males that are actively courting females in the nest (Brantley and Bass 1994). While females and type I males are known to be better suited to detect midshipman vocalizations during the breeding season (Sisneros and Bass 2003;Sisneros 2009b;Rohmann and Bass 2011), the auditory sensitivity of sneaker type II males has yet to be characterized. There is no a priori reason to expect that seasonal plasticity of midshipman auditory sensitivity would be limited to females and type I males.…”

Seasonal plasticity of auditory hair cell frequency sensitivity correlates with plasma steroid levels in vocal fish

“…We have investigated peripheral auditory plasticity in a teleost fish, the plainfin midshipman (Porichthys notatus Girard 1854; family Batrachoididae), that shows seasonal, reproductive state-dependent plasticity in the ability to encode the upper harmonics of vocalizations (Fig.1A,B). As females shift from a non-reproductive to a reproductive state, they exhibit a steroid-dependent improvement in frequency encoding by eighth nerve afferents to the saccule (Sisneros and Bass, 2003;Sisneros et al, 2004a), the main auditory division of the inner ear in midshipman and most teleosts (Fig.1C insert) (McKibben and Bass, 1999;Popper and Fay, 1993). We tested the hypothesis that this plasticity is not sex dependent, with males also exhibiting concurrent shifts in plasma steroid levels and auditory encoding as reflected in frequency sensitivity of the hair cell epithelium of the saccule.…”

“…The study reported here is one of a series of midshipman fish studies investigating yearly events as animals transitional between non-reproductive and reproductive states (Sisneros, 2009;Sisneros and Bass, 2003;Sisneros et al, 2004a). So far, this work has focused on females because early behavioral studies showed females exhibiting robust and consistent positive phonotaxis to playbacks mimicking male advertisement 'hums' (Fig.1A) that females use to localize nesting males (Brantley and Bass, 1994;McKibben and Bass, 1998;McKibben and Bass, 2001).…”