Testosterone Treatment Mimics Seasonal Downregulation of Dopamine Innervation in the Auditory System of Female Midshipman Fish

Abstract

In seasonally breeding vertebrates, hormones coordinate changes in nervous system structure and function to facilitate reproductive readiness and success. Steroid hormones often exert their effects indirectly via regulation of neuromodulators, which in turn can coordinate the modulation of sensory input with appropriate motor output. Female plainfin midshipman fish (Porichthys notatus) undergo increased peripheral auditory sensitivity in time for the summer breeding season, improving their ability to detect mates, which is regulated by steroid hormones. Reproductive females also show differences in catecholaminergic innervation of auditory circuitry compared to winter, non-reproductive females as measured by tyrosine hydroxylase (TH), the rate-limiting enzyme in catecholaminergic synthesis. Importantly, catecholaminergic input to the inner ear from a dopaminergic-specific forebrain nucleus is decreased in the summer and dopamine inhibits the sensitivity of the inner ear, suggesting that gonadal steroids may alter auditory sensitivity by regulating dopamine innervation. In this study, we gonadectomized non-reproductive females, implanted them with estradiol (E2) or testosterone (T), and measured TH immunoreactive (-ir) fibers in auditory nuclei where catecholaminergic innervation was previously shown to be seasonally plastic. We found that treatment with T, but not E2, reduced TH-ir innervation in the auditory hindbrain. T-treatment also reduced TH-ir fiber density in the forebrain dopaminergic cell group that projects to the inner ear, and likely to the auditory hindbrain. Higher T plasma in the treatment group was correlated with reduced-ir TH terminals in the inner ear. These T-treatment induced changes in TH-ir fibers mimic the seasonal downregulation of dopamine in the midshipman inner ear and provide evidence that steroid hormone regulation of peripheral auditory sensitivity is mediated by dopamine.

Functional plasticity of the swim bladder as an acoustic organ for communication in a vocal fish

“…Furthermore, reproductive state-dependent differences in the highest detectable frequency was observed, with reproductive males exhibiting greater frequency bandwidth sensitivity than non-reproductive males at frequencies ranging from 665-950 Hz (figure 2g). Given the observed seasonal differences (figure 2) and that multiple mechanisms have been shown to result in reproductive state-dependent differences in midshipman auditory sensitivity [32][33][34][35]52,53], we tested for seasonal effects of swim bladder morphology on sound pressure sensitivity by comparing the evoked potential magnitudes (μV) and auditory sensitivity (dB re: 1 µPa) of hair cells within the saccule of males of the same reproductive state with intact, sham ablated (i.e. control) or ablated (i.e.…”

“…Given the observed seasonal differences ( figure 2 ) and that multiple mechanisms have been shown to result in reproductive state-dependent differences in midshipman auditory sensitivity [ 32 – 35 , 52 , 53 ], we tested for seasonal effects of swim bladder morphology on sound pressure sensitivity by comparing the evoked potential magnitudes ( μ V) and auditory sensitivity (dB re: 1 µPa) of hair cells within the saccule of males of the same reproductive state with intact, sham ablated (i.e. control) or ablated (i.e.…”