Department of Neurobiology and Behavior, Cornell University, Ithaca, NY, USA.
Department of Biology, Brooklyn College, The City University of New York, Brooklyn, NY, USA.
Integr Comp Biol. 2021 Jul 23;61(1):269-282. doi: 10.1093/icb/icab070.
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 with 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 (TH-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 fibers 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, in part, by dopamine.
在季节性繁殖的脊椎动物中，激素协调神经系统结构和功能的变化，以促进生殖准备和成功。类固醇激素通常通过调节神经调质间接发挥作用，而神经调质反过来又可以协调感觉输入与适当的运动输出的调制。雌性平鳍中期鱼（Porichthys notatus）在夏季繁殖季节会增加外周听觉敏感性，从而提高其检测配偶的能力，这种能力受类固醇激素调节。与冬季非繁殖期的雌性相比，繁殖期雌性的听觉回路儿茶酚胺能神经支配也存在差异，这可以通过酪氨酸羟化酶（TH）来衡量，TH 是儿茶酚胺合成的限速酶。重要的是，来自多巴胺能特定前脑核的内耳多巴胺能传入在夏季减少，而多巴胺抑制内耳的敏感性，这表明性腺类固醇可能通过调节多巴胺能神经支配来改变听觉敏感性。在这项研究中，我们对非繁殖期的雌性进行了性腺切除术，植入了雌二醇（E2）或睾酮（T），并测量了先前显示季节性可塑性的听觉核中儿茶酚胺能神经支配的 TH 免疫反应（TH-ir）纤维。我们发现，T 处理而非 E2 处理减少了听觉后脑的 TH-ir 神经支配。T 处理还减少了投射到内耳的前脑多巴胺能细胞群中的 TH-ir 纤维，并且可能投射到听觉后脑。治疗组中的 T 血浆水平较高与内耳 TH 末端的减少相关。这些 T 处理诱导的 TH-ir 纤维变化模拟了中期鱼内耳多巴胺的季节性下调，并提供了证据表明类固醇激素对周围听觉敏感性的调节部分是通过多巴胺介导的。
