Estradiol-dependent catecholaminergic innervation of auditory areas in a seasonally breeding songbird

Abstract

A growing body of evidence suggests that gonadal steroids such as estradiol (E2) alter neural responses not only in brain regions associated with reproductive behavior, but also in sensory areas. Because catecholamine systems are involved in sensory processing and selective attention, and because they are sensitive to E2 in many species, they may mediate the neural effects of E2 in sensory areas. Here, we tested the effects of E2 on catecholaminergic innervation, synthesis, and activity in the auditory system of white-throated sparrows, a seasonally breeding songbird in which E2 promotes selective auditory responses to song. Non-breeding females with regressed ovaries were held on a winter-like photoperiod and implanted with silastic capsules containing either no hormone or E2. In one hemisphere of the brain, we used immunohistochemistry to quantify fibers immunoreactive for tyrosine hydroxylase or dopamine beta-hydroxylase in the auditory forebrain, thalamus, and midbrain. E2 treatment increased catecholaminergic innervation in the same areas of the auditory system in which E2 promotes selectivity for song. In the contralateral hemisphere, we quantified dopamine, norepinephrine and their metabolites in tissue punches using HPLC. Norepinephrine increased in the auditory forebrain, but not the midbrain, after E2 treatment. We found evidence of interhemispheric differences, both in immunoreactivity and catecholamine content did not depend on E2 treatment. Overall, our results show that increases in plasma E2 typical of the breeding season enhance catecholaminergic innervation and synthesis in some parts of the auditory system, raising the possibility that catecholamines play a role in E2-dependent auditory plasticity in songbirds.

Catecholaminergic Fiber Innervation of the Vocal Motor System Is Intrasexually Dimorphic in a Teleost with Alternative Reproductive Tactics

“…Male morphs are not only divergent in circulating steroid levels but also in brain aromatase, 11β-hydroxylase (11β-H), 11β-hydroxysteroid dehydrogenase (11β-HSD), as well as glucocorticoid and estrogen receptor expression [Schlinger et al, 1999; Arterbery et al, 2010a, 2010b; Bass and Forlano, 2008; Fergus and Bass 2013]. Because steroid hormones are known to regulate CA expression and/or correlate with TH-ir neuron number and fiber density [Wilczynski et al, 2003; Weltzien et al, 2006; LeBlanc et al, 2007; Matragrano et al, 2011], differential circulating or brain-derived steroid hormones may underlie morph differences in the number of TH-ir vagal neurons and innervation patterns of TH-ir fibers terminating into the VMN. Since steroid hormone levels vary seasonally and with vocal behavior in type I males [Sisneros et al, 2004; Genova et al, 2012], there may yet prove to be plasticity in TH-ir innervation of VMN within male morphs between seasons (and likely between courtship and parental phase within the summer reproductive season in type I males), similar to our findings in the auditory system of females [Forlano et al, 2015].…”

“…TH-ir fibers covering the area defined as region of interest (ROI) were subsequently measured using the Region Statistics feature to obtain data on total TH-ir area (µm 2 ), total area sampled (µm 2 ), average intensity (intensity independent of area), and integrated (total) intensity (TH-ir area divided by a 0.3225 µm 2 distance calibration constant and multiplied by average intensity) per section in the hypothalamus and midbrain, and per fractional area in the VMN. This approach has been similarly employed by other studies examining TH-ir fiber plasticity in songbirds and midshipman [LeBlanc et al, 2007; Matragrano et al, 2011; Forlano et al, 2015]. …”

Estradiol-dependent modulation of serotonergic markers in auditory areas of a seasonally breeding songbird.

“…3). We defined cNCM as a strip of tissue approximately 275 μm from the caudal boundary of NCM (Sanford et al, 2010; Matragrano et al, 2011). The acquired images of cNCM captured the majority of that domain, spanning 870 μm from dorsal to ventral (Fig.…”

“…For aNCM, we placed a circle approximately 350 μm in diameter dorsal to Field L and just ventral to the ventricle. For rdNCM and rvNCM, we placed two circles, each approximately 550 μm in diameter, into the dorsal and ventral portions of this region (Matragrano et al, 2011; Sanford et al, 2010) so that they did not overlap with Field L or with the region we defined as cNCM. Because we did not conduct tract tracing or another method that would enable us to discern absolutely the boundary between the rostral domains of NCM and the adjacent subregions of Field L (Vates et al, 1996), it is possible that our samples of aNCM, rdNCM and rvNCM may have captured a bit of L1 and L3, respectively.…”

Catecholaminergic connectivity to the inner ear, central auditory, and vocal motor circuitry in the plainfin midshipman fish porichthys notatus

“…Although homologies of auditory nuclei between fishes and tetrapods is less clear outside of the midbrain TS, CAergic innervation is consistently found in auditory nuclei in hindbrain and thalamus in mammals, birds and frogs (e.g., Appeltants et al, 2001;Bottjer, 1993;Gonzalez and Smeets, 1991;Kitahama et al, 1996;Kitt and Brauth, 1986a;Klepper and Herbert, 1991;Matragrano et al, 2011;Mello et al, 1998;Woods and Azeredo, 1999). Thus, CAergic innervation at multiple levels of ascending auditory circuitry appears to be a common feature across vertebrates.…”