Androgens and estrogens are crucial for the differentiation and function of the vocal control system of songbirds. A major source of estrogens in songbirds is the cerebral aromatization of circulating testosterone by aromatase (ARO). In the vocal control system, songbirds have a unique estrogen receptor (ER)‐containing area, the nucleus hyperstriatalis ventrale pars caudale (HVC) of the caudal neostriatum. Work in the zebra finch has demonstrated ARO expression adjacent to but not in the HVC. Compared with other songbirds, such as the canary, the HVC of adult zebra finches contains only few ERs. To determine whether the disjunctive distribution of ERs and ARO in the forebrain is a songbird‐specific feature, the authors investigated ARO and ER mRNA expression in songbirds (canary, house sparrow, and zebra finch) and in nonsongbirds (budgerigar, ring dove, swift, grey partridge, and barn owl) of five avian orders. In addition, the coexpression of androgen receptor (AR) and ARO mRNAs was studied. Preoptic hypothalamic areas showed similar expression of ARO in all species. In the caudal neostriatum, ARO, AR, and ER transcripts were found only in songbirds. ARO and ER mRNA expression in the caudal forebrain was spatially separated, i.e., the HVC contained ER mRNA but very little or no ARO mRNA, and the caudomedial neostriatum contained high levels of ARO mRNA but few if any ERs. ARO and AR mRNAs, however, were coexpressed in the caudomedial neostriatum. The coexpression of ARO mRNA with AR mRNA but not with ER mRNA was found in further brain areas, such as the nucleus posterior lateralis hypothalami. The area‐specific coexpression of AR, ER, and ARO suggests various possibilities for the steroid‐dependent regulation of ARO and for the role of ARO in controlling AR‐ and ER‐dependent mechanisms. J. Comp. Neurol. 407:115–129, 1999. © 1999 Wiley‐Liss, Inc.
The expression of brain-derived neurotrophic factor (BDNF) mRNA is increased significantly within the high vocal center (HVc) of male but not female zebra finches from posthatching day 30-35 on. The population of HVc cells expressing BDNF mRNA included 35% of the neurons projecting to the nucleus robustus of the archistriatum (RA). In the RA and in RA-projecting neurons of the lateral portion of the magnocellular nucleus of the anterior neostriatum, BDNF mRNA was expressed at very low levels in both sexes. The BDNF-receptor trkB mRNA was expressed in the RA, in RA-projecting neurons of lateral portion of the magnocellular nucleus of the anterior neostriatum, and in the HVc, except in most of its RA-projecting neurons. Premature stimulation and an inhibitory effect on the normal increase of the BDNF mRNA expression in juvenile males occurred after treatments with 17-estradiol and the aromatase inhibitor fadrozole, respectively. The up-regulation of the BDNF expression in the HVc could be a mechanism by which estrogen triggers the differentiation of cells within and connected to the HVc of male zebra finches.
The development of sex differences in brain structure and brain chemistry ("brain sex") of vertebrates is frequently thought to depend entirely on gonadal steroids such as androgens and estrogens, which act on the brain at the genomic level by binding to intracellular transcription factors, the androgen receptors (ARs) and estrogen receptors (ERs). These hormone actions are thought to shift the brain from a monomorphic to a dimorphic phenotype. One prominent such example is the nucleus hyperstriatalis ventrale pars caudale (HVc) of the zebra finch (Poephila guttata), a set of cells in the caudal forebrain involved in the control of singing. In contrast with previous studies using nonspecific cell staining techniques, the size and neuron number of the HVc measured by the distribution of AR mRNA is already sexually dimorphic on posthatching day (P)9. No ARs or ERs are expressed in the HVc before day 9. Slice cultures of the caudal forebrain of P5 animals show that the sexually dimorphic expression of AR mRNA in HVc is independent of the direct action of steroids on this nucleus or any of its immediate presynaptic or postsynaptic partners. Therefore, gonadal steroids do not appear to be directly involved in the initial sex difference in the expression pattern of AR mRNA, size, and neuron number of the HVc. Furthermore, we demonstrate that the initial steroid-independent size and its subsequent steroid-independent growth by extension linearly with the extension of the forebrain explains 60-70% of the masculine development of the HVc. Thus, we suggest that epigenetic factors such as the gonadal steroids modify but cannot overwrite the sex difference in HVc volume determined autonomously in the brain.
In mammals, stress hormones have profound influences on spatial learning and memory. Here, we investigated whether glucocorticoids influence cognitive abilities in birds by testing a line of zebra finches selectively bred to respond to an acute stressor with high plasma corticosterone (CORT) levels. Cognitive performance was assessed by spatial and visual one-trial associative memory tasks. Task performance in the high CORT birds was compared with that of the random-bred birds from a control breeding line. The birds selected for high CORT in response to an acute stressor performed less well than the controls in the spatial task, but there were no significant differences between the lines in performance during the visual task. The birds from the two lines did not differ in their plasma CORT levels immediately after the performance of the memory tasks; nevertheless, there were significant differences in peak plasma CORT between the lines. The high CORT birds also had significantly lower mineralocorticoid receptor mRNA expression in the hippocampus than the control birds. There was no measurable difference between the lines in glucocorticoid receptor mRNA density in either the hippocampus or the paraventricular nucleus. Together, these findings provide evidence to suggest that stress hormones have important regulatory roles in avian spatial cognition.
Androgens and estrogens are crucial for the differentiation and function of the vocal control system of songbirds. A major source of estrogens in songbirds is the cerebral aromatization of circulating testosterone by aromatase (ARO). In the vocal control system, songbirds have a unique estrogen receptor (ER)-containing area, the nucleus hyperstriatalis ventrale pars caudale (HVC) of the caudal neostriatum. Work in the zebra finch has demonstrated ARO expression adjacent to but not in the HVC. Compared with other songbirds, such as the canary, the HVC of adult zebra finches contains only few ERs. To determine whether the disjunctive distribution of ERs and ARO in the forebrain is a songbird-specific feature, the authors investigated ARO and ER mRNA expression in songbirds (canary, house sparrow, and zebra finch) and in nonsongbirds (budgerigar, ring dove, swift, grey partridge, and barn owl) of five avian orders. In addition, the coexpression of androgen receptor (AR) and ARO mRNAs was studied. Preoptic hypothalamic areas showed similar expression of ARO in all species. In the caudal neostriatum, ARO, AR, and ER transcripts were found only in songbirds. ARO and ER mRNA expression in the caudal forebrain was spatially separated, i.e., the HVC contained ER mRNA but very little or no ARO mRNA, and the caudomedial neostriatum contained high levels of ARO mRNA but few if any ERs. ARO and AR mRNAs, however, were coexpressed in the caudomedial neostriatum. The coexpression of ARO mRNA with AR mRNA but not with ER mRNA was found in further brain areas, such as the nucleus posterior lateralis hypothalami. The area-specific coexpression of AR, ER, and ARO suggests various possibilities for the steroid-dependent regulation of ARO and for the role of ARO in controlling AR- and ER-dependent mechanisms.
Songbirds have a specialized steroid-sensitive network of brain nuclei, the song system, for controlling song. Most nuclei of the song system express androgen receptors, and the sensory-motor integration nucleus High Vocal Center (HVC) alone also expresses estrogen receptors. Apart from expressing estrogen receptors in the vocal control system, songbirds are unique among birds because they have high concentrations of the estrogen-synthesizing enzyme aromatase in the neostriatum surrounding HVC. However, the role of estrogen in controlling the development of the song structure has been scarcely investigated. In this work, we show that blocking the production of estrogen during testosterone-induced song motor development in adult female canaries alters the song pattern compared to control females treated with testosterone only. These effects were correlated with inhibition of the expression of estrogen-sensitive genes, such as brain-derived nerve growth factor, in HVC. The expression of the ATP-synthase gene, an indicator of cell activity, in HVC, and the size of HVC, were not affected by the treatment. Our results provide the first example of estrogen-sensitive mechanisms controlling the structural features of adult birdsong.
In birds and mammals, including humans, melatonin-binding sites are abundant in brain areas that have no known clock function. Although the role of such binding sites is still unclear, it is assumed that these sites link neural functions to circadian or circannual demands of neuroendocrine homeostasis and reproduction. To investigate a possible direct role of melatonin in motor control, we studied the song and neural song system of the zebra finch. Neurons of two sensory-motor areas of the descending song control circuit that are crucial for the organization of the song pattern, the HVC and RA, express the melatonin-1B receptor (Mel1B), while the hypoglossal motor neurons of the song circuit express melatonin-1C receptors (Mel1C). Application of melatonin to brain slices decreases the firing-rate of RA-neurons. Systemic administration of a Mel1B antagonist at the beginning of the night shortens the song and motif length and affects the song syllable lengths produced the next day. The temporal pattern of the song, however, does not undergo daily changes. Thus, melatonin is likely to affect a non-circadian motor pattern by local modulation of song control neurons and in consequence alters a sexual signal, the song of the zebra finch.
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