Regulatory Mechanisms of Testosterone-stimulated Song in the Sensorimotor Nucleus HVC of Female Songbirds

Background: In male birds, influence of the sex steroid hormone testosterone and its estrogenic metabolites on seasonal song behavior has been demonstrated for many species. In contrast, female song was only recently recognized to be widespread among songbird species, and to date, sex hormone effects on singing and brain regions controlling song development and production (song control nuclei) have been studied in females almost exclusively using domesticated canaries (Serinus canaria). However, domesticated female canaries hardly sing at all in normal circumstances and exhibit only very weak, if any, song seasonally under the natural photoperiod. By contrast, adult female European robins (Erithacus rubecula) routinely sing during the winter season, a time when they defend feeding territories and show elevated circulating testosterone levels. We therefore used wild female European robins captured in the fall to examine the effects of testosterone administration on song as well as on the anatomy and the transcriptome of the song control nucleus HVC (sic). The results obtained from female robins were compared to outcomes of a similar experiment done in female domesticated canaries.

Results: Testosterone treatment induced abundant song in female robins. Examination of HVC transcriptomes and histological analyses of song control nuclei showed testosterone-induced differentiation processes related to neuron growth and spacing, angiogenesis and neuron projection morphogenesis. Similar effects were found in female canaries treated with testosterone. In contrast, the expression of genes related to synaptic transmission was not enhanced in the HVC of testosterone treated female robins but was strongly up-regulated in female canaries. A comparison of the testosterone-stimulated transcriptomes indicated that brain-derived neurotrophic factor (BDNF) likely functions as a common mediator of the testosterone effects in HVC.

Conclusions: Testosterone-induced singing of female robins correlated with cellular differentiation processes in the HVC that were partially similar to those seen in the HVC of testosterone-treated female canaries. Other modes of testosterone action, notably related to synaptic transmission, appeared to be regulated in a more species-specific manner in the female HVC. Divergent effects of testosterone on the HVC of different species might be related to differences between species in regulatory mechanisms of the singing behavior.