ZENK labeling within social behavior brain regions reveals breeding context-dependent patterns of neural activity associated with song in male European starlings (Sturnus vulgaris)

Abstract

In songbirds, song learning and production are regulated by the song control system. How the rest of the brain interacts with song nuclei to ensure that song is produced in an appropriate context is not yet clear. In male European starlings (Sturnus vulgaris), breeding context song is sexually motivated whereas non-breeding context song is more broadly socially motivated. Brain regions involved in regulating social behavior might differentially regulate starling song depending upon the context in which it is produced. Here, we compared the number of ZENK-labeled cells in song and social behavior nuclei in starlings singing in either a breeding or a non-breeding context. Numbers of ZENK-labeled cells in HVC related positively to song produced in both contexts. Interestingly, numbers of ZENK-labeled cells in one subdivision of the lateral septum (LS) related negatively to breeding context song but positively to non-breeding context song. In a subdivision of the medial bed nucleus of the stria terminalis (BSTm) ZENK labeling only related positively to non-breeding context song whereas in the ventromedial nucleus of the hypothalamus (VMH) ZENK labeling showed a tighter positive relationship with breeding context song. Together, these findings indicate that social behavior brain regions outside of the song control system regulate singing behavior differently depending upon whether song is sexually or more broadly socially motivated. Breeding context-dependent regulation of song by LS, BSTm, and VMH suggests that these nuclei may be central to adjusting song production so that it occurs in response to appropriate social and environmental stimuli. Keywords songbird; season; social context; ZENK; high vocal center; lateral septum; bed nucleus of the stria terminalis; ventromedial nucleus of hypothalamus

Opioid receptor densities analyzed across seasons in the POM and VTA of the dark-eyed junco, Junco hyemalis

“…Brain regions were delineated based on anatomical landmarks ( Fig. 1) and followed designations illustrated in Riters et al (2005), Heimovics and Riters (2007), and Reiner et al (2004). The rPOM is along the midline and located ventral to the septum and rostral to the anterior commissure.…”

Structural Changes between Seasons in the Songbird Auditory Forebrain

“…In songbirds, homologues for these regions have been identified (Goodson, 2005) and are implicated in the regulation of singing behavior (Riters and Ball, 1999;Maney and Ball, 2003;Heimovics et al, 2009). More and more studies suggest that the SBN differentially regulates song production within and outside the breeding season (Heimovics and Riters, 2007). In seasonal breeding songbirds, gonadal steroids increase SBN immediate early gene (IEG) expression induced by a socio-sexual signal (Maney et al, 2008).…”

Song competition changes the brain and behavior of a male songbird

“…In birds, one such region is the medial preoptic nucleus, which activates appetitive aspects of male sexual behavior, such as courtship (Balthazart and Ball, 2007), and, in male starlings, may regulate singing motivation and effort (Riters and Ball, 1999). In a breeding context, singing effort in starlings is correlated with the expression of the above-mentioned immediate, early genes in the medial preoptic nucleus (Heimovics and Riters, 2005), as well as in other areas of the basal forebrain and midbrain implicated in the regulation of social behavior (Goodson et al, 2005), including the medial bed nucleus of the stria terminalis, the anterior hypothalamus, the ventromedial nucleus of the hypothalamus, and the lateral septum (Heimovics and Riters, 2006;Heimovics and Riters, 2007). Clearly, future studies may benefit from a thorough examination of how the song environment, which affects singing effort, also affects these brain areas implicated in the neural control of singing effort.…”