Sex differences and similarities in the neural circuit regulating song and other reproductive behaviors in songbirds

Abstract

In the 1970s, Nottebohm and Arnold reported marked male-biased sex differences in the volume of three song control nuclei in songbirds. Subsequently a series of studies on several songbird species suggested that there is a positive correlation between the degree to which there is a sex difference in the volume of these song control nuclei and in song behavior. This correlation has been questioned in recent years. Furthermore, it has become clear that the song circuit is fully integrated into a more comprehensive neural circuit that regulates multiple courtship and reproductive behaviors including song. Sex differences in songbirds should be evaluated in the context of the full complement of behaviors produced by both sexes in relation to reproduction and based on the entire circuit in order to understand the functional significance of variation between males and females in brain and behavior. Variation in brain and behavior exhibited among living songbird species provides an excellent opportunity to understand the functional significance of sex differences related to social behaviors.

Keywords: Area X of the medial striatum; Canaries; HVC (abbreviation used as the common name); Robust nucleus of the arcopallium (RA); Song control system; Steroid hormones; Testosterone.

Figure 1

Photomicrographs of Nissl-stained sections illustrating the larger sex difference in RA volumes observed in zebra finches as compared to canaries. Figure based on material in (Nottebohm and Arnold, 1976).

Figure 2

Photomicrographs of Nissl-stained sections (A-F) and of autoradiograms based onin vitro labeling for alpha2-adrenergic receptors density (G-H) illustrating the sex differences in the volume of the song control nuclei in European starlings. All photomicrographs in the left columns are from males (A,C,E,G) and in the right column from females (B,D,F,H). The boundaries of HVC (A-B), RA (C-D) and Area X (E-F) in Nissl-stained sections are indicated by arrows. The larger Area X in males compared to females is confirmed by a larger volume based on the density of alpha2-adrenergic binding (G-H). Magnification bars= 1 mm. Figure based on material in (Bernard et al., 1993) and (Ball et al., 1993).

Figure 3.

Relationships between sex difference in singing behavior and sex differences in volume of the song control nucleus HVC. Panels A and B illustrate the relationship across multiple species belonging to different families of songbirds between the ratio of HVC volume in females versus males and the relative repertoire size (A) or the relative amount of songs produced (B) in the two sexes. Song output in B was qualitatively estimated as follows 1: females never sing, 2: females rarely sing, 3: females sing but less often than males, 4: females commonly sing and 5: females and males duet. Panel C to F illustrate the relative volume of HVC in males and females of 4 species in which either males and females are duetting and thus producing approximately similar amounts of songs of similar quality (C-E) or in which females sing more than males but songs have a similar quality in both sexes (F). Redrawn from data in (MacDougall-Shackleton and Ball, 1999),(Brenowitz and Arnold, 1988), (Gahr et al., 2008), (Hall et al., 2010)

Figure 4.

Schematic representation of the song control system and its putative relationships with the medial preoptic nucleus POM via the periaqueductal gray (PAG) and the ventral tegmental area (VTA) illustrated by red arrows.

Figure 5.

Schematic representation of the song control system and its downstream projections to the syrinx (required for the production of song), the respiratory muscles (required for the synchronization of singing with respiration) and to the sacral spinal cord neurons that control cloacal contractions and also presumably some of the muscles implicated in the control of the copulatory solicitation display (female sexual receptivity). Whether a similar pathway controls male sexual behavior remains unexplored at this time. Panel A illustrates these connections in the entire body while panel B presents more detail of the implicated brain pathways.

Figure 6.

Summary of the experiments investigating the action of testosterone at multiple brain sites in the context of the activation of singing behavior. Up and down arrows represent increases or decreases of the behavioral trait considered.