Song environment affects singing effort and vasotocin immunoreactivity in the forebrain of male Lincoln's sparrows

Abstract

Male songbirds often establish territories and attract mates by singing, and some song features can reflect the singer's condition or quality. The quality of the song environment can change, so male songbirds should benefit from assessing the competitiveness of the song environment and appropriately adjusting their own singing behavior and the neural substrates by which song is controlled. In a wide range of taxa, social modulation of behavior is partly mediated by the arginine vasopressin or vasotocin (AVP/AVT) systems. To examine the modulation of singing behavior in response to the quality of the song environment, we compared the song output of laboratory-housed male Lincoln's sparrows (Melospiza lincolnii) exposed to 1 week of chronic playback of songs categorized as either high or low quality, based on song length, complexity, and trill performance. To explore the neural basis of any facultative shifts in behavior, we also quantified the subjects' AVT immunoreactivity (AVT-IR) in three forebrain regions that regulate sociosexual behavior: the medial bed nucleus of the stria terminalis (BSTm), the lateral septum (LS), and the preoptic area. We found that high-quality songs increased singing effort and reduced AVT-IR in the BSTm and LS, relative to low-quality songs. The effect of the quality of the song environment on both singing effort and forebrain AVT-IR raises the hypothesis that AVT within these brain regions plays a role in the modulation of behavior in response to competition that individual males may assess from the prevailing song environment.

Figure 1

Distribution of variation in the quality of songs recorded from free-living male Lincoln’s sparrows in their natural environment (white bars). Song quality was quantified as the first-axis factor scores from a Principal Components Analysis (PCA) of song length and total syllable count, which are strongly, positively correlated with song complexity (unique syllable count) and trill performance. For the experimental treatment, in which the quality of the song environment was manipulated, high quality song stimuli (gray bars) were selected from the positive end of the distribution associated with longer, more complex songs containing higher performance trills, and low quality song stimuli (black bars) were from the negative end of the distribution of PCA scores.

Figure 2

Photomicrographs illustrating where frames of focus were placed (top two images) to quantify arginine vasotocin immunoreactivity (AVT-IR) in the bed nucleus of the stria terminalis (BSTm), lateral septum (LS) and preoptic area (POA). Example images from all three brain regions from male Lincoln’s sparrows in the low quality and high quality song environment treatments are included (bottom two rows). Images were taken from sections approximately 600 μm from the midline but it should be noted that the POA is the most medial region and the BSTm is the most lateral region examined, making it difficult to depict in the same photomicrograph the precise locations of both regions. CoA: anterior commissure, OM: occipito-mesencephalic tract, TSM: septopallio-mesencephalic tract

Figure 3

Effects of the quality of the song environment on singing effort (mean daily song count ± S.E.M.) on mornings 1, 3, 5, 7 and 8 in male Lincoln’s sparrows.

Figure 4

(Left Column) Effect of the quality of the song environment on mean arginine vasotocin immunoreactivity (AVT-IR ± S.E.M.) in the bed nucleus of the stria terminalis (BSTm, quantified as number of 1849 μm² squares in digital images with AVT-immunoreactive fibers), lateral septum (LS, quantified as number of 1849 μm² squares in digital images with AVT-immunoreactive fibers) and preoptic area (POA, quantified as the percent area with AVT-IR) for subjects in the high and low quality song environments. (Right Column) Relationship between AVT-IR in each brain region and singing effort (mean day 8 song count ± S.E.M.; values for subjects in the high quality song environment are indicated with open circles, values for subjects in the low quality song environment with closed circles).