Seasonal changes in testosterone, neural attributes of song control nuclei, and song structure in wild songbirds

Abstract

Seasonal changes in the neural attributes of brain nuclei that control song in songbirds are among the most pronounced examples of naturally occurring plasticity in the adult brain of any vertebrate. The behavioral correlates of this seasonal neural plasticity have not been well characterized, particularly in songbird species that lack adult song learning. To address this question, we investigated the relationship between seasonal changes in gonadal steroids, song nuclei, and song behavior in adult male song sparrows (Melospiza melodia). At four times of the year, we measured plasma concentrations of testosterone, neural attributes of song nuclei, and several aspects of song structure in wild song sparrows of a nonmigratory population. We found seasonal changes in the song nuclei that were temporally correlated with changes in testosterone concentrations and with changes in song stereotypy. Male song sparrows sang songs that were more variable in structure in the fall, when testosterone concentrations were low and song nuclei were small, than in the spring, when testosterone concentrations were higher and song nuclei were larger. Despite seasonal changes in the song nuclei, the song sparrows continued to sing the same number of different song types, indicating that changes in the song nuclei were not correlated with changes in song repertoire size. These results suggest that song stereotypy, but not repertoire size, is a potential behavioral correlate of seasonal plasticity in the avian song control system.

Fig. 1.

Seasonal changes in plasma T concentrations. Columns represent mean ± SEM (error bars) plasma T concentrations in male song sparrows collected at each of the four sampling times. Season significantly affected plasma T concentrations (ANOVA,p < 0.001). a–c, Significant differences between seasons (PLSD, p < 0.05). Sample sizes are as follows: early spring, 6; late spring, 9; early fall, 7; late fall, 8.

Fig. 2.

Seasonal changes in the size of HVC and RA. Columns represent mean ± SEM (error bars) volume of HVC and RA. Season significantly affected the volume of HVC and RA (ANOVA,p < 0.001 for both). a, b, Significant differences between seasons (PLSD, p < 0.05). Sample sizes are as follows in both graphs: early spring, 5; late spring, 10; early fall, 7; late fall, 8.

Fig. 3.

Seasonal changes in HVC neuronal attributes. Columns represent mean ± SEM (error bars) cross-sectional area of neuronal somata (A), neuronal density (B), or neuronal number (C) in HVC. HVC neuron size (A) and number (C) changed seasonally (ANOVA,p < 0.01 for both). Neuronal density in HVC (B) did not change seasonally. a, b, Significant differences between seasons (PLSD,p < 0.05). Sample sizes are as follows for all panels: early spring, 5; late spring, 10; early fall, 6; late fall, 8.

Fig. 4.

Seasonal changes in RA neuronal attributes. Columns represent mean ± SEM (error bars) cross-sectional area of neuronal somata (A), neuronal density (B), or neuronal number (C) in RA. RA neuron size (A) and density (B) changed seasonally (ANOVA,p < 0.01 for both). The number of neurons in RA (C) did not change seasonally. a, b, Significant differences between seasons (PLSD,p < 0.05). Sample sizes are as follows for all panels: early spring, 5; late spring, 10; early fall, 7; late fall, 8.

Fig. 5.

Seasonal changes in structural stereotypy of notes. Sound spectrograms of a single note. Left, Three renditions of the same pure tone note sung by the same male song sparrow in the late spring. The three renditions contain little or no frequency modulation and are similar to each other in structure.Right, Three renditions of the same note as on theleft sung by the same song sparrow in the early fall. The three early fall renditions contain more frequency modulation and are less similar to each other. Thus, the structure of this note was more stereotyped in the late spring than in the early fall. Calibration, 0.25 sec.