Breeding conditions induce rapid and sequential growth in adult avian song control circuits: a model of seasonal plasticity in the brain

Abstract

In adult songbirds, seasonal changes in photoperiod and circulating testosterone (T) stimulate structural changes within the neural song control circuitry. The mechanisms that control this natural plasticity are poorly understood. To determine how quickly and in what sequence the song nuclei respond to changing daylength and circulating T, we captured 18 adult male white-crowned sparrows and kept them on short days for 12 weeks. We killed five of these birds and exposed the rest to long days (LD) and elevated T. We killed these birds either 7 or 20 d after LD + T exposure. We measured song nuclei volumes and cellular attributes, the mass of the vocal production organ (the syrinx), and song behavior. The neostriatal song control nucleus HVC (also known as "high vocal center"), added 50,000 neurons and increased in size within 7 d of exposure to LD + T. Efferent targets of HVC, the robust nucleus of the archistriatum (RA), and area X of the parolfactory lobe grew more slowly and were not significantly larger until day 20 of the study. The tracheosyringeal portion of the hypoglossal nucleus (nXIIts), which receives projections from RA and normally grows in response to seasonal cues, did not grow over the time course of this study. Syringeal mass increased within 7 d of LD + T treatment. The anatomical changes in the brain were accompanied by behavioral changes in song production. On day 7 when the song circuitry was incompletely developed, male sparrows sang less stereotyped songs than males at day 20 with more completely developed song circuits. These results suggest that the song circuitry responds rapidly and sequentially to breeding-typical conditions (long days and elevated T), and that song stereotypy increases as nuclei within this circuitry grow.

Fig. 1.

Simplified schematic sagittal view of the avian song control system illustrating the distribution of steroid receptors.Black arrows connect nuclei in the main descending motor circuit, and white arrows connect nuclei in the anterior forebrain circuit. DLM, Dorsolateral nucleus of the medial thalamus; lMAN, lateral portion of the magnocellular nucleus of the anterior neostriatum;nXIIts, the tracheosyringeal portion of the hypoglossal nucleus; RA, the robust nucleus of the archistriatum;syrinx, vocal production organ; V,lateral ventricle; X, area X of the parolfactory lobe.

Fig. 2.

Sound spectrogram showing terminology used to describe Gambel's white-crowned sparrow song.

Fig. 3.

Song system growth in response to long days and testosterone treatment that simulates breeding season conditions. Song nuclei sizes for each bird were expressed as a percentage of each bird's telencephalon volume (Table 2). To determine how quickly each nucleus grew toward its maximum size, mean song nucleus size at each time point was divided by mean song nucleus size at day 20. Note that HVC (black bars), RA (hatched bars), and area X (gray bars) were all fully developed at day 20 (see Results and Discussion).

Fig. 4.

Increased day length and testosterone administration induced significant neuronal attribute changes in HVC and RA (mean ± SEM). Data for HVC are shown in theleft three panels, and data for RA are shown in theright three panels. The cross-sectional areas of HVC and RA neuronal somata both increased significantly by day 7. HVC neuron number was significantly increased by day 7. RA neuron density was significantly decreased at day 20. Letters abovecurves indicate statistical differences among groups.