Breeding Conditions Induce Rapid and Sequential Growth in Adult Avian Song Control Circuits: A Model of Seasonal Plasticity in the Brain

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.