Rapid seasonal-like regression of the adult avian song control system

Abstract

We analyzed how rapidly avian song control nuclei regress after testosterone (T) withdrawal. Regression of neuronal attributes resulting from T withdrawal has been observed in several animal models. The time course over which regression occurs is not known, however. To address this issue, we castrated adult male white-crowned sparrows and rapidly shifted them to short-day photoperiods after being held under breeding conditions (long-day photoperiod and systemic T exposure) for 3 weeks. We found that the volume of one song nucleus, HVC, regressed 22% within 12 h after T withdrawal. Changes in HVC neuron density after T withdrawal were dynamic; density increased at 12 h and then decreased by 4 days. HVC neuron number was reduced by 26% by 4 days. The volumes of Area X and the robust nucleus of the arcopallium (RA) were significantly regressed by 7 and 20 days, respectively. RA somatic area and neuronal spacing were significantly reduced by 2 days. The rapidity of HVC regression is unprecedented among vertebrate models of hormone-sensitive neural circuits. These results reveal that the rapid regression of the song control system provides a model for the important role sex steroid hormones play in mediating adult neural plasticity and in neuroprotection.

Fig. 1.

Coronal sections of HVC and RA of male white-crowned sparrows illustrate the rapid regression of the song control system. (A) HVC and RA grow to full size within 3 weeks of exposure to a LD photoperiod and high levels of T. (B) Twelve hours after T withdrawal, HVC volume regresses significantly, largely driven by a sharp increase in HVC neuron density. RA volume is unchanged. (C) Twenty days after T withdrawal and shift to a SD photoperiod, RA is fully regressed. (Scale bars: 0.5 mm.)

Fig. 2.

The volumes of HVC, RA, and Area X regress rapidly after T withdrawal and photoshift. Each dot represents the ratio of song system nucleus to telencephalon volume for an individual bird, and bars indicate mean for each time point. (A) HVC was significantly regressed within 12 h after T withdrawal. (B and C) RA and Area X regressed more slowly, 20 and 7 days, respectively. Letters above bars illustrate significant differences among groups after post hoc test (Holm–Sidak, P ≤ 0.05).

Fig. 3.

HVC neuronal attributes regress rapidly after T withdrawal and photoshift. (A) Somatic area of HVC neurons decreases within 2 days. (B) HVC neuron density changes dynamically after manipulation. Density increases by 47% within 12 h and decreases to LD+T levels within 4 days. (C) HVC neuron number significantly decreases within 4 days. Dots indicate individual birds, and bar indicates mean.

Fig. 4.

RA neuronal attributes regress rapidly after T withdrawal and photoshift. (A) Somatic area of RA neurons decreases significantly within 2 days and continues to decrease over the time course. (B) RA neuron density increases significantly within 2 days and continues to increase over the time course. (C) RA neuron number does not decrease significantly across the entire time course. Dots indicate individual birds, and bar indicates mean.