Afferent input is necessary for seasonal growth and maintenance of adult avian song control circuits

Abstract

The neural circuits that regulate song behavior in adult songbirds undergo pronounced seasonal changes in morphology, primarily in response to changes in plasma testosterone (T). Most song nuclei have T receptors. We asked whether seasonal growth and maintenance of nuclei within these circuits are direct responses to the effects of T or its metabolites or are mediated indirectly via the effects of T on afferent nuclei. Photosensitive white-crowned sparrows were exposed to one of three treatments. (1) The neostriatal nucleus HVc (also known as the "high vocal center") was lesioned unilaterally, and the birds were exposed to long-day (LD) photoperiods and breeding levels of T for 30 d. (2) Birds were exposed to LD plus T (LD+T) for 30 d; then HVc was lesioned, and the birds were killed after an additional 30 d exposure to LD+T. (3) HVc was lesioned, and the sparrows were housed on short-day (SD) photoperiods in the absence of T treatment for 30 d. In both LD+T groups, the direct efferent targets of HVc, the robust nucleus of the archistriatum (RA) and area X, were smaller ipsilateral to the lesion. The lesion did not prevent growth of the hypoglossal motor nucleus, which does not receive direct afferent input from HVc. RA and area X were also smaller ipsilateral to the lesion in the SD birds. These results indicate that afferent input is required both for the growth of adult song circuits in response to typical breeding photoperiod and hormone conditions and for the maintenance of efferent nuclei in either their regressed or enlarged states.

Fig. 1.

Simplified schematic sagittal view of the avian song control system showing 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.

Photographs showing RA (top) and area X (bottom) ipsilateral (right) and contralateral (left) to a unilateral lesion of HVc in a male white-crowned sparrow exposed to long days plus testosterone treatment for 30 d after the lesion. The maximum extent of each nucleus is indicated with arrows. Scale bars, 1 mm.

Fig. 3.

The volumes (mean ± SEM) of RA (top) and area X (bottom) ipsilateral and contralateral to the lesioned HVc in the SD, growth, and maintenance (maint.) treatment groups. The volume of each nucleus was divided by the volume of the entire telencephalon contralateral to the lesioned HVc. Different letters above thevertical bars indicate significant differences in volume between sides of the brain and between treatment groups.

Fig. 4.

The relationship between the volume of HVc remaining after the lesion, if any, and the volumes of RA (top) and area X (bottom) ipsilateral to the lesion in the growth and maintenance groups.

Fig. 5.

Neuronal attributes (mean ± SEM) of RA ipsilateral and contralateral to the lesioned HVc in the SD, growth, and maintenance groups. Different letters above the vertical bars indicate significant differences between sides of the brain and between treatment groups.