The basal ganglia have been implicated in auditory-dependent vocal learning and plasticity in human and songbirds, but the underlying neural phenotype remains to be clarified. Here, using confocal imaging and three-dimensional electron microscopy, we investigated striatal structural plasticity in response to hearing loss in Area X, the avian vocal basal ganglia, in adult male zebra finch (Taeniopygia guttata). We observed a rapid elongation of dendritic spines, by approximately 13%, by day 3 after deafening, and a considerable increase in spine synapse density, by approximately 61%, by day 14 after deafening, compared with the controls with an intact cochlea. These findings reveal structural sensitivity of Area X to auditory deprivation and suggest that this striatal plasticity might contribute to deafening-induced changes to learned vocal behavior.

Natural background noises are common in the acoustic environments in which most organisms have evolved. Therefore, the vocalization and sound perception systems of vocal animals are inherently equipped to overcome natural background noise. Human-generated noises, however, pose new challenges that can hamper audiovocal communication. The mechanisms animals use to cope with anthropogenic noise disturbances have been extensively explored in a variety of taxa. Bats emit echolocation pulses primarily to orient, locate and navigate, while social calls are used to communicate with conspecifics. Previous studies have shown that bats alter echolocation pulse parameters in response to background noise interference. In contrast to high-frequency echolocation pulses, relatively low-frequency components within bat social calls overlap broadly with ambient noise frequencies. However, how bats structure their social calls in the presence of anthropogenic noise is not known. Here, we hypothesized that bats leverage vocal plasticity to facilitate vocal exchanges within a noisy environment. To test this hypothesis, we subjected the Asian particolored bat, Vespertilio sinensis, to prerecorded traffic noise. We observed a significant decrease in vocal complexity (i.e., an increased frequency of monosyllabic calls) in response to traffic noise. However, an increase in the duration and frequency of social calls, as have been observed in other species, was not evident. This suggests that signal simplification may increase communication efficacy in noisy environments. Moreover, V. sinensis also increased call amplitude in response to increased traffic noise, consistent with the predictions of the Lombard effect.

Deafening elicits a deterioration of learned vocalization, in both humans and songbirds. In songbirds, learned vocal plasticity has been shown to depend on the basal ganglia-cortical circuit, but the underlying cellular basis remains to be clarified. Using confocal imaging and electron microscopy, we examined the effect of deafening on dendritic spines in avian vocal motor cortex, the robust nucleus of the arcopallium (RA), and investigated the role of the basal ganglia circuit in motor cortex plasticity. We found rapid structural changes to RA dendritic spines in response to hearing loss, accompanied by learned song degradation. In particular, the morphological characters of RA spine synaptic contacts between 2 major pathways were altered differently. However, experimental disruption of the basal ganglia circuit, through lesions in song-specialized basal ganglia nucleus Area X, largely prevented both the observed changes to RA dendritic spines and the song deterioration after hearing loss. Our results provide cellular evidence to highlight a key role of the basal ganglia circuit in the motor cortical plasticity that underlies learned vocal plasticity.