Deafening-Induced Vocal Deterioration in Adult Songbirds Is Reversed by Disrupting a Basal Ganglia-Forebrain Circuit

Motor exploration can be an adaptive strategy when behavior fails to achieve an expected outcome. For example, like humans, adult songbirds change their vocal output when auditory feedback is altered or absent. Here, we show that the output of an anterior forebrain pathway (AFP) through the avian basal ganglia directly contributes to the expression of deafening-induced vocal changes in adulthood. Lesioning the output nucleus of this circuit in adult male zebra finches reverses moderate changes in song structure and variability caused by deafening. Furthermore, the results indicate that more severe deafening-induced changes in vocal behavior likely reflect altered function outside the AFP (e.g., within the vocal motor pathway). AFP lesions do not promote recovery if songs are severely deteriorated at the time of lesion even though previous work shows that the AFP is required for such deterioration to emerge. Thus, in birds, as in mammals, the contribution of basal ganglia-thalamic-cortical circuits to motor control may change when feedback is absent or unexpected and includes both “active” and “permissive” roles.

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