A core aspect of human communication is flexible speech, long believed to be unique to humans among primates. However, recent findings suggest that some non-human primates, such as marmosets, also exhibit vocal plasticity. Investigating the neural correlates of vocal flexibility in marmosets provides insight into its origins in humans due to brain homologies. While much research focuses on cortical areas, the role of subcortical regions is understudied. Basal ganglia are related to the choice/initiation of actions, fine motor control, and learning of motor sequences; hence, it is likely to be relevant for vocal flexibility. Here, using previously collected histological data and stereological methods, we tested the hypothesis that the caudate nucleus and the putamen, in the basal ganglia, are activated during vocal communication and used the expression of the immediate early gene egr-1 to map its activation in three groups of marmosets. The first group did not vocalize during testing (C), the second group heard playback vocalizations but did not vocalize (H/O), and the third group heard playback calls and vocalized (H/V). We observed an increase in egr-1 expression in both areas in the H/O condition compared to the C condition and a further significant increase in egr-1 expression in the same areas in the H/V condition compared to the H/O condition. To ensure the specificity of observed changes, we compared erg-1 expressing cells in primary sensory and motor areas, finding no significant difference among the three conditions. Additionally, we quantified locomotion during the one hour preceding the experimental end-point to rule out movement discrepancies as an explanation for observed group differences in erg-1 expression, finding no correlation between locomotion and expression variance. Our results indicate basal ganglia activation during vocal listening and production, independent of other brain areas and body movements, supporting our hypothesis. The relevance of basal ganglia in songbird vocal learning, along with our findings in marmosets, suggests their importance in understanding the evolution of vocal learning.