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Animals flexibly switch between different actions by changing neural activity patterns for motor control. Courting Drosophila melanogaster males produce two different acoustic signals, pulse and sine song, each of which can be promoted by artificial activation of distinct neurons. However, how the activity of these neurons implements flexible song production is unknown. Here, we developed an assay to record neuronal calcium signals in the ventral nerve cord, which contains the song motor circuit, in singing flies. We found that sine-promoting neurons, but not pulse-promoting neurons, show strong activation during sine song. In contrast, both pulse- and sine-promoting neurons are active during pulse song. Furthermore, population calcium imaging in the song circuit suggests that sine song involves activation of a subset of neurons that are also active during pulse song. Thus, differential activation of overlapping, rather than distinct, neural populations underlies flexible motor actions during acoustic communication in D. melanogaster.