A Pathway from the Midbrain to the Striatum is Critical to Multiple Forms of Vocal Learning and Modification in the Songbird

Many of the skills we value most as humans, such as speech and learning to play musical instruments, are learned in the absence of external reinforcement. However, the model systems most commonly used to study motor learning employ learning paradigms in which animals perform behaviors in response to external rewards or punishments. Here I use the zebra finch, an Australian songbird that can learn its song as a juvenile in the absence of external reinforcement as well as modify its song in response to external cues as an adult, to study the circuit mechanisms underlying both internally and externally reinforced forms of learning. Using a combination of intersectional genetic and microdialysis techniques, I show that a striatonigral pathway and its downstream effectors, namely D1-type dopamine receptors, are necessary for both internally reinforced juvenile learning and externally reinforced adult learning, as wells as for song modification in response to social cues or to deafening. In addition, I employ optogenetic stimulation during singing to demonstrate that this striatonigral projection is sufficient to drive learning. Interestingly, I find that neither the striatonigral pathway nor D1-type dopamine receptors are necessary for recovery of pitch after externally driven pitch learning. In all, I establish that a common mechanism underlies both internally and externally reinforced vocal learning.