Understanding the vocal learning basal ganglia circuit in zebra finches: Is there co-release of glutamate from midbrain dopamine neurons terminating in area X?

Abstract

Vocal learning is the process of acquiring and maintaining one of the many complex motor skills that begins to develop from human infancy, during which the brain reliant on auditory input. In this study, zebra finches, a species of songbirds, were used as experimental models to study the underlying neural circuitry that facilitate auditory-guided vocal learning and production of song. After the sensory learning stage and during the sensorimotor learning stage of learning and producing song, zebra finches use their own auditory feedback to approximate their tutor birds’ song as close as they are able to. The avian anterior forebrain pathway, which supports vocal learning, contains a structure called area X (a portion of the avian basal ganglia), which receives dopaminergic input from the ventral tegmental area (VTA). Dopaminergic input from the VTA to area X allows the birds to learn song through reinforcement/trial and error learning using auditory feedback. However, dopamine signaling alone may not be sufficiently rapid or temporally precise to guide changes based on auditory feedback during vocal learning as it is classified as a slow-acting neurotransmitter. It was hypothesized that another fast-acting neurotransmitter, glutamate, may be co-released with dopamine from VTA to area X. Two birds (juvenile and adult) were used to detect the presence of markers for both dopamine and glutamate at the terminal boutons of the neuronal axons extending from VTA to area X. In the juvenile bird, 66% of the axon terminals and in the adult bird, 14% of the axon terminals were labeled with markers of both dopamine and glutamate, suggesting a high possibility of the co-release of both these neurotransmitters from VTA to area X. The juvenile bird also had more double-labeled axon terminals when compared to the adult bird (66% vs. 14%), possibly suggesting that the juvenile bird is at a highly variable stage of learning and therefore requiring more temporally precise reinforcement signaling with the co-release of both dopamine and glutamate.