Anatomical and physiological characterization of the dopaminergic input to a basal ganglia circuit required for vocal learning in songbirds.

摘要

Sensory feedback during performance of a behavior guides motor learning, and the dopaminergic input to the basal ganglia might contribute to this process. Vocal learning in songbirds requires auditory feedback and an anatomically discrete and functionally devoted basal ganglia circuit called the anterior forebrain pathway (AFP). Like the striatum of mammals, the striatal portion of the AFP, Area X, receives dense dopaminergic input from the substantia nigra pars compacta (SNc) and ventral tegmental area (VTA). Dopamine is critical for normal basal ganglia function, but the role of dopamine in the AFP during song learning is not known. My goals were to determine the sources of anatomical input to dopaminergic neurons in songbirds and to measure dopamine signals in Area X during singing. Using intracellular recordings and voltammetry in brain slices, I demonstrated that the physiological properties of dopaminergic neurons and the regulation of dopamine release and uptake are similar in mammals and songbirds. However, unlike the mammalian striatum and other striatal regions in songbirds, Area X does not project directly to the SNc/VTA. Area X nonetheless provides the only connection between song-control regions and dopaminergic neurons via a projection to the ventral pallidum (VP), which projects to the SNc/VTA. This pathway differs in several ways from mammalian basal ganglia circuitry, but in the avian basal ganglia is not unique to Area X. Auditory responses in urethane-anesthetized zebra finches revealed that Area X can disinhibit dopaminergic neurons by inhibiting spontaneously active neurons in VP. Preliminary recordings of dopamine release in behaving zebra finches are consistent with singing-related dopamine signals in Area X, but the sensitivity of these measurements must increase to enable further characterization of the information dopaminergic neurons transmit to the AFP.