Presynaptic Depression of Glutamatergic Synaptic Transmission by D1-Like Dopamine Receptor Activation in the Avian Basal Ganglia

Abstract

Vocal behavior in songbirds exemplifies a rich integration of motor, cognitive, and social functions that are shared among vertebrates. As a part of the underlying neural substrate, the song system, the anterior forebrain pathway (AFP) is required for song learning and maintenance. The AFP resembles the mammalian basal ganglia-thalamocortical loop in its macroscopic organization, neuronal intrinsic properties, and microcircuitry. Area X, the first station in the AFP, is a part of the basal ganglia essential for vocal learning. It receives glutamatergic inputs from pallial structures and sends GABAergic outputs to thalamic structures. It also receives dense dopaminergic innervation from the midbrain. The role of this innervation is essentially unknown. Here we provide evidence that dopamine (DA) can modulate the glutamatergic inputs to spiny neurons in area X. In whole-cell voltage-clamp recordings from neurons in brain slices of adult zebra finches, we found that activation of D1-like DA receptors depresses ionotropic glutamatergic synaptic current in area X spiny neurons. This effect is mediated by a presynaptic site of action, mimicked by activation of adenylyl cyclase, and blocked by protein kinase A inhibitor and an adenosine A1 receptor antagonist. These results suggest that, in addition to altering the input-output function of spiny neurons by modulating their excitability, as we have shown previously, DA can directly influence the excitatory inputs to these neurons as well. Thus, DA can exert fine control over information processing through spiny neurons in area X, the dynamics of the AFP output, and ultimately song learning and maintenance.