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Dopaminergic modulation of basal ganglia output through coupled excitation–inhibition

Significance Trial-and-error learning requires variation in successive trials, but the source of such variability is unknown. We describe a unique striatal glutamatergic neuron in the zebra finch. This neuron exerts a potent, dopamine-regulated action on pallidal output neurons that modifies neuronal firing statistics in the circuit known to contribute to vocal variability. A simple model reveals how this microcircuit could be influenced by social context and striatal dopamine to switch between firing patterns that modify song variability essential for vocal learning. Learning and maintenance of skilled movements require exploration of motor space and selection of appropriate actions. Vocal learning and social context-dependent plasticity in songbirds depend on a basal ganglia circuit, which actively generates vocal variability. Dopamine in the basal ganglia reduces trial-to-trial neural variability when the bird engages in courtship song. Here, we present evidence for a unique, tonically active, excitatory interneuron in the songbird basal ganglia that makes strong synaptic connections onto output pallidal neurons, often linked in time with inhibitory events. Dopamine receptor activity modulates the coupling of these excitatory and inhibitory events in vitro, which results in a dynamic change in the synchrony of a modeled population of basal ganglia output neurons receiving excitatory and inhibitory inputs. The excitatory interneuron thus serves as one biophysical mechanism for the introduction or modulation of neural variability in this circuit.