Propagation of Correlated Activity through Multiple Stages of a Neural Circuit

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Abstract
The timing of spikes can carry information, for instance, when the temporal pattern of firing across neurons results in correlated activity. However, in part because central synapses are unreliable, correlated activity has not been observed to propagate through multiple subsequent stages in neural circuits, although such propagation has frequently been used in theoretical models. Using simultaneous single-unit and multiunit recordings from two or three vocal control nuclei of songbirds, measurement of coherency and time delays, and manipulation of neural activity, we provide evidence here for preserved correlation of activity through multiple steps of the neural circuit for song, including a basal ganglia circuit and its target vocal motor pathway. This suggests that these pathways contain highly functionally interconnected neurons and represent a neural architecture that can preserve information about the timing of firing of groups of neurons. Because the interaction of these song pathways is critical to vocal learning, the preserved correlation of activity may be important to the learning and production of sequenced motor acts and could be a general feature of basal ganglia–cortical interaction.