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Logo of nihpaAbout Author manuscriptsSubmit a manuscriptNIH Public Access; Author Manuscript; Accepted for publication in peer reviewed journal;
J Neurosci. Author manuscript; available in PMC Jan 17, 2011.
Published in final edited form as:
PMCID: PMC3022006
NIHMSID: NIHMS82319

Neurons in a forebrain nucleus required for vocal plasticity rapidly switch between precise firing and variable bursting depending on social context

Abstract

Song is a learned vocal behavior influenced by social interactions. Prior work has suggested that the anterior forebrain pathway (AFP), a specialized pallial–basal ganglia circuit critical for vocal plasticity, mediates the influence of social signals on song. Here, we investigate the signals the AFP sends to song motor areas and their dependence on social context by characterizing singing-related activity of single neurons in the AFP output nucleus LMAN (lateral magnocellular nucleus of the anterior nidopallium). We show that interaction with females causes marked, real-time changes in firing properties of individual LMAN neurons. When males sing to females (`directed'), LMAN neurons exhibit reliable firing of single spikes precisely locked to song. In contrast, when males sing alone (`undirected'), the same LMAN neurons exhibit prominent burst firing and trial-by-trial variability. Burst structure and timing vary substantially across repeated undirected trials. Despite context-dependent differences in firing statistics, the average pattern of song-locked firing for an individual neuron is similar across behavioral contexts, suggesting a common underlying signal. Different LMAN neurons in the same bird, however, exhibit distinct firing patterns, suggesting that subsets of neurons jointly encode song features. Together, our findings demonstrate that behavioral interactions reversibly transform the signaling mode of LMAN neurons. Such changes may contribute to rapid switching of motor activity between variable and precise states. More generally, our results suggest that pallial–basal ganglia circuits contribute to motor learning and production through multiple mechanisms: patterned signals could guide changes in motor output while state-dependent variability could subserve motor exploration.

Keywords: basal ganglia, vocal learning, burst firing, spike count variability, zebra finch, LMAN
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