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The Journal of Neuroscience, December 3, 2008, 28(49):13232-13247; doi:10.1523/JNEUROSCI.2250-08.2008

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Behavioral/Systems/Cognitive
Neurons in a Forebrain Nucleus Required for Vocal Plasticity Rapidly Switch between Precise Firing and Variable Bursting Depending on Social Context

Mimi H. Kao,¹ Brian D. Wright,^1,2  and Allison J. Doupe^1,2

¹Keck Center for Integrative Neuroscience, Departments of Physiology and Psychiatry, and ²Sloan–Swartz Center for Theoretical Neurobiology, University of California, San Francisco, San Francisco, California 94143-0444

Correspondence should be addressed to Mimi H. Kao, Department of Physiology, Box 0444, 513 Parnassus Avenue, University of California, San Francisco, San Francisco, CA 94143-0444. Email: mimi{at}phy.ucsf.edu

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.

Key words: basal ganglia; vocal learning; burst firing; spike count variability; zebra finch; LMAN

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Received May 18, 2008; revised Aug. 29, 2008; accepted Oct. 16, 2008.

Correspondence should be addressed to Mimi H. Kao, Department of Physiology, Box 0444, 513 Parnassus Avenue, University of California, San Francisco, San Francisco, CA 94143-0444. Email: mimi{at}phy.ucsf.edu

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