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The Journal of Neuroscience, May 20, 2009, 29(20):6558-6567; doi:10.1523/JNEUROSCI.5571-08.2009

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Behavioral/Systems/Cognitive
Plastic and Stable Electrophysiological Properties of Adult Avian Forebrain Song-Control Neurons across Changing Breeding Conditions

John Meitzen,¹ Adam L. Weaver,² Eliot A. Brenowitz,^3,4 and David J. Perkel^2,3

¹Program in Neurobiology and Behavior and ²Departments of Otolaryngology, ³Biology, and ⁴Psychology, University of Washington, Seattle, Washington 98195

Correspondence should be addressed to John Meitzen at his present address: Department of Neuroscience, University of Minnesota, 6-145 Jackson Hall, 321 Church Street SE, Minneapolis, MN 55455. Email: meitz010{at}umn.edu

Steroid sex hormones drive changes in the nervous system and behavior in many animal taxa, but integrating the former with the latter remains challenging. One useful model system for meeting this challenge is seasonally breeding songbirds. In these species, plasma testosterone levels rise and fall across the seasons, altering song behavior and causing dramatic growth and regression of the song-control system, a discrete set of nuclei that control song behavior. Whereas the cellular mechanisms underlying changes in nucleus volume have been studied as a model for neural growth and degeneration, it is unknown whether these changes in neural structure are accompanied by changes in electrophysiological properties other than spontaneous firing rate. Here we test the hypothesis that passive and active neuronal properties in the forebrain song-control nuclei HVC and RA change across breeding conditions. We exposed adult male Gambel's white-crowned sparrows to either short-day photoperiod or long-day photoperiod and systemic testosterone to simulate nonbreeding and breeding conditions, respectively. We made whole-cell recordings from RA and HVC neurons in acute brain slices. We found that RA projection neuron membrane time constant, capacitance, and evoked and spontaneous firing rates were all increased in the breeding condition; the measured electrophysiological properties of HVC interneurons and projection neurons were stable across breeding conditions. This combination of plastic and stable intrinsic properties could directly impact the song-control system's motor control across seasons, underlying changes in song stereotypy. These results provide a valuable framework for integrating how steroid hormones modulate cellular physiology to change behavior.

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Received Nov. 20, 2008; revised April 9, 2009; accepted April 16, 2009.

Correspondence should be addressed to John Meitzen at his present address: Department of Neuroscience, University of Minnesota, 6-145 Jackson Hall, 321 Church Street SE, Minneapolis, MN 55455. Email: meitz010{at}umn.edu

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