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The Journal of Neuroscience, October 31, 2007, 27(44):12045-12057; doi:10.1523/JNEUROSCI.3289-07.2007

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Behavioral/Systems/Cognitive
Steroid Hormones Act Transsynaptically within the Forebrain to Regulate Neuronal Phenotype and Song Stereotypy

John Meitzen,¹ Ignacio T. Moore,⁵ Karin Lent,² Eliot A. Brenowitz,^2,3 and David J. Perkel^3,4

¹Graduate Program in Neurobiology and Behavior, ²Department of Psychology, ³Department of Biology, and ⁴Department of Otolaryngology, University of Washington, Seattle, Washington 98195, and ⁵Department of Biological Sciences, Virginia Tech, Blacksburg, Virginia 24061

Correspondence should be addressed to John Meitzen, Department of Otolaryngology, University of Washington, Box 356515, Seattle, WA 98195. Email: jmeitzen{at}u.washington.edu

Steroid sex hormones induce dramatic seasonal changes in reproductive related behaviors and their underlying neural substrates in seasonally breeding vertebrates. For example, in adult white-crowned sparrows, increased Spring photoperiod raises circulating testosterone, causing morphological and electrophysiological changes in song-control nuclei, which modify song behavior for the breeding season. We investigated how photoperiod and steroid hormones induce these changes in morphology, electrophysiology, and behavior. Neurons in a song premotor nucleus, the robust nucleus of the arcopallium (RA), show increased intrinsic spontaneous firing rate and soma size when birds are in breeding condition. Using combinations of systemic and unilateral local intracerebral hormonal manipulations, we show that long-day photoperiod accelerates the effects of systemic testosterone on RA neurons via the estradiol-synthesizing enzyme aromatase (CYP19A1); these changes require inputs from the afferent song control nucleus HVC (used as a proper name) and steroid receptor activation within HVC; local coactivation of androgen and estrogen receptors (ARs and ERs, respectively) within HVC, but not RA, is sufficient to cause neuronal changes in RA; activation of ARs in RA is also permissive. Using bilateral local intracerebral hormone-receptor blockade, we found that ARs and ERs in the song-control nucleus HVC mediate systemic testosterone-induced changes in song stereotypy but not rate. This novel transsynaptic effect of gonadal steroids on activity and morphology of RA neurons is part of a concerted change in key premotor nuclei, enabling stereotyped song.

Key words: androgen; estrogen; testosterone; electrophysiology; birdsong; seasonal plasticity

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Received July 19, 2007; revised Sept. 18, 2007; accepted Sept. 20, 2007.

Correspondence should be addressed to John Meitzen, Department of Otolaryngology, University of Washington, Box 356515, Seattle, WA 98195. Email: jmeitzen{at}u.washington.edu

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				A. M. Wissman and E. A. Brenowitz The Role of Neurotrophins in the Seasonal-Like Growth of the Avian Song Control System J. Neurosci., May 20, 2009; 29(20): 6461 - 6471. [Abstract] [Full Text] [PDF]

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