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Steroid hormones act transsynaptically within the forebrain to regulate neuronal phenotype and song stereotypy

TitleSteroid hormones act transsynaptically within the forebrain to regulate neuronal phenotype and song stereotypy
Publication TypeJournal Article
Year of Publication2007
AuthorsMeitzen J, Moore IT, Lent K, Brenowitz EA, Perkel DJ
JournalJ Neurosci
Date Published2007
ISBN Number1529-2401 (Electronic)0270-6474 (Linking)
KeywordsAnalysis of Variance, Animals, Male, Gonadal Steroid Hormones/*administration & dosage/blood, Membrane Potentials/drug effects/physiology/radiation effects, Patch-Clamp Techniques/methods, Photoperiod, Neuronal Plasticity/*drug effects/physiology, Vocalization, Animal/*drug effects/physiology, Radioimmunoassay/methods, Prosencephalon/*drug effects, Sparrows/physiology, Stereotyped Behavior/*drug effects/physiology, Universities

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.