Sound-induced monoaminergic turnover in the auditory forebrain depends on endocrine state in a seasonally-breeding songbird.

Abstract

Sensory responses to courtship signals can be altered by reproductive hormones. In seasonally-breeding female songbirds, for example, sound-induced immediate early gene expression in the auditory pathway is selective for male song over behaviourally irrelevant sounds only when plasma estradiol reaches breeding-like levels. This selectivity has been hypothesized to be mediated by release of monoaminergic neuromodulators in the auditory pathway. We previously showed that in oestrogen-primed female white-throated sparrows, exposure to male song induced dopamine and serotonin release in auditory regions. In order to mediate hormone-dependent selectivity, this release must be (1) selective for song and (2) modulated by endocrine state. Therefore, in the current study we addressed both questions by conducting playbacks of song or a control sound to females in a breeding-like or non-breeding endocrine state. We then used high performance liquid chromatography to measure turnover of dopamine, norepinephrine, and serotonin in the auditory midbrain and forebrain. We found that sound-induced turnover of dopamine and serotonin did in fact depend on endocrine state; hearing sound increased turnover in the auditory forebrain only in the birds in a breeding-like endocrine state. Contrary to our expectations, these increases occurred in response to either song or artificial tones; in other words, they were not selective for song. The selectivity of sound-induced monoamine release was thus strikingly different from that of immediate early gene responses described in previous studies. We did, however, find that constitutive monoamine release was altered by endocrine state; whether the birds heard sound or not, turnover of serotonin in the auditory forebrain was higher in a breeding-like state than in a non-breeding endocrine state. Our results suggest that dopaminergic and serotonergic responses to song and other sounds, as well as serotonergic tone in auditory areas, could be seasonally modulated. This article is protected by copyright. All rights reserved.