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

• Authors: Carlos A. Rodriguez-Saltos, Emory University; Susan M. Lyons, University of North Carolina; Keith W. Sockman, University of North Carolina; Donna Maney, Emory University
• Journal Title: JOURNAL OF NEUROENDOCRINOLOGY
• Volume: Volume 30, Number 6
• Publisher: WILEY | 2018-06-01, Pages e12606-e12606
• Type of Work: Article | Post-print: After Peer Review
• Publisher DOI: http://doi.org/10.1111/jne.12606
• Subjects: Biology, Neuroscience
• Keywords: Science & Technology; Life Sciences & Biomedicine; Endocrinology & Metabolism; Neurosciences; Neurosciences & Neurology; catecholamine; dopamine; norepinephrine; serotonin; song; white-throated sparrow; WHITE-THROATED SPARROWS; VOCAL CONTROL NUCLEI; MALE COURTSHIP SONG; MALE ZEBRA FINCHES; GENOMIC RESPONSES; CELL GROUPS; BEHAVIORAL PHENOTYPES; DOPAMINERGIC-NEURONS; INCENTIVE SALIENCE; SOCIAL-BEHAVIOR

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 oestradiol reaches breeding-like levels. This selectivity has been hypothesised to be mediated by the 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. To mediate hormone-dependent selectivity, this release must be (i) selective for song and (ii) modulated by endocrine state. Therefore, in the present study, we addressed both questions by conducting playbacks of song or a control sound to females in a breeding-like or a nonbreeding 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 depended 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; irrespective of whether the birds heard sound or not, turnover of serotonin in the auditory forebrain was higher in a breeding-like state than in a nonbreeding endocrine state. The results of the present study suggest that dopaminergic and serotonergic responses to song and other sounds, as well as serotonergic tone in auditory areas, could be seasonally modulated.