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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.

SUBMITTER: Rodriguez-Saltos CA

PROVIDER: S-EPMC6365208 | biostudies-literature | 2018 May

REPOSITORIES: biostudies-literature

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

Rodríguez-Saltos Carlos A CA Lyons Susan M SM Sockman Keith W KW Maney Donna L DL

Journal of neuroendocrinology 20180508

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 ...[more]

PMID: 29738608

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Project description:In many organisms, food availability is a proximate cue that synchronizes seasonal development of the reproductive system with optimal environmental conditions. Growth of the gonads and secondary sexual characteristics is orchestrated by the hypothalamic-pituitary-gonadal (HPG) axis. However, our understanding of the physiological mechanisms by which food availability modulates activity of the HPG axis is limited.It is thought that many factors, including energetic status, modulate seasonal reproductive activation. We tested the hypothesis that food availability modulates the activity of the HPG axis in a songbird. Specifically, we food-restricted captive adult male Abert's Towhees Melozone aberti for 2 or 4 weeks during photoinduced reproductive development. A third group (control) received ad libitum food throughout. We measured multiple aspects of the reproductive system including endocrine activity of all three levels of the HPG axis [i.e. hypothalamic gonadotropin-releasing hormone-I (GnRH-I), plasma luteinizing hormone (LH) and testosterone (T)], and gonad morphology. Furthermore, because gonadotropin-inhibitory hormone (GnIH) and neuropeptide Y (NPY; a potent orexigenic peptide) potentially integrate information on food availability into seasonal reproductive development, we also measured the brain levels of these peptides.At the hypothalamic level, we detected no effect of food restriction on immunoreactive (ir) GnRH-I, but the duration of food restriction was inversely related to the size of ir-GnIH perikarya. Furthermore, the number of ir-NPY cells was higher in food-restricted than control birds. Food restriction did not influence photoinduced testicular growth, but decreased plasma LH and T, and width of the cloacal protuberance, an androgen-sensitive secondary sexual characteristic. Returning birds to ad libitum food availability had no effect on plasma LH or T, but caused the cloacal protuberance to rapidly increase in size to that of ad libitum-fed birds.Our results support the tenet that food availability modulates photoinduced reproductive activation. However, they also suggest that this modulation is complex and depends upon the level of the HPG axis considered. At the hypothalamic level, our results are consistent with a role for the GnIH and NPY systems in integrating information on energetic status. There also appears to be a role for endocrine function at the anterior pituitary gland and testicular levels in modulating reproductive development in the light of energetic status and independently of testicular growth.

Project description:Deviants are stimuli that violate one's prediction about the incoming stimuli. Studying deviance detection helps us understand how nervous system learns temporal patterns between stimuli and forms prediction about the future. Detecting deviant stimuli is also critical for animals' survival in the natural environment filled with complex sounds and patterns. Using natural songbird vocalizations as stimuli, we recorded multi-unit and single-unit activity from the zebra finch auditory forebrain while presenting rare repeated stimuli after regular alternating stimuli (alternating oddball experiment) or rare deviant among multiple different common stimuli (context oddball experiment). The alternating oddball experiment showed that neurons were sensitive to rare repetitions in regular alternations. In the absence of expectation, repetition suppresses neural responses to the 2nd stimulus in the repetition. When repetition violates expectation, neural responses to the 2nd stimulus in the repetition were stronger than expected. The context oddball experiment showed that a stimulus elicits stronger neural responses when it is presented infrequently as a deviant among multiple common stimuli. As the acoustic differences between deviant and common stimuli increase, the response enhancement also increases. These results together showed that neural encoding of a stimulus depends not only on the acoustic features of the stimulus but also on the preceding stimuli and the transition patterns between them. These results also imply that the classical oddball effect may result from a combination of repetition suppression and deviance enhancement. Classification analyses showed that the difficulties in decoding the stimulus responsible for the neural responses differed for deviants in different experimental conditions. These findings suggest that learning transition patterns and detecting deviants in natural sequences may depend on a hierarchy of neural mechanisms, which may be involved in more complex forms of auditory processing that depend on the transition patterns between stimuli, such as speech processing.

Dataset Information

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

Publications

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

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