Biological Rhythms Of Vocal Behavior In Fish: Hormonal, Neuronal, And Genetic Mechanisms

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Abstract
Vocalization is a prominent feature of social communication among vertebrates. For energetically costly vocal-acoustic courtship behaviors, timing across seconds, days, and seasons is critical and can enhance sender-receiver coupling, reproductive success, and reproductive isolation. Many species of fish produce sound to communicate in different social contexts, such as courtship. Here, I investigated hormonal, neuronal, and genetic mechanisms underlying the timing of vocal behavior in the plainfin midshipman fish (Porichthys notatus), across timescales spanning milliseconds to seasons. I demonstrated that the robust daily rhythm of midshipman male's nocturnal courtship vocalization is under endogenous, circadian control. Exogenous delivery of melatonin, the nocturnal hormone in vertebrates, rescued the inhibition of courtship vocalization under constant light, which abolishes endogenous melatonin production. Melatonin also rescued the inhibition of neural excitability in the midshipman vocal network under constant light. Furthermore, melatonin receptor 1b mRNA was shown to be expressed in neuroendocrine, sensory (including auditory) and vocal motor pathways. Together, these results support the hypothesis that melatonin plays a central role in timing the nocturnal midshipman courtship vocalization by acting on specific neural pathways. Finally, I used RNA-sequencing to characterize the transcriptome of the vocal motor nucleus (VMN), the final node of the hindbrain vocal pattern generator that directly determines vocalization temporal characteristics such as duration and frequency. I identified a suite of candidate genes, including ion channels, for shaping the precise and synchronous firing of VMN motor neurons. Many candidate genes showed day-night and seasonal changes in expression. Furthermore, enrichment and high expression of cellular respiration genes in VMN compared to the surrounding hindbrain tissue likely enable midshipman courtship calls that can last up to hours, and suggest that the neural patterning of vocal behavior is energetically costly. Finally, high expression of several antioxidant genes in VMN suggested a high capacity for combating cellular respiration-generated oxidative stress, which may also enable long duration courtship call production. Altogether, these chapters identify mechanisms underlying the timing of vocalization that may be applicable across other lineages of vertebrates, including birds and mammals, which exhibit rhythmic production of vocalization across multiple timescales.
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2016-02-01
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Melatonin; Vocalization; Biological rhythms
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Bass,Andrew Howard
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Fetcho,Joseph R.
Deitcher,David Lawrence
Place,Ned J.
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Neurobiology
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Ph. D., Neurobiology
Degree Level
Doctor of Philosophy
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Government Document
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dissertation or thesis
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