Dissertations, Theses, and Capstone Projects

Date of Degree

9-2019

Document Type

Dissertation

Degree Name

Ph.D.

Program

Psychology

Advisor

Paul M. Forlano

Committee Members

Christopher B. Braun

Thomas Preuss

Adrian Rodriguez-Contreras

Joseph A. Sisneros

Subject Categories

Biological Psychology | Neuroscience and Neurobiology | Systems Neuroscience

Keywords

dopamine, auditory, inner ear, neuromodulation, acoustic communication, neuroethology

Abstract

The neuromodulator dopamine is considered essential for coordinating the internal motivational state of an organism with appropriate behavioral responses to stimuli in the external environment. This could be accomplished by modifying the function of neural circuits involved in sensory processing such that they are “tuned in” and optimally sensitive to important stimuli during critical time windows. While dopamine modulation of auditory processing has been studied in the central nervous system, neuromodulation can also occur outside the brain, in the inner ear. The majority of investigations of dopamine in the ear are conducted using rodents and focus on its role in preventing noise induced trauma to the inner ear. However, few studies have considered other functions and a natural behavioral role of dopamine in the inner ear of any vertebrate remains unknown. This dissertation examines the structure and function of dopamine input to the inner ear of the plainfin midshipman, a vocal fish and an exemplar organism for the study of neural mechanisms of social-acoustic communication.

Previous work in our lab suggested that seasonal, reproductive state-related changes to dopamine in the brain and inner ear could be responsible, in part, for a well-documented seasonal change to auditory sensitivity that facilities the detection of male courtship calls during the summer breeding season. Chapter 2 expands on this work by characterizing the synaptic connections between dopamine neurons in the forebrain and the main organ of hearing in the midshipman inner ear, the saccule. It confirms that the same dopamine nucleus that projects to the saccule also send inputs to a cholinergic nucleus in the hindbrain that has efferent projections to the saccule. We found that neurons in this nucleus have dopamine terminals directly synapsing onto both their somata and dendrites. In the saccule, dopamine terminals do not form traditional synapses, suggesting a role for paracrine release, and the potential for dopamine to affect signal transduction and transmission at multiple points within the inner ear. Together this work shows that a single dopaminergic cell group in the forebrain can exert direct modulation on peripheral auditory processing within the saccule and indirect effects through modulation of the cholinergic auditory efferent hindbrain.

Chapter 3 examines the effect of dopamine on sound-evoked activity in the saccule. We found that dopamine reduces the sensitivity of the saccule in both summer reproductive and winter non-reproductive females. Using pharmacology and quantitative analysis of receptor transcript expression, we determined this inhibition is produced via a D2 receptor which is upregulated in winter females. Expression of this dopamine receptor subtype (D2a) is negatively correlated with individual baseline saccular auditory sensitivity, suggesting an important role for inner ear dopamine in modulating the sensitivity to social-acoustic signals.

Chapter 4 examines the effect of hearing a male courtship call on dopamine release in the inner ear and cholinergic auditory efferent hindbrain of females in the summer. Using an activity marker for the synthesis and release of dopamine, we found that exposure to a noise stimulus produces no change relative to ambient controls. Exposure to recordings of the male call however reduce the synthesis and release of dopamine in the cholinergic hindbrain and the saccule. Therefore, the shorter time-scale dynamics of dopamine release within the peripheral and efferent auditory system are responsive to social-acoustic signals. The reduction of dopamine release, which we found in chapter 2 to inhibit saccular sensitivity, likely results in enhanced sensitivity during the detection and localization of male mates.

Chapter 5 describes the seasonal, reproductive state-related changes of the dopaminergic auditory efferent system at the ultrastructural level. Females in reproductive condition during the summer have fewer dopamine terminals in the saccule. These terminals are smaller in volume and less likely to directly contact a hair cell in summer females as compared to winter females. In the cholinergic auditory efferent hindbrain, the neurons of summer females have more direct dopamine terminals contacting somata and dendrites. These results confirm previously reported seasonal changes observed using fluorescence microscopy. Taken together, our results suggest that the reduction of dopaminergic inhibition, both via seasonal changes to innervation and receptor expression, and reduced dopamine release in response to hearing the male courtship call, is an important contributing mechanism that modulates female peripheral auditory sensitivity during the breeding season, improving the ability to detect and find male mates. This work provides support for a novel biological function for dopamine as a modulator of social-acoustic signals in the inner ear, extending its role from the central nervous system out to the auditory periphery.

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