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Author ORCID Identifier

0000-0003-2960-3756

Document Type

Open Access Dissertation

Degree Name

Doctor of Philosophy (PhD)

Degree Program

Neuroscience and Behavior

Year Degree Awarded

2019

Month Degree Awarded

May

First Advisor

Luke Remage-Healey

Second Advisor

Jeffrey Podos

Third Advisor

Joseph Bergan

Fourth Advisor

Agnès Lacreuse

Subject Categories

Behavioral Neurobiology

Abstract

Birdsong, as with human speech, is learned during an age- and experience-dependent sensitive period early in life. Songbirds must first memorize their parents’ song during a sensory phase, then refine their own burgeoning vocalizations to match the auditory memory of their parents’ song during a sensorimotor phase. While the error-correction aspect of the sensorimotor phase of song learning is comparatively well understood, it is largely unknown how auditory memories are formed and how auditory processing may change across development to facilitate song memorization. The songbird caudomedial nidopallium (NCM) is a brain region that encodes complex communication signals like song and is rich in aromatase (enzyme necessary for converting precursor androgens to estrogens) and estrogen receptors. In adults, acute estrogen signaling enhances auditory encoding, suggesting that one role for 17β-estradiol (E2) in NCM during development may be to enhance auditory processing and facilitate auditory memorization. Moreover, in the hippocampus of rodents, birds, and nonhuman primates, local E2 acts to enhance post-training memory consolidation. As such, I set out to determine whether this role for E2 in auditory processing and memorization occurs within the auditory cortex of juvenile songbirds. I tested this hypothesis across several experiments: I first tested how local E2 administration in NCM modulated auditory processing in developing songbirds. Next, I explored how changes in developing neural architecture and aromatase expression are aligned with distinct song learning phases. I then tested how global and local aromatase inhibition following song learning sessions impacted motor production, vocal learning, and neurophysiology in developing songbirds. Finally, using a stimulus-specific adaptation paradigm, I determined whether findings in juvenile songbirds extended to adults. Specifically, I locally blocked local E2 synthesis in NCM immediately following song exposure and subsequently measured neural recognition of the exposed song. My results showed that sensory coding is substantially enhanced in the NCM of sensory-aged birds compared to song-producing (sensorimotor-aged) juvenile birds, and that E2 exerts an age- and hemisphere-dependent effect on modulation of auditory processing. I also found that cell density in NCM peaks in sensory-aged birds, and is overall higher in dorsal vs. ventral NCM, but that aromatase and parvalbumin expression remain high and constant across development; no hemispheric differences for cell density or expression were found. Further, I found that neither circulating nor locally-derived E2 are required for tutor song memorization in development and adulthood; however, estrogen synthesis blockade can impair song production in developing birds and can also transform the lasting neural representations of autogenous and tutor song in adulthood. Taken together, this dissertation provides new insights into the pleiotropic effects of rapid steroid signaling and synthesis within the auditory cortex of developing male songbirds with implications for communication processing and sensorimotor learning.

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