Hormone-Dependent Modulation of Auditory Processing and Selectivity in a Seasonally Breeding Songbird Open Access

Matragrano, Lisa Leilani (2012)

Permanent URL: https://etd.library.emory.edu/concern/etds/pr76f437g?locale=en
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Abstract

Behavioral responses to sociosexual signals change significantly according to gonadal hormone levels. These changes may be partially explained by hormone-dependent modulation of sensory processing, which has been described in seasonally breeding songbirds. In female white-throated sparrows, sound-induced expression of immediate early genes (IEGs) in auditory areas is selective for song over behaviorally irrelevant tones only when plasma estradiol reaches breeding-typical levels. Here, I explored the neurochemical mechanisms underlying steroid-dependent plasticity in the auditory system in this species. I hypothesized that the effects of estradiol in sensory areas are mediated by monoamine systems, which are sensitive to gonadal steroids and involved in sensory processing and selective attention. Specifically, I tested whether seasonal changes in plasma levels of gonadal steroids modify monoaminergic activity in auditory areas and whether those changes are associated with changes in neural responses to behaviorally relevant stimuli. Estradiol treatment of females increased catecholaminergic and serotonergic innervation of the same areas of the auditory system in which estradiol promotes selective IEG responses, and increased levels of norepinephrine and a serotonin metabolite in the auditory forebrain. This result is consistent with the hypothesis that estradiol primes the auditory system via monoamines. In order to test whether monoaminergic influences on auditory responses may be due to sound-induced release, I examined whether exposure to song playback causes rapid changes in monoaminergic activity. I detected changes in monoamine synthesis and release in the auditory forebrain of estrogen-primed females after as little as 15 minutes of song, demonstrating that the monoaminergic cells innervating this region can respond rapidly to this sound and that they may play an active role in the modulation of auditory responses. Finally, I tested whether seasonal changes in gonadal steroid levels may affect auditory responses in males of the same species. Similar to estradiol in females, testosterone induced selective IEG responses in the auditory forebrain in males. Unlike estradiol, which increased monoaminergic innervation of auditory areas in females, testosterone decreased it in males. These studies show that gonadal hormones alter the selectivity of auditory IEG responses and may modulate monoaminergic activity in the auditory system in both sexes.

Table of Contents

Table of Contents
Chapter 1: General Introduction...1

1.1 The role of hormones in sensory processing in vertebrates...2
1.2 Seasonally breeding songbirds as a model system...4
1.3 Hormonal effects on the auditory system in songbirds...8
1.4 Hormonal effects on monoamines and the role of monoamines in auditory selectivity...10
1.5 Monoaminergic influences on auditory responses...16
1.6 Conclusions and dissertation goals...18

Chapter 2: Estradiol-dependent monoaminergic innervation of auditory areas in the female white-throated sparrow...20

2.1 Abstract...21
2.2 Introduction...22
2.3 Methods...26
2.4 Results...40
2.5 Discussion...45

Chapter 3: Rapid sound-induced changes in catecholamine synthesis and release in auditory areas in the female white-throated sparrow...62

3.1 Abstract...63
3.2 Introduction...64
3.3 Methods...67
3.4 Results...79
3.5 Discussion...81

Chapter 4: Testosterone modulates genomic responses to song and monoaminergic innervation of auditory areas in the male white-throated sparrow...90

4.1 Abstract...91
4.2 Introduction...92
4.3 Methods...95
4.4 Results...104
4.5 Discussion...106

Chapter 5: Conclusions...117

5.1 Summary of key findings...118
5.2 Effects of E2 on sound-induced auditory responses in females: Conclusions & Implications...119
5.3 Effects of E2 on sound-induced responses in females: Future directions...123
5.4 Effects of testosterone on auditory ZENK responses in males: Conclusions & Implications...127
5.5 Effects of testosterone on auditory ZENK responses in males: Future directions...128
5.6 Final conclusions...129

References…………………………………………………………………………….. 132

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