Estradiol modulates neural response to conspecific and heterospecific song in female house sparrows: An in vivo positron emission tomography study

Abstract

Although there is growing evidence that estradiol modulates female perception of male sexual signals, relatively little research has focused on female auditory processing. We used in vivo 18F-fluorodeoxyglucose (18F-FDG) positron emission tomography (PET) imaging to examine the neuronal effects of estradiol and conspecific song in female house sparrows (Passer domesticus). We assessed brain glucose metabolism, a measure of neuronal activity, in females with empty implants, estradiol implants, and empty implants ~1 month after estradiol implant removal. Females were exposed to conspecific or heterospecific songs immediately prior to imaging. The activity of brain regions involved in auditory perception did not differ between females with empty implants exposed to conspecific vs. heterospecific song, but neuronal activity was significantly reduced in females with estradiol implants exposed to heterospecific song. Furthermore, our within-individual design revealed that changes in brain activity due to high estradiol were actually greater several weeks after peak hormone exposure. Overall, this study demonstrates that PET imaging is a powerful tool for assessing large-scale changes in brain activity in living songbirds, and suggests that after breeding is done, specific environmental and physiological cues are necessary for estradiol-stimulated females to lose the selectivity they display in neural response to conspecific song.

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

“…In a variety of seasonally breeding songbirds, auditory responses to conspecific song are in fact greater during the breeding season. Such changes have been demonstrated using auditory evoked potentials, neurophysiological recording, in vivo imaging and the expression of immediate early genes . There is thus good evidence that the auditory system becomes more attuned to conspecific song when a bird enters a breeding‐like endocrine state.…”

“…Such changes have been demonstrated using auditory evoked potentials, 8,9 neurophysiological recording, 10,11 in vivo imaging [12][13][14] and the expression of immediate early genes. 5,15 There is thus good evidence that the auditory system becomes more attuned to conspecific song when a bird enters a breeding-like endocrine state.…”

Neural mechanisms of auditory species recognition in birds

“…Regarding real‐time in situ neuronal responses, for example, studies using electrophysiology have recorded conspecific‐selective firing patterns from individual neurons at the microsecond scale (Chew et al , ; Chew, Vicario, & Nottebohm, ; Woolley, Hauber, & Theunissen, ; Hauber et al , ; Smulders & Jarvis, ). Brain imaging, such as functional magnetic resonance imaging (fMRI) and positron emission tomography (PET), also showed that conspecific sounds evoke greater neural activity at a stimulus‐length (several seconds) time scale, when compared to sequential playbacks of heterospecific sounds (Poirier et al , ; Louder et al , ; Lattin, Stabile, & Carson, ). Furthermore, genes that are induced in response to regulatory signals from external stimuli, known as immediate early genes (IEGs), can be used to infer the intensity of neural activity across a longer time scale of continued exposure to stimuli, ranging from minutes to hours.…”

“…Studies using electrophysiology have recorded conspecific‐selective greater firing for neurons within Field L (Woolley et al , ; Hauber et al , ), as well as in the NCM and CMM (Chew et al , , ; Smulders & Jarvis, ). fMRI and PET showed that conspecific sounds evoke greater neural activity when compared to heterospecific sounds (Poirier et al , ; Louder et al , ; Lattin et al , ). Furthermore, the numbers of neurons that express IEGs such as ZENK , c‐FOS and Arc selectively increase in response to conspecific versus heterospecific auditory stimuli in the NCM and CMM of birds (Mello et al , ; Bailey & Wade, ; Velho et al , ).…”

“…Similarly, the steroid hormone oestradiol serves a necessary role in auditory processing and memory formation of conspecific, but not heterospecific songs (Yoder, Lu, & Vicario, 2012;Yoder et al, 2015). Oestradiol increases spike rates for conspecific, but not heterospecific, song exposure in male zebra finches (Remage-Healey et al, 2010) and induces detectable differences in conspecific-selective brain responses in female house sparrow Passer domesticus (Lattin et al, 2017). By targeting brain regions in the social decision-making network (O'Connell & Hofmann, 2012), as well as sensory regions, these hormones and neuromodulators transform passive listeners into active responders that are able to minimize errors in their responses to signals.…”