A neural circuit perspective on brain aromatase

Spool, Jeremy A.; Bergan, Joseph F; Remage‐Healey, Luke

doi:10.1016/j.yfrne.2021.100973

Cited by 16 publications

(10 citation statements)

References 243 publications

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“…But it is generally accepted that the songbird brain has widespread capacity to convert DHEA into aromatizable androgens ( 24 , 81 – 83 ). And neurons in VTA and GCt of passerine and non-passerine birds express the aromatase enzyme ( 84 , 85 ). This makes it reasonable to hypothesize that neuroestrogen levels in VTA and GCt were elevated in DHEA-implanted subjects relative to CON-implanted subjects.…”

Section: Discussionmentioning

confidence: 99%

Dehydroepiandrosterone (DHEA) increases undirected singing behavior and alters dopaminergic regulation of undirected song in non-breeding male European starlings (Sturnus vulgaris)

2023

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IntroductionIt has been proposed that in species that defend territories across multiple life history stages, brain metabolism of adrenal dehydroepiandrosterone (DHEA) regulates aggressive behavior at times when gonadal androgen synthesis is low (i.e. the non-breeding season). To date, a role for DHEA in the regulation of other forms of social behavior that are expressed outside of the context of breeding remains unknown.MethodsIn this experiment, we used the European starling (Sturnus vulgaris) model system to investigate a role for DHEA in the neuroendocrine regulation of singing behavior by males in non-breeding condition. Starling song in a non-breeding context is spontaneous, not directed towards conspecifics, and functions to maintain cohesion of overwintering flocks.ResultsUsing within-subjects design, we found that DHEA implants significantly increase undirected singing behavior by non-breeding condition male starlings. Given that DHEA is known to modulate multiple neurotransmitter systems including dopamine (DA) and DA regulates undirected song, we subsequently used immunohistochemistry for phosphorylated tyrosine hydroxylase (pTH, the active form of the rate-limiting enzyme in DA synthesis) to investigate the effect of DHEA on dopaminergic regulation of singing behavior in a non-breeding context. Pearson correlation analysis revealed a positive linear association between undirected singing behavior and pTH immunoreactivity in the ventral tegmental area and midbrain central gray of DHEA-implanted, but not control-implanted, males.DiscussionTaken together, these data suggest that undirected singing behavior by non-breeding starlings is modulated by effects of DHEA on dopaminergic neurotransmission. More broadly, these data expand the social behavior functions of DHEA beyond territorial aggression to include undirected, affiliative social communication.

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Section: Discussionmentioning

confidence: 99%

Dehydroepiandrosterone (DHEA) increases undirected singing behavior and alters dopaminergic regulation of undirected song in non-breeding male European starlings (Sturnus vulgaris)

2023

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“…Alternatively, the lack of estradiol may have affected BS neurons directly rather than via NS neurons in a way that decreased ASA but not firing rate z-scores or accuracy. A similar proportion of inhibitory GAD1 and CaMKIIa excitatory neurons have been observed to co-express aromatase in the NCM (Spool et al, 2022), but the functional neurophysiology outcomes for the network needs more study.…”

Section: Effects Of Aromatase Inhibition On Neural and Behavioral Aud...mentioning

confidence: 94%

Acute Aromatase Inhibition Impairs Neural and Behavioral Auditory Scene Analysis in Zebra Finches

Fernández-Vargas,

Macedo-Lima,

Remage-Healey

2024

eNeuro

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Auditory perception can be significantly disrupted by noise. To discriminate sounds from noise, auditory scene analysis (ASA) extracts the functionally relevant sounds from acoustic input. The zebra finch communicates in noisy environments. Neurons in their secondary auditory pallial cortex (caudomedial nidopallium; NCM) can encode song from background chorus, or scenes, and this capacity may aid behavioral ASA. Furthermore, song processing is modulated by the rapid synthesis of neuroestrogens when hearing conspecific song. To examine whether neuroestrogens support neural and behavioral ASA in both sexes, we retrodialyzed fadrozole (aromatase inhibitor, FAD) and recordedin vivoawake extracellular NCM responses to songs and scenes. We found that FAD affected neural encoding of songs by decreasing responsiveness and timing reliability in inhibitory (narrow-spiking), but not in excitatory (broad-spiking) neurons. Congruently, FAD decreased neural encoding of songs in scenes for both cell types, particularly in females. Behaviorally, we trained birds using operant conditioning and tested their ability to detect songs in scenes after administering FAD orally or injected bilaterally into NCM. Oral FAD increased response bias and decreased correct rejections in females, but not in males. FAD in NCM did not affect performance. Thus, FAD in the NCM impaired neuronal ASA but that did not lead to behavioral disruption suggesting the existence of resilience or compensatory responses. Moreover, impaired performance after systemic FAD suggests involvement of other aromatase-rich networks outside the auditory pathway in ASA. This work highlights how transient estrogen synthesis disruption can modulate higher-order processing in an animal model of vocal communication.Significance StatementThe ability to extract relevant sounds from a complex acoustic input, or acoustic scene, can decline with age and is often impaired in auditory and neurological disorders. Moreover, hearing decline and speech-in-noise processing have been associated with hormonal changes during perimenopause or menopause in women. However, hormone-dependent hearing impairments are understudied in female animal models. Here, we explore the role of neuroestrogen synthesis in auditory scene analysis (ASA) in a songbird. We found that blocking the synthesis of neuroestrogens with the drug fadrozole (FAD) impaired ASA in auditory neurons. FAD administered orally caused females to decrease correct rejections and respond indiscriminately during behavioral ASA using operant conditioning. These results elucidate potential neural and hormonal mechanisms underlying speech-in-noise impairments in women.

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“…These sensorimotor integrative brain areas may be the inputs and recipients of regulatory information upon the activation of the SBNW, a view articulated recently. 22,76 Notably, in both passerines and rodents, some of these integrative brain areas contain abundant synaptic aromatase. 18,19,20,44 Schlinger et al 22 proposed two hypotheses stemming from the model above.…”

Section: Central Aromatization As a Coordinator Of E 2 -Dependent Beh...mentioning

confidence: 99%

“…Importantly, the SBNW receives inputs from, and projects directly to multiple brain areas critical in regulating the integration of behaviors such as the caudal nidopallium, hippocampus, striatum, and certain song nuclei including the HVC. These sensorimotor integrative brain areas may be the inputs and recipients of regulatory information upon the activation of the SBNW, a view articulated recently 22,76 . Notably, in both passerines and rodents, some of these integrative brain areas contain abundant synaptic aromatase 18,19,20,44 .…”

Section: Central Aromatization As a Coordinator Of E2‐dependent Behaviormentioning

confidence: 99%

Spatial and temporal specificity of neuroestradiol provision in the songbird

Saldanha

2022

J Neuroendocrinology

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Steroid hormones are often synthesized in multiple tissues, affect several different targets, and modulate numerous physiological endpoints. The mechanisms by which this modulation is achieved with temporal and spatial specificity remain unclear. 17β‐estradiol for example, is made in several peripheral tissues and in the brain, where it affects a diverse set of behaviors. How is estradiol delivered to the right target, at the right time, and at the right concentration? In the last two decades, we have learned that aromatase (estrogen‐synthase) can be induced in astrocytes following damage to the brain and is expressed at central synapses. Both mechanisms of estrogen provision confer spatial and temporal specificity on a lipophilic neurohormone with potential access to all cells and tissues. In this review, I trace the progress in our understanding of astrocytic and synaptic aromatization. I discuss the incidence, regulation, and functions of neuroestradiol provision by aromatization, first in astrocytes and then at synapses. Finally, I focus on a relatively novel hypothesis about the role of neuroestradiol in the orchestration of species‐specific behaviors.

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A neural circuit perspective on brain aromatase

Cited by 16 publications

References 243 publications

Dehydroepiandrosterone (DHEA) increases undirected singing behavior and alters dopaminergic regulation of undirected song in non-breeding male European starlings (Sturnus vulgaris)

Dehydroepiandrosterone (DHEA) increases undirected singing behavior and alters dopaminergic regulation of undirected song in non-breeding male European starlings (Sturnus vulgaris)

Acute Aromatase Inhibition Impairs Neural and Behavioral Auditory Scene Analysis in Zebra Finches

Spatial and temporal specificity of neuroestradiol provision in the songbird

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