Effects of castration and testosterone treatment on the activity of testosterone‐metabolizing enzymes in the brain of male and female zebra finches

Vockel, A.; Pröve, Ekkehard; Balthazart, Jacques

doi:10.1002/neu.480210514

Cited by 91 publications

(55 citation statements)

References 59 publications

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“…Seasonal changes in AROM expression or activity in temperate birds might be modulated by the strong seasonal fluctuations in gonadal T secretion. In several bird species it has been shown that T up-regulates AROM activity and its expression in the preoptic area and anterior hypothalamus (Steimer and Hutchison, 1981;Schumacher and Balthazart, 1986;Vockel et al, 1990). The lack of seasonal changes in AROM expression despite the seasonal fluctuations in plasma T concentrations in male spotted antbirds suggests that in this species, AROM expression might be dissociated from circulating T. This might be an adaptive mechanism because it differs from what has been found in most studies on temperate birds.…”

Section: Ar Era and Arom Expression In Pommentioning

confidence: 80%

Low sex steroids, high steroid receptors: Increasing the sensitivity of the nonreproductive brain

Canoine

Fusani

Schlinger

et al. 2006

Developmental Neurobiology

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Male aggressive behavior is generally regulated by testosterone (T). In most temperate breeding males, aggressive behavior is only expressed during the reproductive period. At this time circulating T concentrations, brain steroid receptors, and steroid metabolic enzymes are elevated in many species relative to the nonreproductive period. Many tropical birds, however, display aggressive behavior both during the breeding and the nonbreeding season, but plasma levels of T can remain low throughout the year and show little seasonal fluctuation. Studies on the year-round territorial spotted antbird (Hylophylax n. naevioides) suggest that T nevertheless regulates aggressive behavior in both the breeding and nonbreeding season. We hypothesize that to regulate aggressive behaviors during the nonbreeding season, when T is at its minimum, male spotted antbirds increase brain sensitivity to steroids. This can be achieved by locally up-regulating androgen receptors (ARs), estrogen receptors (ERs), or the enzyme aromatase (AROM) that converts T into estradiol. We therefore compared mRNA expression of AR, ERa, and AROM in freeliving male spotted antbirds across reproductive and nonreproductive seasons in two brain regions known to regulate both reproductive and aggressive behaviors. mRNA expression of ER in the preoptic area and AR in the nucleus taeniae were elevated in male spotted antbirds during the nonbreeding season when circulating T concentrations were low. This unusual seasonal receptor regulation may represent a means for the year-round regulation of vertebrate aggressive behavior via steroids by increasing the brain's sensitivity to sex steroids during the nonbreeding season.

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Section: Ar Era and Arom Expression In Pommentioning

confidence: 80%

Low sex steroids, high steroid receptors: Increasing the sensitivity of the nonreproductive brain

Canoine

Fusani

Schlinger

et al. 2006

Developmental Neurobiology

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“…To test for the neurosteroid specificity of estradiol effects on auditory processing, a separate group of birds (n = 3) was tested with retrodialysis of the nonaromatizable androgen 5β-DHT, with experimental procedures as above for aCSF pretreatment and stimuli playback. Similar to aromatase, the enzyme that synthesizes 5β-DHT from testosterone (5β-reductase) is expressed throughout zebra finch telencephalon (14,41).…”

Section: Methodsmentioning

confidence: 99%

Brain estrogens rapidly strengthen auditory encoding and guide song preference in a songbird

Remage‐Healey

Coleman

Oyama

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

189

224

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Higher cognitive function depends on accurate detection and processing of subtle features of sensory stimuli. Such precise computations require neural circuits to be modulated over rapid timescales, yet this modulation is poorly understood. Brainderived steroids (neurosteroids) can act as fast signaling molecules in the vertebrate central nervous system and could therefore modulate sensory processing and guide behavior, but there is no empirical evidence for this possibility. Here we report that acute inhibition of estrogen production within a cortical-like region involved in complex auditory processing disrupts a songbird's ability to behaviorally respond to song stimuli. Identical manipulation of local estrogen levels rapidly changes burst firing of single auditory neurons. This acute estrogen-mediated modulation targets song and not other auditory stimuli, possibly enabling discrimination among species-specific signals. Our results demonstrate a crucial role for neuroestrogen synthesis among vertebrates for enhanced sensory encoding. Cognitive impairments associated with estrogen depletion, including verbal memory loss in humans, may therefore stem from compromised moment-by-moment estrogen actions in higher-order cortical circuits.I n vertebrates, steroid hormones can rapidly influence the activity of neurons and neural circuits (1-3), although the functional consequences for higher processing are unclear. The exquisite recognition of species-typical vocalizations (4, 5) and abundant production of neuroestrogens (6, 7) are both especially prominent in songbirds. A cortical-like auditory region (the caudomedial nidopallium, or NCM) of songbirds is a critical locus for song learning as well as auditory processing and song recognition (8-11). NCM exhibits rich expression of the estrogen-synthetic enzyme aromatase in both cell bodies and synaptic terminals (6, 12), and neuroestrogen levels within NCM fluctuate rapidly (<30 min) and independent of peripheral sex-steroid levels during social interactions, song playback, and after neurotransmitter activation (13). In songbirds, therefore, rapid changes in the local production of NCM neuroestrogens could in turn rapidly affect processing of complex auditory stimuli, such as song.Here, we test this hypothesis in male Australian zebra finches (Taeniopygia guttata). Our recent optimization of in vivo microdialysis in this species has enabled the measurement and manipulation of local estrogen production within discrete brain regions in awake, behaving males (13). We have further established that local estrogen levels are dependent on the activity of the enzyme aromatase within NCM, because retrodialysis (reverse delivery using microdialysis) of the aromatase inhibitor fadrozole (FAD) into NCM transiently suppresses local estradiol levels (13). ResultsIn Vivo Retrodialysis and Behavior. Adult zebra finches express a robust behavioral preference for acoustic playback of their tutor's song or bird's own song (BOS) compared with conspecific male song (CON) (4, 5, 8), and be...

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“…Aromatase was initially characterized in the ovary and then detected in multiple areas of the basal forebrain in mammals (Naftolin et al, 1971(Naftolin et al, ,1972, raising the hypothesis that some effects of gonadal T on sexual and aggressive behavior are dependent upon local conversion of T to E 2 by brain aromatase. Indeed, a variety of data now show that brain aromatase is a key mediator of the link between T and behavior, and research on birds has provided seminal insights into 1) the cellular localization of aromatase protein and mRNA in neurons (Balthazart et al, 1990c;Shen et al, 1994), 2) the presence of aromatase at the synapse (Schlinger and Callard, 1989;Peterson et al, submitted), 3) hippocampal aromatase expression (Vockel et al, 1990;Saldanha et al, 2000), 4) the expression of aromatase in glia , 5) the regulation of aromatase by endocrine and environmental factors (Hutchison et al, 1986;Balthazart et al, 1990a;Schlinger and Callard, 1990), and 6) behavioral functions of aromatase (Adkins 1975;Adkins and Nock, 1976;Schumacher et al, 1984; and see first section).…”

Section: Aromatasementioning

confidence: 99%

“…The accompanying rise in circulating T coordinates a variety of processes in the brain, many of which require that T be aromatized to E 2 . These include, but are not limited to, increased expression of neuropeptides (e.g., AVT within the BSTm-LS system) (Viglietti- Panzica et al, 2001;Plumari et al, 2004), dramatic restructuring and growth of telencephalic song nuclei (Tramontin & Brenowitz, 2000;Nottebohm, 2004), and an increase in aromatase activity within the VMH and POA (Vockel et al, 1990).…”

Section: Multi-system Integration: Birdsong and Neuroendocrine Cascadesmentioning

confidence: 99%

Recent advances in behavioral neuroendocrinology: Insights from studies on birds

Goodson

Saldanha

Hahn

et al. 2005

Hormones and Behavior

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Ever since investigations in the field of behavioral endocrinology were hatched with experiments on roosters, birds have provided original insights into issues of fundamental importance for all vertebrate groups. Here we focus on more recent advances that continue this tradition, including 1) environmental regulation of neuroendocrine and behavioral systems, 2) steroidogenic enzyme functions that are related to intracrine processes and de novo production of neurosteroids, and 3) hormonal regulation of neuroplasticity. We also review recent findings on the anatomical and functional organization of steroid-sensitive circuits in the basal forebrain and midbrain. A burgeoning body of data now demonstrates that these circuits comprise an evolutionarily conserved network, thus numerous novel insights obtained from birds can be used (in a relatively straightforward manner) to generate predictions for other taxa as well. We close by using birdsong as an example that links these areas together, thereby highlighting the exceptional opportunities that birds offer for integrative studies of behavioral neuroendocrinology, and behavioral biology in general. Keywords aggression; reproduction; song; limbic system; vasotocin; photoperiod; neurosteroid; DHEA; aromatase; adult neurogenesis; estrogen; testosterone; thyroxin; hypothalamus; hippocampus; HVC; septum; GnRH; SCN; season; neuroplasticity Birds offer excellent opportunities for behavioral and neuroendocrine experiments in both the field and the laboratory, and studies conducted at this interface have historically placed avian models on the cutting edge of research (Konishi et al., 1989; also see Wingfield, this issue). Indeed, wild birds offer a combination of accessibility (being diurnal and terrestrial) and diversity (social and ecological) that makes them invaluable models for studying mechanistic and evolutionary questions that are not as tractable in other vertebrate groups. This diversity can be studied within the context of neural and endocrine systems that share many features with those of other taxa (thereby increasing the general relevance of avian studies) (Goodson, 2005), although these features are often more pronounced in birds. Such examples include exceptionally robust and widespread neural aromatase activity, and adult neurogenesis in the forebrain, both of which are considered further below (also see Ball and Balthazart, 2004;

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Effects of castration and testosterone treatment on the activity of testosterone‐metabolizing enzymes in the brain of male and female zebra finches

Cited by 91 publications

References 59 publications

Low sex steroids, high steroid receptors: Increasing the sensitivity of the nonreproductive brain

Low sex steroids, high steroid receptors: Increasing the sensitivity of the nonreproductive brain

Brain estrogens rapidly strengthen auditory encoding and guide song preference in a songbird

Recent advances in behavioral neuroendocrinology: Insights from studies on birds

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