Androgen affects cholinergic enzymes in syringeal motor neurons and muscle

doi:10.1016/0006-8993(80)91011-2

Brain Research

Volume 192, Issue 1, 16 June 1980, Pages 89-107

https://doi.org/10.1016/0006-8993(80)91011-2 Get rights and content

Summary

We examined the role of testosterone (T) in regulating the weight of the songbird syrinx and the activity of two cholinergic enzymes, choline acetyltransferase (CAT) and acetylcholinesterase (AChE). Castration of adult male zebra finches or neonatal canaries results in a lowering of syringeal weight and CAT and AChE activity. Administration of T for 1–4 weeks restores syringeal weight and AChE to intact levels in male zebra finches. Activity of CAT in muscle is not fully restored. Ovariectomy of female zebra finches and canaries does not affect these syringeal parameters, but T administration to ovariectomized females for 1 month increased syringeal weight and AChE activity. In the zebra finch tracheosyringealis nerve, activity of CAT and AChE is decreased on moonth after castration. T administration to castrates maintains nerve AChE activity but not CAT. In contrast to changes in the syrinx, tongue muscles do not change in weight or enzyme activity when circulating T levels are altered. Effects of muscle use and disuse were found on syringeal weight and AChE activity, but an androgenic effect also operates in addition. Results suggest that one mechanism for T regulation of singing in passerine birds is through induction of specific enzymatic proteins in androgen target neurons and muscles.

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In many species, birds sing much more frequently at the beginning of the breeding season than during the winter [115,116]. These and other behaviors are strongly influenced by seasonal fluctuation of hormones, such as testosterone [117–122]. Testosterone acts across multiple areas of the songbird brain to modify different qualities of singing behavior: in HVC, testosterone release is associated with increased song stereotypy [123•]; while targeted release of testosterone in the medial preoptic nucleus (POM) causes higher rates of singing even in castrated males [122,123•].
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Our conclusion is that birds with testosterone implanted in both POM and HVC sang songs similar to birds with systemic testosterone except that their songs had a lower energy. We also investigated the actions of testosterone directly at the level of the syringeal muscles that are known to express androgen receptors (Lieberburg and Nottebohm, 1979; Luine et al., 1980; Veney and Wade, 2004). Theories of sexual selection predicted that testosterone action on peripheral effector organs might be especially important in regulating traits related to male-male competition or female choice (Folstad and Karter, 1992; Hillgarth and Wingfield, 1997; Witschi, 1961).
In the 1970s, Nottebohm and Arnold reported marked male-biased sex differences in the volume of three song control nuclei in songbirds. Subsequently a series of studies on several songbird species suggested that there is a positive correlation between the degree to which there is a sex difference in the volume of these song control nuclei and in song behavior. This correlation has been questioned in recent years. Furthermore, it has become clear that the song circuit is fully integrated into a more comprehensive neural circuit that regulates multiple courtship and reproductive behaviors including song. Sex differences in songbirds should be evaluated in the context of the full complement of behaviors produced by both sexes in relation to reproduction and based on the entire circuit in order to understand the functional significance of variation between males and females in brain and behavior. Variation in brain and behavior exhibited among living songbird species provides an excellent opportunity to understand the functional significance of sex differences related to social behaviors.
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Although such correlations were lacking in males of red-winged blackbirds (Harding et al., 1988; Johnsen, 1998), quantification of songs of more spontaneously-singing female canaries in the future would increase the power of the correlational analysis. Elevated testosterone levels have been shown to increase the volume of the song control nuclei HVC and RA in adult canaries (Madison et al., 2015; Nottebohm, 1980) and the syrinx weight in zebra finches and canaries (Bleisch et al., 1984; Luine et al., 1980; Wade and Buhlman, 2000). We observed statistical differences of HVC and RA volumes between female singers and non-singers (Fig. 3), but did not find differences in syrinx weights (Supplementary Fig. 4).
Females of many northern temperate songbird species sing sporadically. However, detailed descriptions of female song are rare. Here we report a detailed analysis of song in a small number of spontaneously-singing female domesticated canaries (Serinus canaria) under non-breeding, laboratory conditions in a large population of domesticated birds. In-depth analysis showed that these females sang rarely, and the spontaneous songs varied between and within birds over time. Furthermore, spontaneous female songs were distinct from songs of testosterone-induced singing female canaries and from songs of male canaries in both temporal and spectral features. Singing females had significantly elevated plasma androgen levels and a larger size of the major song controlling brain nuclei HVC (used as a proper name) and the robust nucleus of the arcopallium (RA) than non-singing females housed under similar conditions. The sporadically observed production of song and accompanying differences in brain anatomy in female canaries may thus depend on minute intraspecific differences in androgen levels.
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Testosterone activates singing within days in castrated male songbirds but full song quality only develops after a few weeks. Lesions of the medial preoptic nucleus (POM) inhibit while stereotaxic testosterone implants into this nucleus increase singing rate suggesting that this site plays a key role in the regulation of singing motivation. Testosterone action in the song control system works in parallel to control song quality. Accordingly, systemic testosterone increases POM volume within 1–2 days in female canaries, while the increase in volume of song control nuclei takes at least 2 weeks. The current study tested whether testosterone action is associated with similar differences in latencies in males. Photosensitive castrated male canaries were implanted with testosterone-filled Silastic™ implants and control castrates received empty implants, while simultaneously the photoperiod was switched from short- to long-days. Brains were collected from all subjects two days later. Plasma testosterone was elevated in testosterone-treated but not in controls. HVC volumes were not affected, but testosterone significantly increased the POM volume as identified by the dense group of aromatase-immunoreactive neurons, the number and somal area of these neurons and the fractional area they cover in POM. Testosterone-treated females from a previous experiment had a smaller POM volume in similar conditions suggesting the existence of a stable sex difference potentially affecting singing behavior. Thus testosterone induces male POM growth and aromatase expression in this nucleus within two days without affecting HVC size, further supporting the notion that testosterone increases singing motivation via its action in POM.
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The zebra finch is a common model organism in neuroscience, endocrinology, and ethology. Zebra finches are generally considered opportunistic breeders, but the extent of their opportunism depends on the predictability of their habitat. This plasticity in the timing of breeding raises the question of how domestication, a process that increases environmental predictability, has affected their reproductive physiology. Here, we compared circulating steroid levels in various “strains” of zebra finches. In Study 1, using radioimmunoassay, we examined circulating testosterone levels in several strains of zebra finches (males and females). Subjects were wild or captive (Captive Wild-Caught, Wild-Derived, or Domesticated). In Study 2, using liquid chromatography–tandem mass spectrometry (LC–MS/MS), we examined circulating sex steroid profiles in wild and domesticated zebra finches (males and females). In Study 1, circulating testosterone levels in males differed across strains. In Study 2, six steroids were detectable in plasma from wild zebra finches (pregnenolone, progesterone, dehydroepiandrosterone (DHEA), testosterone, androsterone, and 5α-dihydrotestosterone (5α-DHT)). Only pregnenolone and progesterone levels changed across reproductive states in wild finches. Compared to wild zebra finches, domesticated zebra finches had elevated levels of circulating pregnenolone, progesterone, DHEA, testosterone, androstenedione, and androsterone. These data suggest that domestication has profoundly altered the endocrinology of this common model organism. These results have implications for interpreting studies of domesticated zebra finches, as well as studies of other domesticated species.
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^*: Present address: Dept. of Psychology, Hunter College, New York, N.Y. 10021, U.S.A.

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Androgen affects cholinergic enzymes in syringeal motor neurons and muscle

Summary

Gen. comp. Endocr.

Analyt. Biochem.

Gen. comp. Endocr.

J. biol. Chem.

Brain Research

J. biol. Chem.

Exp. Neurom.

J. neurol. Sci.

J. neurol. Sci.

A Study of Bird Song

Behavioral Effects of Androgen in Zebra Finches (Poephila guttata) and a Search for its Sites of Action

The effects of castration and androgen replacement on song, courtship and aggression in zebra finches(Poephila guttata)

Exp. Zool.

Hormone concentrating cells in vocal control and other areas of the brain of the zebra finch(Poephila guttata)

J. comp. Neurol.

Sexual differences in pattern of hormone accumulation in the brain of a song bird

Science

Effects of testosterone propionate on female roller canaries under complete song isolation

Testosterone effects on choline acetylase and acetylcholinesterase in the XIIth cranial nerve and syringeal muscle of the zebra finch

Neurosci. Abstr.

Hormone accumulation in motoneurons innervating penile striated muscles in the rat

Neurosci. Abstr.

Testes stimulation of the chaffinch obtained in winter by artificial illumination, gonadotrophin and thyroxin

C.R. Acad. Sci. (Paris)

Prostatic involution: effect on androgen receptors and intracellular androgen transport

Biochem. Biophys. res. Commun.

androgen receptors in mouse kidney: a study of male, female and androgen-insensitive(tfm/y) mice

Endocrinology

The functions of advertising song in the sedge warbler(Acrocephalus schoenobaenus) and the reed warbler(A. scirpaceus)

Behaviour

Etudes sur les caracteres sexuels des Pinsons

Fringilla coelebset F. montifringilla, Gerfaut

Androgen and estrogen binding in rat skeletal and perineal muscles

Canad. J. Biochem.

Testosterone and ‘5α-dihydrotestosterone’ levels in plasma of male and female ring doves(Streptopelia risoria) during the reproductive cycle

Biol. Reprod.

Radiochemical micro assays for the determination of choline acetyltransferase and acetylcholinesterase activities

Biochem. J.

A simple, quick microassay for choline acetyltransferase

J. Neurochem.

Demonstration and partial characterization of cytosol receptors for testosterone

Biochemistry

Changes in cholinesterase activity of rat muscle during growth and hypertrophy

Amer. J. Physiol.

Changes in the choline acetyltransferase and cholinesterase activities in the levator ani muscle of rats following castration

Physiol. Bohemoslov.