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MRC Unit on the Development and Integration of Behaviour, Madingley, Cambridge, CB3 8AA
(Received 29 May 1974)
Intra-hypothalamic testosterone propionate (TP) implants are less effective in evoking pre-copulatory courtship behaviour in long-term (90-day) than in short-term (30-day) castrated male doves, suggesting that there is a decline in sensitivity to androgen after castration (Hutchison, 1969). Because photoperiod was shortened from 13 h/day to 8·5 h/day immediately after castration in this experiment, it was not possible to establish whether the decline in effectiveness of intra-hypothalamic TP was due to the effects of shortening the photoperiod or to the prolonged absence of gonadal hormones. The object of the experiment reported here was to determine whether castrated doves maintained on a long photoperiod (13 h/day) showed a similar decline in behavioural responsiveness to intra-hypothalamic TP.
The experimental methods have been described previously (Hutchison, 1971). Males were brought in from outside aviaries for a period
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SUMMARY
To determine whether the display of male courtship behaviour depends on the action of androgen on discrete areas of the brain, single crystalline implants of testosterone propionate (TP) (mean weight 40 μg) were positioned unilaterally in the brains of castrated male Barbary doves. Implants in the preoptic, anterior hypothalamic and lateral hypothalamic areas induced the full courtship display consisting of chasing, bowing and nestsoliciting. None of these behaviour patterns was re-established at precastration levels measured in terms of duration of display. Durations of courtship displayed by implanted males were similar to those induced by daily intramuscular injections of TP (300 μg/day × 15) into castrated birds.
The effectiveness of implants of TP into other regions of the brain could be related to their proximity to the preoptic and anterior hypothalamic regions. There were marked deficits in the pattern of courtship of castrated doves with implants in areas adjacent to the preoptic and anterior hypothalamic regions — the neostriatum intermediale, the area basalis, and posterior hypothalamus; implants more distantly placed in the paleostriatum primitivum and lateral forebrain bundle area did not induce courtship behaviour.
Cholesterol implants (59 μg) and blank implant tubing in the preoptic and anterior hypothalamic areas did not affect behaviour.
The results obtained were not specific for TP implants; chasing and nest-soliciting displays were also induced by either testosterone implants (51 μg) or oestradiol-17β monobenzoate implants (47 μg). In both cases, the courtship display lacked bowing.
It is concluded that the preoptic and anterior hypothalamic areas are directly sensitive to testosterone and that these areas are associated with the control of courtship behaviour.
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MRC Unit on the Development and Integration of Behaviour, Madingley, Cambridge and Department of Veterinary Clinical Studies, Cambridge, CB3 8AA
(Received 16 October 1974)
Male behaviour during the reproductive cycle of the Barbary dove begins with courtship behaviour and, after a series of behavioural transitions, progresses to incubation. Male courtship appears to be androgen-dependent because it can be restored in castrated birds by systemic or intrahypothalamic administration of testosterone propionate (Hutchison, 1971). However, progesterone is thought to be causally related to the termination of courtship and the onset of incubation behaviour (Lehrman, 1965). The objects of the present study were to determine (a) whether testosterone (T) is present in the peripheral blood plasma of courting male doves, and (b) whether T levels are similar to those of incubating males when progesterone is thought to be functionally active. Because there is evidence in the male for a transition early in the
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ABSTRACT
Intact male hamsters show olfactory behaviour (sniffing and licking) to novel females. After exposure to female vaginal secretions, they show less sniffing towards a novel female if she does not match previously encountered odours (Steel, 1984). Male hamsters, castrated and injected s.c. with various steroids, were tested for the amount of sniffing they directed towards novel and mismatching females.
5α-Dihydrotestosterone propionate (DHTP),17β-hydroxy-17α-methyl-estra-4,9,11-triene-3-one (methyltrienolone, R1881) and oestradiol benzoate alone did not influence olfactory behaviour, while testosterone propionate (TP), DHTP plus oestradiol and R1881 plus oestradiol all increased sniffing to a novel female over the levels shown by saline-treated, castrated controls. Our results also indicated that only the aromatizable androgen (TP) or non-aromatizable androgens DHTP and R1881, in combination with oestradiol, reduced sniffing directed to a mismatching female after exposure to vaginal odour.
We conclude that both androgenic and oestrogenic actions are required not only for olfactory behaviour, but also for olfactory recognition as indicated by a reduction in sniffing directed towards mismatching females. This suggests that aromatization of testosterone may be involved in the control of olfactory processes associated with reproductive behaviour.
J. Endocr. (1986) 110, 525–531
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ABSTRACT
The effects of testosterone propionate (TP) on brain mechanisms involved in the sexual differentiation of ultrasonic vocalizations were examined in Mongolian gerbils (Meriones unguiculatus). Treatment of neonatal females with TP fully masculinized the rate of emission of the upsweep precopulatory ultrasound during adult sexual interactions with oestrous females. Intracranial implantation of small crystals of TP mixed with cholesterol (65 ng) into females 1–15 h after birth also masculinized the upsweep vocalization emitted in adulthood. Implants of TP positioned in the hypothalamic area had a significantly greater masculinizing effect than TP implants outside this region, or pure cholesterol implants. Two other sexually dimorphic vocalizations, the modulated (mainly precopulatory) and unmodulated (mainly copulatory) calls were masculinized by systemic TP, but intracranial TP had no significant masculinizing action on these calls. Genital structures of females which received neonatal injections of TP were strongly virilized in that their clitorides were lengthened and male-type cornified spines were present on the glans. Females which had received intracranial implants of TP were not virilized peripherally in adulthood. We conclude that testosterone or its metabolites have a direct hypothalamic effect on the development of masculine upsweep vocalizations. Because the other vocalizations were insensitive to intracranial TP, the underlying neural tissues may have different thresholds of response to androgen.
J. Endocr. (1985) 107, 355–363
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ABSTRACT
Three independent components of hamster masculine behaviour (approaching, leaving and sniffing the female) have been shown to depend on both androgenic and oestrogenic action. The behavioural role of 5α-reduced androgens was assessed by blocking 5α-reduction of testosterone by means of 17β-N,N-diethylcarbamoyl-4-aza-5α-androstan-3-one (4-MA) through slow-release silicone elastomer implants. Three dose levels of 4-MA were given to intact, sexually active males. The probability of approaching the female and the amount of sniffing directed to her were both decreased, while the probability of leaving the female was increased. Sniffing and the tendency to approach were affected at lower dose levels than was the tendency to leave. The higher dosage of 4-MA also abolished odour-based discrimination between females shown by normal males. These effects of 4-MA on behaviour were confirmed in castrated hamsters maintained on testosterone. The suppressive effects of 4-MA on behaviour were reversed by treatment with 5α-dihydrotestosterone (DHT). We conclude that testosterone maintains sociosexual behaviour in part by conversion to its 5α-reduced metabolites; components of this behaviour differ in their relative dependence on DHT. In this species, DHT is likely to be a behaviourally active metabolite of testosterone involved in the fine control of behaviour.
J. Endocr. (1988) 119, 483–491
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ABSTRACT
Changes in plasma concentrations of sex steroids were examined in male and female zebra finch chicks during the sensitive period for differentiation of sexually dimorphic brain nuclei associated with the control of song. Using a chromatographic separation procedure and radioimmunoassay, androstenedione, testosterone and 5α-dihydrotestosterone were detected in plasma at relatively high concentrations immediately after hatching. There were no sex differences in concentrations of these androgens. An oestrogen, oestradiol-17β, which is known to differentiate the song-control system, is raised specifically in the circulating plasma of male zebra finch chicks, and not in females. The surge in oestradiol, which occurs during the first week after hatching, coincides with the period when capacity for differentiation of the song system is maximal. Exposure of the male brain to oestradiol-17β could trigger neuronal differentiation.
J. Endocr. (1984) 103, 363–369
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ABSTRACT
Oestrogen is formed in the female dove brain. The aim of this study was to determine whether (a) the catalytic properties of the brain aromatase are similar to the ovarian enzyme and (b) aromatase activity in the female brain changes during the reproductive cycle and is influenced by steroids and environmental stimuli.
The results show that female preoptic aromatase has a higher substrate affinity than the enzyme in ovarian follicles (apparent K m: preoptic area, 7 nmol/l; ovarian follicles, 29 nmol/l), but a lower activity in the preoptic area (Vmax: preoptic area, 290 fmol/mg tissue per h; ovarian follicles, 843 fmol/mg tissue per h). In intact females with developing follicles, oestradiol-17β formation was higher in the posterior hypothalamus than the preoptic area. Females in a later stage of reproductive development (yolked follicles) had a different distribution of oestrogen formation with increased aromatase activity in the preoptic area. Preoptic and posterior hypothalamic aromatase activity of females paired with males for 10 days was positively correlated (r = 0·84, P = 0·0001; r = 0·75, P = 0·001 respectively) with ovarian development. Females with undeveloped ovaries which interacted with males had higher preoptic aromatase activity than visually isolated females with similar ovarian development, suggesting that behavioural stimuli have direct effects on brain aromatase activity which are independent of the ovary. Oestradiol benzoate treatment increased preoptic and posterior hypothalamic aromatase activity in intact and ovariectomized females, and testosterone propionate treatment increased anterior hypothalamic aromatase activity, but did not affect other areas, indicating that the distribution of induced aromatase activity is steroid-specific. Oestrogen treatment in ovariectomized or intact females did not replicate the maximal hypothalamic aromatase activity seen when the ovary contained yolked follicles.
We conclude that brain aromatase activity is related directly to ovarian condition during the reproductive cycle of the female dove. As in the male, steroids have a role in the regulation of oestrogen formation in the female hypothalamus; behavioural stimuli are also likely to be involved in the control of the brain enzyme.
Journal of Endocrinology (1992) 134, 385–396
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ABSTRACT
The effects of photoperiod and castration on brain aromatase activity have been examined using an in-vitro radioassay. Formation of oestradiol-17β was lower in the preoptic area of male Barbary doves on a short daylength (6 h light: 18 h darkness) than in males on a long daylength (14 h light: 10 h darkness). This was a specific effect of photoperiod which did not influence aromatase activity in the anterior or posterior hypothalamic areas, and was not accompanied by changes in hormone-sensitive vocal behaviour. Production of 5β-dihydrotestosterone, 5β-androstane-3α,17β-diol and 5α-dihydrotestosterone by the preoptic area did not differ between birds on long or short days. Therefore, a short photoperiod does not appear to influence other pathways of androgen metabolism. In contrast to the effects of photoperiod, castration reduced oestradiol formation in both preoptic and hypothalamic areas. Intramuscular injection of testosterone propionate (TP) in intact males on short days did not restore the pattern of distribution of aromatase activity seen in males on long days. Preoptic aromatase activity was, however, restored by TP in castrated birds. We conclude that a short photoperiod influences both the activity of aromatase and the inductive effect of testosterone on enzyme activity in the preoptic area, which is known to be associated with the behavioural action of oestrogen in the dove. Photoperiod is likely to act both through changes in circulating androgen and by a direct action on preoptic cells.
J. Endocr. (1986) 109, 371–377
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Differences in the effectiveness of oestradiol-17β and testosterone on male courtship and vocal behaviour were examined in long-term castrated doves. Nest-orientated behaviour was restored by intramuscular injection of oestradiol-17β. Testosterone was effective in restoring aggressive courtship and vocal behaviour, but not for the nest-orientated behaviour. The effects of these hormones were separable, therefore, under conditions of prolonged androgen deficit, suggesting differences in their specificity of action. In-vitro assay of brain enzyme activity indicated that aromatization of testosterone to oestradiol-17β occurred in the preoptic area of long-term castrated doves. Preoptic aromatase activity of long- and short-term castrated doves did not differ. The ineffectiveness of testosterone in restoring nest-orientated behaviour in long-term castrated doves did not appear, therefore, to be due to a difference between the groups in the basal rate of testosterone aromatization in the preoptic area.
