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Steroid-induced plasticity in the sexually dimorphic vasotocinergic innervation of the avian brain: behavioral implications.
Panzica GC, Aste N, Castagna C, Viglietti-Panzica C, Balthazart J.
Department
of Anatomy, Pharmacology, and Forensic Medicine, Laboratory of
Neuroendocrinology, Rita Levi Montalcini Center for Brain Repair,
University of Torino, Torino, Italy. giancarlo.panzica@unito.it
Vasotocin
(VT, the antidiuretic hormone of birds) is synthesized by diencephalic
magnocellular neurons projecting to the neurohypophysis. In addition,
in male quail and in other oscine and non-oscine birds, a sexually
dimorphic group of VT-immunoreactive (ir) parvocellular neurons is
located in a region homologous to the mammalian nucleus of the stria
terminalis, pars medialis (BSTm) and in the medial preoptic nucleus
(POM). These cells are not visible in females. VT-ir fibers are present
in many diencephalic and extradiencephalic locations. Quantitative
morphometric analyses demonstrate that, in quail, these elements are
expressed in a sexually dimorphic manner (males>females) in regions
involved in the control of different aspects of reproduction: i.e., the
POM (copulatory behavior), the lateral septum (secretion of
gonadotropin-releasing hormone [GnRH]), the nucleus intercollicularis
(control of vocalizations), and the locus coeruleus (the main
noradrenergic center of the avian brain). In many of these regions,
VT-ir fibers are closely related to aromatase-ir, GnRH-ir, or estrogen
receptor-expressing neurons. This dimorphism has an organizational
nature: administration of estradiol-benzoate to quail embryos (a
treatment that abolishes male sexual behavior) results in a dramatic
decrease of the VT-immunoreactivity in all sexually dimorphic regions
of the male quail brain. Conversely, the inhibition of estradiol (E2)
synthesis during embryonic life (a treatment that stimulates the
expression of male copulatory behavior in adult testosterone
(T)-treated females) results in a male-like distribution of VT-ir cells
and fibers. Castration markedly decreases the immunoreactivity in both
the VT-immunopositive elements of the BSTm and the innervation of the
SL and POM, whereas T-replacement therapy restores the VT
immunoreactivity to a level typical of intact birds. These changes
reflect modifications of VT mRNA concentrations (and probably
synthesis) as demonstrated by in situ hybridization and they are
paralleled by similar changes in male copulatory behavior (absent in
castrated male quail, fully expressed in CX+T males). The aromatization
of T into estradiol (E2) also controls VT expression and, in parallel
limits the activation of male sexual behavior by T. In castrated male
quail, the restoration by T of the VT immunoreactivity in POM, BSTm and
lateral septum could be fully mimicked by a treatment with E2, but the
androgen 5alpha-dihydrotestosterone (DHT) had absolutely no effect on
the VT immunoreactivity in these conditions. At the doses used in this
study, DHT also did not synergize with E2 to enhance the density of VT
immunoreactive structures. Systemic or i.c.v. injections of VT markedly
inhibit the expression of all aspects of male sexual behavior. VT,
presumably, does not simply represent one step in the biochemical
cascade of events that is induced by T in the brain and leads to the
expression of male sexual behavior. Androgens and estrogens presumably
affect reproductive behavior both directly, by acting on
steroid-sensitive neurons in the preoptic area, and indirectly, by
modulating peptidergic (specifically vasotocinergic) inputs to this and
other areas. The respective contribution of these two types of actions
and their interaction deserves further analysis.
Publication Types:
PMID: 11744086 [PubMed - indexed for MEDLINE]
-
Effects of testosterone on the synaptology of the medial preoptic nucleus of male Japanese quail.
Castagna C, Obole A, Viglietti-Panzica C, Balthazart J, Panzica GC.
Department of Anatomy, Pharmacology and Forensic Medicine, University of Torino, Italy.
The
medial preoptic nucleus (POM) of male Japanese quail is a sexually
dimorphic testosterone-dependent structure that plays a key role in the
activation of male sexual behavior. Both the total volume of the
nucleus and the size of the dorsolateral neurons are decreased in
gonadectomized males. Immunocytochemical studies have revealed a
complex pattern of innervation: immunopositive fibers for several
neuropeptides and neurotransmitters have been detected in the POM; some
of them (e.g. vasotocin-immunoreactive fibers) are sexually dimorphic
and testosterone-dependent To understand the anatomical bases of these
testosterone-dependent neurochemical changes, we performed an
ultrastructural study of the POM neuropil in intact sexually mature,
gonadectomized, or testosterone-treated gonadectomized males. A complex
synaptic organization of the POM neuropil was observed in intact male
quail reflecting the heterogeneity of the neurotransmitters and
neuropeptides present in this nucleus. Changes in this organization
were observed after the endocrine manipulations. The number of
axosomatic synapses per cell body decreased after gonadectomy and was
restored to the level observed in the intact group after the
administration of testosterone. By contrast, no significant change was
observed in the density of axodendritic and axospinal synapses after
hormonal manipulations which suggests that the total number of synapses
in the nucleus should be affected by testosterone (constant density in
a changing total volume). The cross-sectional area of synaptic boutons
was also decreased by castration and restored to intact level by
testosterone. The action of testosterone on the activation of male
copulatory behavior in gonadectomized birds is hence paralleled by an
extensive rearrangement of neuropil in the POM.
PMID: 10582522 [PubMed - indexed for MEDLINE]
Organizational effects of estrogens on brain vasotocin and sexual behavior in quail.
Panzica GC, Castagna C, Viglietti-Panzica C, Russo C, Tlemcani O, Balthazart J.
Department of Anatomy, Pharmacology, and Forensic Medicine, University of Torino, Italy.
Reproductive
behavior is sexually differentiated in quail: The male-typical
copulatory behavior is never observed in females even after treatment
with high doses of testosterone (T). This sex difference in behavioral
responsiveness to T is organized during the embryonic period by the
exposure of female embryo to estrogens. We showed recently that the
sexually dimorphic medial preoptic nucleus (POM), a structure that
plays a key role in the activation of male copulatory behavior, is
innervated by a dense steroid-sensitive network of
vasotocin-immunoreactive (VT-ir) fibers in male quail This innervation
is almost completely absent in the female POM and is not induced by a
chronic treatment with T, suggesting that this neurochemical difference
could be organizational in nature. This idea was tested by injecting
fertilized quail eggs of both sexes on day 9 of incubation with either
estradiol benzoate (EB) (25 microg, a treatment that suppresses the
capacity to show copulatory behavior in adulthood) or the aromatase
inhibitor R76713 (10 microg, a treatment that makes adult females
behaviorally responsive to T), or with the solvents as a control (C).
At 3 weeks posthatch, all subjects were gonadectomized and later
implanted with Silastic capsules filled with T. Two weeks later, all
birds were perfused and brain sections were processed for VT
immunocytochemistry. Despite the similarity of the adult endocrine
conditions of the subjects (all were gonadectomized and treated with T
Silastic implants providing the same plasma level of steroid to all
subjects), major qualitative differences were observed in the density
of VT-ir structures in the POM of the different groups. Dense
immunoreactive structures (fibers and a few cells) were observed in the
POM of C males but not females; EB males had completely lost this
immunoreactivity (and lost the capacity to display copulatory
behavior); and, conversely, R76713 females displayed a male-typical
VT-ir system in the nucleus (and also high levels of copulatory
behavior). Similar changes in immunoreactivity were seen in the nucleus
of the stria terminalis and in the lateral septum (VT-ir fibers only in
this case) but not in the magnocellular vasotocinergic system. These
neurochemical changes closely parallel the effects of the embryonic
treatments on male copulatory behavior. The vasotocinergic system of
the POM can therefore be considered an accurate marker of the sexual
differentiation of brain circuits mediating this behavior.
PMID: 9858268 [PubMed - indexed for MEDLINE]
-
Systemic and intracerebroventricular injections
of vasotocin inhibit appetitive and consummatory components of male
sexual behavior in Japanese quail.
Castagna C, Absil P, Foidart A, Balthazart J.
Laboratory of Biochemistry, University of Liege, Belgium.
The
authors investigated the behavioral actions of vasotocin (VT) in
castrated testosterone-treated male Japanese quail. The appetitive and
consummatory components of sexual behavior as well as the occurrence
frequency of crows were inhibited, in a dose-dependent manner, by
injections of VT. The authors observed opposite effects after injection
of the V1 receptor antagonist, dPTyr(Me)AVP. Lower doses of VT were
more active after central than after systemic injection, and effects of
systemic injections of VT were blocked by a central injection of
dPTyr(Me)AVP. The behavioral inhibition was associated with a modified
diuresis after systemic but not central injection. These results
provide direct evidence that VT affects male sexual behavior in quail
by a direct action on the brain independent of its peripheral action on
diuresis.
PMID: 9517831 [PubMed - indexed for MEDLINE]
-
Effects of dopamine agonists on appetitive and consummatory male sexual behavior in Japanese quail.
Castagna C, Ball GF, Balthazart J.
European Graduate School for Neuroscience, University of Liege, Laboratory of Biochemistry, Belgium.
The
effects of pharmacological manipulations of dopaminergic transmission
on appetitive and consummatory aspects of male sexual behavior were
investigated in castrated male Japanese quail treated with exogenous
testosterone. Appetitive male sexual behavior was assessed by measuring
a learned social proximity response and consummatory behavior was
assessed by measuring copulatory behavior per se. The nonselective
dopamine receptor agonist, apomorphine, inhibited in a dose-dependent
manner both components of male sexual behavior. Two indirect dopamine
agonists were also tested. Nomifensine, a dopamine re-uptake inhibitor,
decreased appetitive sexual behavior but increased the frequency of
mount attempts, a measure of consummatory sexual behavior. Amfonelic
acid, a compound that enhances dopaminergic tone by a complex
mechanism, increased aspects of both appetitive and consummatory
behaviors. These data suggest that, in quail, as in rodents, increases
in dopaminergic tone facilitate both appetitive and consummatory
aspects of male sexual behavior. Apomorphine may be inhibitory in quail
because it acts primarily on D2-like receptors, unlike in rats, where
it stimulates sexual behavior and acts primarily on D1-like receptors
at low doses but interacts with D2-like receptors at higher doses. This
is supported by the observation that stereotyped pecking, a behavior
stimulated selectively in quail by D2 agonists, was increased by
apomorphine but not by the two indirect agonists. The observed partial
dissociation between the effects of these dopaminergic agonists on
appetitive and consummatory sexual behaviors suggests that these two
components of male sexual behavior may be controlled by the action of
dopamine through different neuronal systems.
PMID: 9300599 [PubMed - indexed for MEDLINE]
-
Differential effects of D1 and D2
dopamine-receptor agonists and antagonists on appetitive and
consummatory aspects of male sexual behavior in Japanese quail.
Balthazart J, Castagna C, Ball GF.
European
Graduate School of Neuroscience (EURON), Laboratory of Biochemistry,
University of Liege, Belgium. jbalthazart@ulg.ac.be
Pharmacological
studies in Japanese quail based on behavioral tests with a variety of
dopaminergic compounds suggest that the activation of D2 dopamine
receptors inhibits, and the activation of D1 dopamine receptors
enhances, appetitive and consummatory components of male sexual
behavior. This hypothesis was tested by studying the behavioral effects
of specific D1 and D2 dopaminergic-receptor agonists and antagonists in
castrated male Japanese quail chronically treated with exogenous
testosterone (subcutaneous Silastic implants). The effects of 5
compounds were tested: 1 D1 (SKF38393) and 2 D2 (PPHT and quinpirole)
agonists, and 1 D1 (SCH23390) and 1 D2 (Spiperone) antagonist. All
compounds were tested at a low and a high dose (0.1 and 1 mg/kg,
respectively, for all drugs, except spiperone where the doses were 2
and 10 mg/kg). A consistent effect of all drugs on consummatory sexual
behavior was observed: it was stimulated by the D1 agonist and the D2
antagonist, but inhibited by the D1 antagonist and the D2 agonists. Far
fewer effects of the treatments were detected on the measures of
appetitive behavior. Measures of appetitive behavior were decreased by
the 2 D2 agonists, but not affected by the other treatments. These data
suggest that male copulatory behavior in quail is stimulated by
dopamine acting on D1 receptors, but inhibited by activation of the D2
receptor subtype. The partial dissociation observed between the effects
of the same treatments on appetitive and consummatory aspects of sexual
behavior also suggests that these 2 behavioral systems may be
controlled by the action of dopamine on different neuronal systems.
PMID: 9272666 [PubMed - indexed for MEDLINE]
-
Aromatase inhibition blocks the activation and sexual differentiation of appetitive male sexual behavior in Japanese quail.
Balthazart J, Castagna C, Ball GF.
Laboratory of Biochemistry, University of Liege, Belgium. jbalthazart@ulg.ac.be
Two
experiments investigated the role of estrogens in the activation and
sexual differentiation of appetitive sexual behavior (ASB) in Japanese
quail (Coturnix japonica) as measured by a learned social proximity
response. Injection of the aromatase inhibitor R767 13 in castrated,
testosterone (T)-treated male quail completely suppressed ASB,
confirming that, like consummatory sexual behavior, ASB is mediated by
T aromatization. ASB is not observed in female quail, even if they are
treated with T as adults. The role of embryonic estrogens in the sexual
differentiation of ASB was tested by blocking estrogen synthesis in
ovo. Control male and T-treated female quail deprived of estrogens
during embryonic life learned the social proximity response used to
assess ASB, whereas control female quail did not, despite the presence
of high T. Thus, ASB is demasculinized by the action of embryonic
estrogens during ontogeny as is consummatory behavior.
PMID: 9106677 [PubMed - indexed for MEDLINE]
-
Testosterone effects on the neuronal ultrastructure in the medial preoptic nucleus of male Japanese quail.
Panzica GC, Castagna C, Aste N, Viglietti-Panzica C, Balthazart J.
Department of Human Anatomy and Physiology, University of Torino, Italy.
Dorsolateral
neurons of the medial preoptic nucleus (POM) of male Japanese quail are
sensitive to the plasma levels of testosterone: their volume and
optical density in Nissl-stained sections increase in castrated birds
treated with testosterone. The present study was performed on castrated
male quail treated or not with Silastic implants filled with
testosterone to describe the ultrastructural variations induced by
testosterone in these neurons. Gonadally intact male birds were
included as controls. The ultrastructure of neurons, taken from the
dorsolateral portion of the POM, was dramatically affected by the
endocrine manipulations. Quantitative evaluations demonstrated a
significant decrease in castrated birds of the rough endoplasmic
reticulum (RER), of free polyribosomes, of Golgi complexes, and of
dense bodies; these changes paralleled the decrease in cell size. The
cell size and the percentage of volume occupied by the intracellular
organelles in castrated birds treated with testosterone were comparable
to values observed in controls. These ultrastructural changes are
similar to those observed in neuronal targets for other gonadal
hormones, supporting the idea that testosterone stimulates the
development of cytoplasmic structures involved in protein synthesis and
secretion. In addition, exposure to testosterone affects the synaptic
inputs to POM. These ultrastructural changes are presumably related to
the physiological effects (e.g., activation of male sexual behavior)
exerted by testosterone on this preoptic region.
PMID: 8705315 [PubMed - indexed for MEDLINE]
-
Ultrastructural characterization of the sexually dimorphic medial preoptic nucleus of male Japanese quail.
Panzica GC, Spigolon S, Castagna C.
Department of Human Anatomy and Physiology, University of Torino, Italy.
The
medial preoptic nucleus is a sexually dimorphic structure whose
cytoarchitecture, afferent and efferent connections, and functions have
been previously described. No detailed ultrastructural study has,
however, been performed to date. Here we describe the ultrastructural
organization of this important preoptic structure of the male quail.
Neuronal cell bodies of the medial preoptic nucleus generally show
extensive development of protein-synthesis-related organelles (rough
endoplasmic reticulum, polysomes), and of secretory structures (Golgi
complexes, secretory vesicles, dense bodies). Previous morphometrical
studies at the light-microscopical level have demonstrated the presence
of a medial and a lateral neuronal population distinguished by the size
of their cell bodies (the medial neurons are smaller than the lateral
neurons). The present ultrastructural investigation confirms the
difference in size, but no difference has been observed in the
ultrastructural organization of the neurons. In both the medial and the
lateral part, the nucleus is characterized by a large variety of cell
bodies, including some that, on the basis of their ultrastructure, can
be considered as putative peptidergic neurons. Close contacts are
frequently observed between adjacent cell bodies that are normally
arranged in clusters. Various types of synaptic endings are also
present, suggesting a rich supply of nerve fibers. A few glial cells
are scattered within the nucleus. In view of the crucial role of this
region in regulating quail sexual behavior, the large heterogeneity of
neurons and of afferent nervous fibers suggest that this region might
have an important role in the integration of information arriving from
different brain regions.
PMID: 7736550 [PubMed - indexed for MEDLINE]
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