Download Anatomical and Neurochemical Definition of the Nucleus of the Stria

THE JOURNAL OF COMPARATIVE NEUROLOGY 396:141–157 (1998)
Anatomical and Neurochemical Definition
of the Nucleus of the Stria Terminalis
in Japanese Quail (Coturnix japonica)
N. ASTE,1 J. BALTHAZART,2 P. ABSIL,2 R. GROSSMANN,3 E. MÜLHBAUER,3
C. VIGLIETTI-PANZICA,1 AND G.C. PANZICA1*
1Department of Anatomy, Pharmacology, and Forensic Medicine,
University of Torino, 10126 Torino, Italy
2Laboratory of Biochemistry, University of Liège, 4020 Liège, Belgium
3Institute for Small Animal Research, Federal Research Center of Agriculture,
29223 Celle, Germany
ABSTRACT
This study in birds provides anatomical, immunohistochemical, and hodological data on a
prosencephalic region in which the nomenclature is still a matter of discussion. In quail, this
region is located just dorsal to the anterior commissure and extends from the level of the
medial part of the preoptic area at its most rostral end to the caudal aspects of the nucleus
preopticus medialis. At this caudal level, it reaches its maximal elongation and extends from
the ventral tip of the lateral ventricles to the dorsolateral aspects of the paraventricular
nucleus. This area contains aromatase-immunoreactive cells and a sexually dimorphic
population of small, vasotocinergic neurons. The Nissl staining of adjacent sections revealed
the presence of a cluster of intensely stained cells outlining the same region delineated by the
vasotocin-immunoreactive structures. Cytoarchitectonic, immunohistochemical, and in situ
hybridization data support the notion that this area is similar and is probably homologous to
the medial part of the nucleus of the stria terminalis of the mammalian brain. The present
data provide a clear definition of this nucleus in quail: They show for the first time the
presence of sexually dimorphic vasotocinergic neurons in this region of the quail brain and
provide the first detailed description of this region in an avian species. J. Comp. Neurol.
396:141–157, 1998. r 1998 Wiley-Liss, Inc.
Indexing terms: vasotocin; aromatase; sex dimorphism; in situ hybridization; bird
The bed nucleus of the stria terminalis (BST) has been
studied intensively in mammals, whereas its location and
characteristics are still a matter of discussion in other
classes of vertebrates. Traditionally, this nucleus has been
divided into a medial and a lateral subdivision (Krettek
and Price, 1978; De Olmos et al., 1985) that consist of
several subnuclei (Del Abril et al., 1987; Moga et al., 1989;
Hines et al., 1992). The medial subdivision 3 (BSTm) is
part of the circuitry that controls mating behavior. It
receives inputs from the accessory olfactory bulb and the
medial amygdala, and it sends projections to the medial
preoptic area and the ventromedial hypothalamus (De
Olmos and Ingram, 1972; De Olmos et al., 1978; Krettek
and Price, 1978; Weller and Smith, 1982; Simerly and
Swanson, 1986, 1988; Akesson et al., 1988; Simerly et al.,
1989; Canteras et al., 1995). These regions are involved in
the control of sexual motivation and/or performance (for
recent reviews, see Segovia and Guillamon, 1993; Van
Furth et al., 1995). In contrast, the lateral subdivision
r 1998 WILEY-LISS, INC.
(BSTl) is characterized by reciprocal connections with
nuclei that are involved in central autonomic regulation
(for a review of the literature, see Moga et al., 1989).
Several anatomical (Del Abril et al., 1987; Allen and
Gorski, 1990; Hines et al., 1992; Segovia and Guillamon,
Grant sponsor: MURST; Grant sponsor: CNR; Grant number
97.04308CT04; Grant sponsor: NIMH; Grant number MH 50388; Grant
sponsor: European Community; Grant number: CT94–0472; Grant sponsor: Belgian FRFC; Grant number: 9.4565.96F; Grant sponsor: University
of Liège; Grant sponsor: Government of the French Community of Belgium;
Grant number: AC 93/98–171; Grant sponsor: German Research Foundation; Grant sponsor: European Science Foundation; Grant number: RG95/203.
N. Aste is presently at the Institute of Molecular Neurobiology, Shiga
University of Medical Science, Otsu, Shiga, Japan.
*Correspondence to: Dr. G.C. Panzica, Department of Anatomy, Pharmacology, and Forensic Medicine, Corso M. D’Azeglio 52, 10126 Torino, Italy.
E-mail: [email protected]
Received 7 July 1997; Revised 30 December 1997; Accepted 10 February 1998
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N. ASTE ET AL.
1993) and neurochemical (Woodhams et al., 1983; Walter
et al., 1991) characteristics of the BSTm or of its subdivisions are sexually dimorphic and are organized in early life
by steroid hormones (for review, see Guillamon and Segovia, 1997). In particular, sex differences that favor males
compared with females affect the number of vasopressinimmunoreactive (VP-ir) neurons and the VP content of
BSTm in the rat brain (De Vries et al., 1994a; Wang et al.,
1994). Moreover, the rodent BSTm is an important site of
testosterone aromatization (transformation of testosterone into 17b-estradiol), as shown by measures of the
enzymatic activity and immunocytochemical detection of
the protein (Roselli, 1991; Roselli and Resko, 1993; Jakab
et al., 1993; Shinoda et al., 1994; Tsuruo et al., 1994;
Foidart et al., 1995a). Recently, the presence of nitric oxide
synthase has been demonstrated in many of the nuclei
that control the rodent mating behavior, including the BST
(Hadeishi and Wood, 1996).
In the rat, the BSTm is one element of the pathway that
connects the vomeronasal organ to the preoptic regionhypothalamus; therefore, it is implicated in the control of
various aspects of reproductive behavior that are governed
by chemosensory stimuli (Segovia and Guillamon, 1993;
Guillamon and Segovia, 1997). Several studies indicate
that lesions aimed at the rat BST disrupt consummatory
and/or motivational aspects of male and female sexual
behavior (Emery and Sachs, 1976; Valcourt and Sachs,
1979; Lopez and Carrer, 1982; Claro et al., 1995; Takeo et
al., 1995) and impair maternal behavior (Numan and
Numan, 1996). Moreover, a recent study suggests that the
volume of the central subdivision of the BST, as identified
by vasoactive intestinal polypeptide immunoreactivity, is
related to gender identity in humans (Zhou et al., 1995).
However, despite numerous studies investigating morphological and functional characteristics of the BST in mammals, the definition of the homologous nucleus in other
classes of vertebrates is still a matter of controversy.
The Japanese quail is an experimental model that has
been employed widely in the study of the neural and
endocrine bases of male sexual behavior (for recent reviews, see Balthazart and Foidart, 1993; Panzica et al.,
1996b). The action of steroids in the quail preoptichypothalamic region is necessary and sufficient to activate
male copulatory behavior (Balthazart and Surlemont,
1990a,b); accordingly, this area contains large numbers of
cells that express steroid receptors (Watson and Adkins
Regan, 1988; Balthazart et al., 1989, 1992b). Aromatization of testosterone into estrogens is a limiting step in the
activation of male quail copulatory behavior; consequently,
the distribution and regulation of preoptic aromatase
(ARO) activity and ARO-containing neurons have been
intensively studied (for recent reviews, see Balthazart et
al., 1996b; Balthazart, 1997). ARO-ir neurons are present
in the nucleus preopticus medialis (POM), the tuberal
region, an area dorsal to the anterior commissure (CA),
and a V-shaped structure extending from a region ventral
to the lateral septal area to the caudal aspects of the POM
(Balthazart et al., 1990a,b, 1997; Foidart et al., 1995b).
With the exception of the POM, which is outlined clearly
by ARO-ir cells and can be observed also in Nissl-stained
material, the regions containing ARO-ir cells in the quail
brain do not match exactly the structures that have been
defined previously based on Nissl-stained sections. Their
identification and nomenclature is therefore somewhat
unclear.
Numerous peptidergic elements have also been identified within the quail septopreoptic-hypothalamic region
(Panzica et al., 1992a; Aste et al., 1997). In particular,
several studies have been devoted to the vasotocin (VT)-ir
fibers of the POM and of the lateral septum, because these
peptidergic structures are sexually dimorphic and steroidsensitive (Viglietti-Panzica et al., 1992, 1994; Panzica et
al., 1996a; Aste et al., 1997; for review see Panzica et al.,
1997). However, these studies have paid little attention to
the distribution of this neuropeptide in the aforementioned region of the quail brain, which is located between
the septum and the caudal aspects of the POM.
In a number of immunocytochemical studies analyzing
the distribution of ARO-ir or VT-ir structures in quail and
other avian species (fowl, canary, zebra finch), this region
was named the nucleus of the stria terminalis (Kiss et al.,
1987; Balthazart et al., 1990b; Viglietti-Panzica et al.,
1992; Voorhuis and De Kloet, 1992; Foidart et al., 1995b;
Shen et al., 1995; Jurkevich et al., 1997). However, the
Abbreviations
AA
Ac
AM
ARO
BSTl
BSTm
CA
CPa
DLA
E
FPL
GLv
HA
Hp
HV
ir
LA
LHy
LPO
LV
N
nCPa
archistriatum anterior
nucleus accumbens
nucleus anterior medialis hypothalami
aromatase
bed nucleus striae terminalis, pars lateralis
bed nucleus striae terminalis, pars medialis
commissura anterior
commissura pallii
nucleus dorsolateralis anterior thalami
ectostriatum
fasciculus prosencephali lateralis (lateral forebrain bundle)
nucleus geniculatus lateralis, pars ventralis
hyperstriatum accessorium
hippocampus
hyperstriatum ventrale
immunoreactive
nucleus lateralis anterior thalami
nucleus lateralis hypothalami
lobus paraolfactorius (medial part of the dorsal striatum)
lateral ventricle
neostriatum
nucleus commissurae pallii
NI
OM
PA
POA
POD
POM
PP
PVN
QF
ROT
SCNl
SCNm
SL
SM
Tn
TPO
TSM
VLT
VMN
VP
VT
neostriatum intermedium
occipitomesencephalic tract
paleostriatum augmentatum (lateral part of the dorsal
striatum)
nucleus preopticus anterior
nucleus preopticus dorsalis
nucleus preopticus medialis
paleostriatum primitivum (dorsal pallidum)
nucleus paraventricularis
tractus quintofrontalis
nucleus rotundus
nucleus suprachiasmaticus, pars lateralis
nucleus suprachiasmaticus, pars medialis
nucleus septali lateralis
nucleus septali medialis
nucleus taeniae
area temporoparietooccipitalis
tractus septomesencephalicus
nucleus ventrolateralis thalami
nucleus ventromedialis hypothalami
ventral paleostriatum (ventral pallidum)
vasotocin
DEFINITION OF THE NUCLEUS OF THE STRIA TERMINALIS IN BIRDS
region identified in these relatively recent immunocytochemical studies does not always correspond to the area
labeled the nucleus stria terminalis in atlases of the avian
brain, which are based largely on Nissl-stained material
(Stokes et al., 1974; Kuenzel and Masson, 1988; Breazile
and Kuenzel, 1993), and some atlases do not even mention
this structure (Karten and Hodos, 1967; Baylé et al., 1974).
Furthermore, different atlases or publications do not make
a consistent use of terminology for the cell groups that
constitute the ventral striatal regions and that include the
nucleus accumbens, the BST, and the tuberculum olfactorium. The boundaries and exact localization of the BST
and its position relative to the nucleus accumbens, therefore, have not been defined consistently in different studies
(compare Brauth et al., 1978; Reiner et al., 1983; Kitt and
Brauth, 1986a,b; Berk, 1987; Anderson and Reiner, 1991;
Veenman et al., 1995). There has been also a lack of
detailed anatomical investigations describing the full extent of this nucleus, which probably explains the discrepancies in the nomenclature of this region across and within
the avian species.
Neurochemical markers provides a useful method to
analyze homology between brain structures (Gahr, 1997).
Therefore, the present study was designed to provide a
detailed description of this region in quail and attempts to
establish its homology with the mammalian BSTm based
on topographical and neurochemical criteria. Special attention was paid here to the VT-ir and ARO-ir structures that
are clear anatomical markers of the BSTm in mammals.
MATERIALS AND METHODS
Subjects
The experiments described in this paper were carried
out on adult male and female Japanese quail (Coturnix
japonica) that were obtained from local breeders in Belgium (Dujardin Farms, Liernu) or Italy (Morini, Modena).
Throughout their life, they received water and food ad
libitum and were submitted to a photoperiod of 16 hours of
light and 8 hours of darkness. All experimental procedures
have been reviewed by the appropriate authorities and are
in compliance with the relevant laws and regulations of
Italy, Germany, and Belgium that govern the treatment of
experimental animals.
Immunocytochemistry
Seven male and seven female quail were used for
immunocytochemical investigations. They were injected
with 0.1 ml of heparin solution (30 mg/ml; Sigma, St.
Louis, MO) into the wing vein and deeply anaesthetized
with an overdose of Hypnodil (50 mg/kg; Janssen Pharmaceutica, Beerse, Belgium). The animals were then perfused
intracardially with a saline solution followed by 4% paraformaldehyde in 0.1 M phosphate buffer, pH 7.2. The
dissected brains were postfixed in the same fixative for 12
hours at 4°C and washed with 0.01 M phosphate buffer
containing 0.125 M NaCl, pH 7.2 (PBS). After cryoprotection with a solution containing 20% sucrose in PBS, brains
were rapidly frozen on dry ice and stored at 280°C.
Brains were cut in 30-µm-thick coronal sections that
were collected in multiwell plates filled with PBS. Adjacent sections were collected in three separate series, so
that sections placed in the same well were 90 µm apart.
One series was stained with toluidine blue for Nissl
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material, and two series were submitted to immunocytochemical procedures.
Sections were stained by immunocytochemistry for VT
and ARO by using procedures that have been described in
previous studies (Aste et al., 1995; Foidart et al., 1995b).
Briefly, after a 30-minute wash in PBS containing 0.2%
Triton X-100 (PBST) and inhibition of endogenous peroxidase activity by an incubation in hydrogen peroxide,
sections were incubated with normal serum (Vectastain
Labtek; Vector Laboratories, Burlingame, CA) for 20
minute at room temperature. Adjacent sections were then
incubated overnight at room temperature in a primary
antibody diluted in PBST (anti-VT, 1:8,000; anti-ARO,
1:1,000).
The polyclonal anti-VT serum was developed originally
by Dr. D. Gray at the Max Plank Institute of Clinical and
Physiological Research of Bad Nauheim, Germany (Gray
and Simon, 1983). The characteristics and specificity of
this antibody for the detection of quail VT were reported in
a previous study (Viglietti-Panzica et al., 1994). The
polyclonal anti-ARO serum (kindly provided by Dr. N.
Harada, Fujita Health University, Toyoake, Japan) was
raised in rabbit against quail recombinant ARO, as described by Foidart et al. (1995b).
On the next day, sections were incubated for 45 minutes
in a secondary biotinylated antibody and for 30 minutes in
an avidin-biotin-peroxidase complex (Vectastain Elite
Labtek; Vector Laboratories). The peroxidase activity was
revealed with a solution containing 0.187 mg/ml 38,38diaminobenzidine and 0.003% hydrogen peroxide in 0.05
M Tris-HCl, pH 7.6. Several rinses in PBS were made after
each step. The sections were mounted on slides, dehydrated, and coverslipped with Entellan (Merck, Milano,
Italy). The sections were photographed with a Zeiss Axioplan microscope (Thornwood, NY) with a Kodak Wratten
44 or 75 gelatine filter (Eastman Kodak, Rochester, NY) to
increase the contrast.
In situ hybridization
Five adult male and five adult female quail were killed
by decapitation. The brains were quickly dissected and
frozen on dry ice. Coronal sections were cut on a cryostat at
20 µm thickness, serially collected on 3-aminopropyltriethoxy silane-coated slides, and fixed by immersion for 5
minutes in 4% paraformaldehyde in 0.1 M phosphate
buffer, pH 7.2.
After dehydration, the slides were incubated for 2 hours
at 52°C in prehybridization buffer (50% formamide, 5I
Denhardt’s solution, 0.75 M NaCl, 25 mM PIPES, 25 mM
EDTA, 0.2% sodium dodecylsulfate [SDS], 10 mM DTT,
and 250 µg/ml herring sperm DNA). The hybridization
proceeded overnight at 52°C in prehybridization buffer
plus 10% sodium dextran sulfate. The AVT-specific probe
(a 260-bp cDNA directed toward the 38 distal part of the
chicken AVT gene; Hamann et al., 1992) was labeled
with[33P]dCTP by using the random priming method
(Megaprime DNA labeling system; Amersham, Braunschweig, Germany). Approximately 4,000 cpm/µl of
[33P]dCTP-labelled probe were used for each section. The
specificity of this probe for quail AVT mRNA was described
in a previous study (Aste et al., 1996).
Sections were then washed three times in 53 standard
saline citrate (SSC; 3 M NaCl, 0.3 M Na-citrate, pH 7.0),
washed three more times in 23 SSC at room temperature
for 5 minutes, and dried under a vacuum. Slides were
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N. ASTE ET AL.
coated with autoradiography emulsion (LM-1; Amersham,
Little Chalfont, UK) and exposed for 4 days at 6°C. The
sections were finally counterstained with Toluidine blue to
help in the identification of brain nuclei. They were
photographed on a Leitz Diaplan microscope (Wetzlar,
Germany) by using darkfield illumination.
The nomenclature used in this study is based largely on
the chicken atlas of Kuenzel and Masson (1988) with some
modifications, according to our previous studies on the
quail preoptic region (Panzica et al., 1991, 1996b), and on
some recent studies on the pigeon prosencephalon (Veenman et al., 1995; Medina and Reiner, 1997). The drawings
in Figure 1 summarize the distribution of nuclei in the
quail prosencephalon as they are used in this paper.
Discussion of some of the choices made for nomenclature
can be found below (see Results and Discussion).
RESULTS
VT immunoreactivity in males
The septopreoptic-hypothalamic area of male quail contains several discrete clusters of VT-ir structures (cells and
fibers). In agreement with previous observations on quail
(Viglietti-Panzica, 1986; Panzica et al., 1992a, 1996a;
Viglietti-Panzica et al., 1992, 1994; Aste et al., 1997), VT-ir
fibers are observed in the lateral septum, the periventricular hypothalamus, and the tuberal region. In particular, at
the level of the preoptic area, a dense cluster of VT-ir fibers
outlines the whole POM throughout its entire rostral-tocaudal extent (Viglietti-Panzica et al., 1994). VT-ir neurons are found in a periventricular position, lining the
ependymal wall of the third ventricle, close to the pial
surface of the preoptic area and in the nucleus paraventricularis. They are also seen more laterally in the lateral
and dorsal thalamic areas (see Fig. 2E–H).
In addition, VT-ir cells and fibers are observed in a
discrete area located above and caudal to the anterior
commissure, where they have never been described in
detail previously in the quail brain. This region, as discussed below, corresponds to an identifiable cell cluster in
Nissl-stained sections (Fig. 2A–D). This cluster has been
named nucleus of the stria terminalis in a number of
previous publications, but this identification was never
evaluated critically. It is the purpose of the present paper
to provide neurochemical criteria confirming and specifying this nomenclature. In this section, we describe the data
and use the term BSTm without making any additional
comments on the name. In the Discussion, a critical
evaluation of this decision is presented.
VT-ir structures are present in the entire area connecting the lateral septum with the medial preoptic region.
However, they are distributed heterogeneously, and higher
densities of immunoreactive structures allow one to define
the BSTm. These structures are located ventral to the
septal area and extend in the rostrocaudal direction from
about 100 µm rostral to the CA to sections located 200–300
µm caudal to the caudal edge of this commissure. Just
rostral to the CA, a small, dense cluster of VT-ir fibers is
observed ventromedial to the tip of the lateral ventricle. In
slightly more caudal sections, where the first signs of the
CA become visible, this cluster expands to form a larger
structure that also contains a few scattered, immunopositive cell bodies (Figs. 2E, 3C,E). When the CA reaches its
full extension, VT-ir cells are seen in larger numbers above
the commissure, and the cluster of VT-ir fibers extends
above and below the commissure (Figs. 2F, 3G). More
caudally, in sections where the CA is reduced or is no
longer visible, numerous vasotocinergic cells and fibers
cover an ovoid area that is positioned in oblique manner
(dorsolateral-to-ventromedial direction) and border the
dorsal edge of the occipitomesencephalic tract (OM) and of
the lateral forebrain bundle (FPL; Figs. 2G,H, 4B,F, 5B,D).
The most rostral aspect of this ovoid structure merges at
its ventral edge with the most dorsal and caudal aspects of
the VT-ir structures, identifying the POM (Figs. 2G, 3G).
This cluster of VT-ir cells and fibers suddenly disappears
in more caudal sections. The VT-ir fibers defining the
BSTm (Figs. 3E, 4D) are associated only with a few
punctate structures. These VT-ir fibers are often organized
in basket-like ring structures around immunonegative
cells (Fig. 4D).
Scattered VT-ir cells are also present in the most caudal
aspects of the POM at the level of the CA (Figs. 2E–G, 3G,
4B,C). These cells are similar morphologically to those
observed in the BSTm (Figs. 3E, 4D, 5D). Although the
VT-ir cells are not distributed homogeneously in the
BSTm, and although they increase in number as one
progresses in rostrocaudal direction (compare Fig. 3E with
Fig. 5D), their morphological characteristics are similar in
the entire region. These cell bodies are round or slightly
elongated, mainly bipolar, and their diameter ranges
between 5 µm and 12 µm. The density of the immunoreactive material in these cells is variable (Figs. 4C, 5D), but,
in general, it is lower than in the magnocellular elements
observed in the lateral, periventricular, and subpial groups
(Fig. 3G; see also Viglietti-Panzica, 1986; Viglietti-Panzica
et al., 1994).
Distribution of VT mRNA in males
Detection of mRNA for VT by using in situ hybridization
revealed a distribution of large and small elements that is
in agreement with a previous study (Aste et al., 1996).
Magnocellular elements were observed bordering the third
ventricle wall and were also found in a more lateral
position (Fig. 6B,D). In addition, smaller and weakly
labeled cells were revealed by using in situ hybridization
in the septopreoptic region and had a general distribution
that was similar to that of the VT-ir cells described above
in the BSTm and the POM. In particular, a group of VT
gene-expressing cells could be observed easily that corresponded topographically to the group of VT-ir cells located
just above the CA from the rostral edge of this structure to
a level slightly caudal to the end of the POM (Fig. 6B,D).
The small variation in the number of VT-ir cells that has
been described in the rostrocaudal extent of the BSTm
based on the immunocytochemistry could also be observed
at the level of the mRNA. More VT gene-expressing cells
were observed in the caudal portion (Fig. 6D) than in the
rostral portion of the BSTm (Fig. 6B). In situ hybridization
also confirmed the presence of VT gene-expressing cells in
the caudal part of the POM (Fig. 6B,D).
Sexual dimorphism of vasotocinergic
structures
A qualitative sexual dimorphism in the number of VT-ir
cells could be observed in the entire BSTm. VT-ir cells were
detectable only in males (compare Figs. 3G, 4F, 5B,D, and
7A–D), and no VT-ir cell body could be observed in this
area of the female brain, even after prolonged development
of the peroxidase reaction.
Fig. 1. A–H: Schematic drawings throughout the rostral to caudal
(A through H) prosencencephalon of the Japanese quail illustrating
the organization of the preoptic and telencephalic nuclei in this
species. Hatched areas represent the major fiber tracts of the region.
The nomenclature used in these drawings is based largely on the
chicken atlas of Kuenzel and Masson (1988), with some more recent
modifications for the preoptic region (Panzica et al., 1991, 1996b) and
the limbic system (Veenman et al., 1995; Medina and Reiner, 1997).
For abbreviations, see list.
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Fig. 2. A–D: Schematic drawings of Nissl-stained sections throughout the male quail septopreoptic-hypothalamic area, including the
medial part of the bed nucleus of the stria terminalis (BSTm)
throughout its rostrocaudal extent. Shaded areas indicate the presence of Nissl-stained cell clusters. E,F: Schematic distribution of the
vasotocin-immunoreactive (VT-ir) cells in the quail septopreoptic
region. Small and large dots indicate the parvocellular and magnocel-
N. ASTE ET AL.
lular perikarya, respectively. I–L: Distribution of aromatase (ARO)-ir
cells (triangles) in the quail septopreoptic region. LV, lateral ventricle;
BSTl, lateral part of the bed nucleus of the stria terminalis; nCPa,
nucleus of the pallial commissure; POM, medial preoptic nucleus; CA,
anterior commissure; FPL, lateral forebrain bundle. For other abbreviations, see list.
Fig. 3. A: Low-power enlargement of a Nissl-stained section of the
male quail septopreoptic area. Arrow indicates the rostral pole of the
bed nucleus of the stria terminalis (BSTm). The relationship of this
region (arrow) with the lateral septum, the lateral ventricle, and the
anterior commissure can be appreciated. B,C: Consecutive sections
illustrating the clustered, Nissl-stained cells (B) and vasotocin (VT)-ir
structures (C) in the rostral part of the BSTm. The two arrows indicate
two blood vessels for reference. The VT-ir elements in C (identified by
the dashed line) cover the denser Nissl-stained region that is observed
in B (dashed line). D: High magnification of aromatase (ARO)-ir
elements in the BSTm that are visible in F. E: High magnification of
the VT-ir cells and fibers shown in C. Small bipolar elements are
visible (arrows) among the network of positive fibers. F,G: Topographical correspondence between the ARO-ir neurons (F) and VT-ir structures (G) in the medial preoptic nucleus (POM) and in the BSTm in
adjacent sections. Asterisks indicate the lateral ventricle and the third
ventricle. CA, anterior commissure; FPL, lateral forebrain bundle. For
abbreviations, see list. Scale bars 5 200 µm in A,B,C, 100 µm in D–G.
Fig. 4. A: Nissl-stained section at the level of the pallial commissure (CPa). The medial preoptic nucleus (POM) and the bed nucleus of
the stria terminalis (BSTm) are at caudal levels, where they merge.
B: Adjacent section showing the distribution of vasotocin (VT)-ir
structures. C,D: High magnification of VT-ir cells and fibers in the
POM (C) and the BSTm (D). Cell bodies are round and weakly stained.
A broad network of ir fibers is also present. E,F: Consecutive sections
representing the caudal BSTm and its merging with the POM. Note
the correspondence of the blood vessels (arrows) and their identical
relationship between the Nissl-stained cluster of cells (E) and the
VT-ir structures (F). Asterisk indicates the third ventricle. Scale
bars 5 200 µm in A,B,E,F, 100 µm in C,D.
DEFINITION OF THE NUCLEUS OF THE STRIA TERMINALIS IN BIRDS
Fig. 5. A–D: Caudal portion of the male quail bed nucleus of the
stria terminalis (BSTm). A,C: Distribution of aromatase (ARO)-ir
elements. B,D: Distribution of vasotocin (VT)-ir elements. Cells and
fibers positive for these two markers are distributed in the same
region. ARO-ir cell bodies are more numerous than VT-ir perikarya,
149
whereas the number of VT-ir fibers is higher than the number of
ARO-ir fibers. Asterisks in B indicate the large VT-ir elements of the
magnocellular system. Scale bars 5 200 µm in A,C (also apply to B,D,
respectively).
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N. ASTE ET AL.
Fig. 6. A–D: Vasotocin (VT) gene-expressing neurons in the bed
nucleus of the stria terminalis (BSTm) of female (A,C) or male (B,D)
Japanese quail. The levels represented in A and B are comparable to
the drawing in Figure 1F. The level represented in C and D corresponds to Figure 1H. In the photomicrographs both small, weakly
labeled and large, intensely labeled (asterisks) neurons are visible.
Small neurons are present in the BSTm and medial preoptic nucleus
(POM), whereas large, intensely labeled neurons belong to the periventricular and lateral subdivisions of the magnocellular system. Scale
bar 5 200 µm.
VT-ir fibers also formed a less compact network in
females than in males (compare Figs. 3E and 4D with Fig.
7B,D), and VT-ir fibers were often seen surrounding negative cell bodies (compare Fig. 3G,D with Fig. 7B,D) in both
sexes.
A sexual dimorphism affecting the vasotocinergic perikarya was also observed at the level of gene expression.
The sex difference observed at this level, however, was not
as dramatic as the difference observed by using immunocytochemistry. VT gene-expressing neurons were present in
the BSTm of both sexes (Fig. 6), but, in males, the density
of grains on the autoradiography was obviously higher
over each cell than in females, suggesting a sex difference
in the amount of expressed mRNA per cell (compare Fig.
6A,C with Fig. 6B,D, respectively). This sex difference did
not appear to affect the magnocellular cell bodies.
sections just rostral to the CA. It then increased progressively in size at the level of the CA (Fig. 2I,J), and, in
sections caudal to this commissure, the group of ARO-ir
cells appeared as an oblique structure that extended from
the ventral tips of the lateral ventricles to the dorsocaudal
aspects of the POM, which is also identified by a dense
cluster of ARO-ir neurons (Fig. 2K). These two clusters of
cells eventually merged to form an extended group of
immunoreactive cells and then disappeared abruptly
(Fig. 2L).
The analysis of consecutive sections that were immunostained for VT or ARO indicated a clear topographical
overlapping between the area covered by the VT-ir structures and the area that contained ARO-ir neurons (compare Figs. 3F and 5A, respectively, with Figs. 3G and 5B).
ARO-ir cells were distributed uniformly and showed the
same morphological characteristics in the whole area (Fig.
3D, anterior BSTm; Fig. 5C, posterior BSTm). The ARO-ir
cells located in this region and those located in the POM
were observed to merge at the same rostrocaudal level
where the fusion of the VT-ir structures occurred (Fig.
5A,B). It must be stressed that ARO-ir cells were more
numerous by far than VT-ir cells in the BSTm.
Distribution of ARO-ir elements
In agreement with previously published studies (Balthazart et al., 1990b; Foidart et al., 1994, 1995b), a dense
cluster of ARO-ir cells was observed in the septopreoptic
region in the exact same location as the dense cluster of
VT-ir fibers (Fig. 2I–L). When moving in a rostral-tocaudal direction, this cell group was first observed in
DEFINITION OF THE NUCLEUS OF THE STRIA TERMINALIS IN BIRDS
151
Fig. 7. Vasotocin (VT)-ir structures in the septopreoptic region of
female Japanese quail. A,C: Low-power magnification of the rostral
(A) and caudal (C) parts of the bed nucleus of the stria terminalis
(BSTm; for comparison with the male, see Figs. 2G and 4B). No
immunoreactive cell body is visible. Asterisks indicate the intensely
stained magnocellular neurons (for comparison with in situ hybridization, see Fig. 6A,C). B,D: High magnification of the VT-ir fibers
observed in the female BSTm. Even at this magnification, no cell
bodies are visible, but in some cases, positive fibers surround negative
cell bodies. Scale bars 5 200 µm in A,C, 100 µm in B,D.
Analysis of Nissl-stained sections
could be made between the distribution of the densely
packed, Nissl-stained neurons and the distribution of
VT-ir fibers.
When it was observed in Nissl-stained sections, the
BSTm first appeared at its most rostral level as a dense
cell group located above and, to a lesser extent, below the
CA (Fig. 2A,B). At this level, the dense cluster of Nisslstained cells matched perfectly the group of ARO-ir cells,
but there was only a partial overlap with VT-ir structures:
The correspondence was good in the area dorsal to the CA,
but the Nissl-stained cell group located below the CA did
not correspond to matching VT-ir material (Fig. 2A,B,
E,F,I,J).
Caudal to the CA, the overlap between Nissl staining,
ARO-ir cells, and VT-ir cells and fibers was very reliable.
The staining of the BSTm increased gradually in a rostrocaudal gradient, reaching a maximum where the BSTm
merges with the POM (Fig. 4E). Visual inspection of the
sections did not reveal significant cytoarchitectural differences between the Nissl-stained cells of the POM and
those of the BSTm (Fig. 4A). When, at their most caudal
level, these two nuclei merge, they constitute a single,
oblique structure in which no subdivision can be made
based on cell characteristics (Fig. 4E).
A comparison of the sections stained by immunocytochemistry with the alternate Nissl-stained sections revealed the presence of a cluster of Nissl-stained cells that
had never been identified precisely before the topographical data derived from the immunocytochemical studies
were available. This cell group is characterized by a higher
cell density than the surrounding area and allows one to
define the extension of the BSTm. The cells in this cluster
are also stained in a slightly denser manner than in the
surrounding area.
Throughout most of the rostrocaudal extent of the BSTm
(Fig. 2A–D), a perfect match was observed between the
boundaries of this cell cluster: They could be drawn at low
magnification based on the distribution of either the VT-ir
fibers and cells, the ARO-ir cells, or the densely packed,
Nissl-stained cells (compare Figs. 3B and 4A,E, respectively, with Figs. 3C and 4B,F). However, in the rostral
part of the region, scattered ARO-containing cells were
also present outside the boundaries of the BSTm, and the
cluster of Nissl-stained cells was very small and was not
easily recognizable. At the very rostral tip of the BSTm
(rostral to the beginning of the CA), sometimes, no match
152
N. ASTE ET AL.
DISCUSSION
The present study describes the location and some
neurochemical characteristics of a region of the quail
forebrain that has been identified previously by different
names. Its rostral portion has been named the dorsal
diencephalon, the caudal paleostriatum pars ventralis, or
the septal area (Kiss et al., 1987; Voorhuis et al., 1988;
Balthazart et al., 1992a; Voorhuis and De Kloet, 1992;
Foidart et al., 1995b). This study also provides the first
evidence for the presence of a sexually dimorphic population of vasotocinergic neurons within this region of the
quail brain. The ARO-ir cells and the VT-ir cells and fibers
in this region can be considered as neurochemical markers
of a clearly recognizable cluster of Nissl-stained cells that
bear the anatomical characteristics of a nucleus. These
data further confirm the existence of a close association
between ARO-ir cells and VT-ir fibers that was observed
previously in the quail brain (Balthazart et al., 1997).
VP (the mammalian homologue of VT in birds) and ARO
are two neurochemical markers of the rat BSTm. This
nucleus is also defined as a part of the accessory olfactory
pathway due to its afferents, which originate from the
medial amygdala. The rat BSTm also shows special topographical relationships with the lateral portion of the CA
that are similar to those of the region investigated here.
Therefore, the data presented in this paper strongly
suggest that the cluster of Nissl-stained neurons that is
located dorsal to the CA and that matches the ARO-ir and
VT-ir structures fulfills the requirements to be identified
as the avian homologue of the BSTm.
Similarity of connections and
of topographical organization
A detailed description of the olfactory inputs to the
septopreoptic region of the avian brain was proposed
originally for the pigeon by Zeier and Karten (1971). In
that study, the authors defined the stria terminalis as a
portion of the dorsal occipitomesencephalic tract (OM) that
showed degenerating fibers ending in a region ventral to
the lateral septum and the lateral ventricle after lesions of
the posteromedial archistriatum, including the nucleus
taeniae. In more recent studies, which were performed
mainly in pigeons, the BST has been described as a
distinct, small, round region that bulges into the lateral
base of the lateral ventricle throughout nearly the entire
rostrocaudal extent of the paraolfactory lobe. At its most
caudal level, the BST extends laterally and ventrally
toward the archistriatal complex (see drawings and discussion in Veenman et al., 1995; Medina and Reiner, 1997).
However, this region was previously named the nucleus
accumbens (Karten and Hodos, 1967; Reiner et al., 1983),
whereas the name BST was employed to indicate different
parts of the septohypothalamic area or was not used at all
in some brain atlases (see above). A recent study (Veenman
et al., 1995; see Fig. 1) presented a graphical description of
the relative positions of the BST, paraolfactory lobe, and
nucleus accumbens in the pigeon basal telencephalon. The
same authors also emphasized that some neurochemical
characteristics are comparable between the pigeon BST
and the mammalian BST (Moga et al., 1989). In particular,
both are relatively poor in dopaminergic innervation
(Reiner et al., 1994) and in substance P-containing fibers
and cells (Reiner et al., 1983), whereas neurotensin fibers
and neurons are relatively abundant (Reiner and Carr-
away, 1987). In our previous studies in quail, we also
demonstrated a paucity of substance P-ir elements as well
as a prominent population of corticotrophin releasingfactor (CRF)-like-positive neurons in the same region
(Panzica et al., 1986; Aste et al., 1995). Tract-tracing
studies have also demonstrated a peculiar reciprocal connection of pigeon BST with the parabrachial region and
with the nucleus of the solitary tract (Arends et al., 1988;
Wild et al., 1990). Comparing these data in birds with the
wide literature in mammals (for a list of references, see
Moga et al., 1989), it appears that many of these characteristics are not typical to the entire BST but chiefly to its
lateral portion (BSTl). In particular, the BSTl is distinguished by its reciprocal connections with nuclei involved
in central autonomic regulation, including the parabrachial nucleus. Moreover, it is characterized by a large
population of CRF- and neurotensin-positive neurons (Moga
et al., 1989). Therefore, here, we propose to name this
region in the pigeon (and the quail homologue) the BSTl,
whereas the area that we have described in the present
study would be named the BSTm.
The name BST had been used previously to describe the
caudal portion of this region in quail (Balthazart et al.,
1990b, 1992a; Panzica et al., 1991, 1994; Foidart et al.,
1995b) as well as in other avian species (Kiss et al., 1987;
Balthazart et al., 1990b, 1996a; Voorhuis and De Kloet,
1992; Shen et al., 1995; Deviche et al., 1996; Jurkevich et
al., 1996, 1997). Topographically, the anterior portions of
the quail and the rat BSTm show similar relationships
with the lateral ventricle, the septal area, and the CA. In
particular, the BSTm is partitioned at this level by the
lateral edge of the CA, which creates a very characteristic
anatomical relationship. Similarly, the caudal portion of
this nucleus in quail and in mammals forms a structure
running from the ventral edge of the lateral ventricle to
the dorsolateral aspects of the periventricular region (De
Olmos et al., 1985; present study). Thus, overall, the
appearance and connectivity of the BSTm in mammals
and quail are very similar.
Neurochemical criteria
VP has been considered classically to be a useful marker
of the medial portion of the BST (De Vries and Buijs, 1983;
Miller et al., 1989). However, whether the population of
VP-ir cells and fibers is restricted to the BSTm or is only
most intense in this region is unclear. In the present study,
fibers immunoreactive for VT, the avian homologue of VP,
were shown to identify the full extent of the structure that
we suggest to be homologous to the mammalian BSTm. We
demonstrated also the presence of VT-ir cells in this brain
area, which provides an additional similarity with the
mammalian BSTm. The distribution of VT- or VP-ir cells
follows a similar rostrocaudal gradient in these two nuclei,
which are more abundant in their caudal aspects than in
their rostral aspects (Van Leeuwen and Caffé, 1983; Van
Leeuwen et al., 1985; present study). This differential
distribution allows a distinction between a rostral portion
of the nucleus (which shows a relatively low content in VPor VT-ir cells) and a caudal portion (where these neurons
are more abundant).
In the present study, a cluster of intensely Nissl-stained
cells was also observed just ventral to the lateral aspects of
the CA in a location that is reminiscent of the ventral
subdivision of the rat BSTm (Del Abril et al., 1987). This
portion of the BSTm contains VP-ir cells in rat (De Vries et
DEFINITION OF THE NUCLEUS OF THE STRIA TERMINALIS IN BIRDS
al., 1985; Van Leuween et al., 1985). By contrast, neither
VT-ir cells nor VT-expressing neurons were observed in
this specific position in the present study. Therefore, we
cannot discard the hypothesis that some other small areas
that do not contain VT-ir elements must also be viewed as
part of the BST.
Furthermore, it must be considered that, although VT
and VP can be regarded as a useful markers of the quail
and mammalian BSTm, interclass and interspecies differences may also occur. The BST of the male hamster, for
example, contains fewer VP-ir cells than the BST of the rat
(Ferris et al., 1995). Conspicuous interspecific differences
have also been reported in the BST of birds: VT-ir neurons
or VT gene-expressing cells are far more evident in this
region of the canary, zebra finch, chicken, and junco than
in the quail (Kiss et al., 1987; Voorhuis and De Kloet, 1992;
Aste et al., 1996; Deviche et al., 1996; Jurkevich et al.,
1997).
Incidentally, it must also be observed that the present
study, by using optimized immunocytochemical procedures for VT immunocytochemistry, has identified for the
first time the presence of a small number of VT-ir perikarya within the boundaries of the POM. The presence of
these cells was confirmed independently by using in situ
hybridization. Whether these VT-ir cells located in the
POM and BSTm are the origin of the immunoreactive
fibers that outline these two nuclei remains to be analyzed
experimentally with tract-tracing studies combined with
immunocytochemistry.
A high level of ARO activity has been reported to be
present in the BST of rats (Roselli et al., 1985; for recent
review, see Roselli et al., 1997). Surprisingly, however,
immunocytochemical studies have largely failed to identify high numbers of ARO-ir cells in this structure (Sanghera et al., 1991; Shinoda et al., 1994), with the exception
of one study by Jakab et al. (1993). This failure must be
due to technical problems associated with the relative lack
of specificity of antibodies, because more recent work using
in situ hybridization has confirmed that the rat BSTm can
be identified both during ontogeny and in adulthood by a
high density of ARO-expressing cells (Lauber and Lichtensteiger, 1994; Wagner and Morrell, 1996). Thus, the presence of a dense cluster of ARO-ir cells in the quail BSTm,
as defined here, provides additional evidence for the
homology of this nucleus with the mammalian BSTm.
The presence of ARO-ir cells or VT-ir fibers within the
boundaries of a nucleus (as defined by the observation of
Nissl-stained sections) had been reported previously only
for the POM (Balthazart et al., 1990a; Viglietti-Panzica et
al., 1994). Therefore, this nucleus shows considerable
similarities with the region investigated in this study. The
definition of the boundaries between the POM and the
BSTm has always represented a difficult question. In our
previous work, we decided to proceed operationally on the
premise that the POM ends caudally, where it fuses with
the dorsal cell group that we define here as the caudal
portion of the BSTm (Panzica et al., 1991). By using
neurochemical markers (ARO and VT), it is impossible to
distinguish two separate subpopulations at this level. It is
possible that the dorsocaudal POM and the ventral portion
of the BSTm fuse caudally in a single morphological
structure that is still composed of two functionally distinct
units. Alternatively the elongated structure might be
considered to be entirely part of the BSTm. The cytoarchitectonic and neurochemical criteria used in the present
153
study do not permit differentiation between these two
interpretations.
Two other neurochemical markers have been considered
to be typical of the mammalian BST (mostly in the BSTm):
galanin (Planas et al., 1994) and nitric oxide synthase
(Hadeishi and Wood, 1996). A subpopulation of galaninexpressing neurons is associated specifically with VP
neurons in the rat BSTm (Planas et al., 1995). In quail, the
distribution of galanin and its binding sites have been
studied recently (Azumaya and Tsutsui, 1996), but no
details have been provided concerning the presence of this
peptide in the region of the BST. In contrast, our study of
the distribution of nicotinamide adenine dinucleotide phosphate (NADPH)-diaphorase (the enzymatic activity associated with nitric oxide synthase) in the quail brain (Panzica
et al., 1994) described a population of positive neurons in a
region corresponding to the posterior part of the BSTm
(see Fig. 6B in Panzica et al., 1994). In the hamster,
NADPH-diaphorase activity is also highly concentrated in
the posterior BSTm (Hadeishi and Wood, 1996).
Sex differences
A comparison between the present data and previous
studies on other avian species indicates that the presence
of a sexual dimorphism in vasotocinergic elements is a
common feature of the BST, although interspecific differences do occur (for reviews, see Jurkevich et al., 1996;
Panzica et al., 1997). VT-ir cells or VT gene-expressing
cells are present in canary, zebra finch, and fowl in a region
corresponding to the quail BSTm (Kiss et al., 1987; Voorhuis
and De Kloet, 1992; Jurkevich et al., 1997). However,
neither VT-ir nor VT gene-expressing neurons were reported in the hen (Jurkevich et al., 1997), and no sexual
dimorphism in VT-ir structures has been reported in the
zebra finch (Voorhuis and De Kloet, 1992). VT-ir cells are
present in both sexes in the canary, but they are less
abundant in females than in males (Voorhuis et al., 1988).
This dimorphism observed in canaries is activational in
nature, in that testosterone administration to gonadectomized females increases the number of vasotocinergic
elements of this region to typical male levels (Voorhuis et
al., 1988). On the other hand, an analogous hormonal
treatment performed in gonadectomized female quail fails
completely to increase the vasotocinergic immunoreactivity of this region (Viglietti-Panzica et al., 1992). These data
suggest that the sexual dimorphism in VT-ir fibers in quail
depends in this species on an organizational effect of
gonadal hormones (Panzica et al., 1997).
The presence of a sexual dimorphism in the number of
VT-ir neurons and in the density of the in situ hybridization signal in the quail BSTm provides an additional
criteria that supports the homology of this region with the
mammalian BSTm. The number of the vasopressinergic
neurons in the rat BST, defined by using in situ hybridization or immunocytochemistry for the peptide, is higher in
males than in females (De Vries et al., 1985; Miller et al.,
1989; De Vries and Al Shamma, 1990). In contrast to our
results, De Vries et al. (1985) reported the presence of
VP-ir neurons in the BST of females. However, that study
and subsequent investigations on the rat vasopressinergic
system were based on colchicine-treated animals in which
the peptidergic concentration in the cell bodies was enhanced by blocking axonal transport (Van Leeuwen and
Caffé, 1983; De Vries et al., 1985; De Vries and Al Shamma,
1990). It is possible that the use of colchicine could also
154
enable us to see these cells in female quail, as suggested by
the fact that cells containing a low level of mRNA were
detected in the female BSTm. To our knowledge, no study
is available so far on the rate of VT gene transcription vs.
translation or on the stability of the mRNA for VT in the
two sexes of quail. The specific absence of VT mRNA
translation in female quail, therefore, cannot be ruled out
completely.
Functional significance of the quail BSTm
The vasotocinergic system of the quail BSTm that is
described in detail in the present study is known to be
exquisitely steroid-sensitive (Viglietti-Panzica et al., 1992).
A similar sensitivity to steroids has also been demonstrated for the VT-ir fibers in the lateral septum and in the
POM (Viglietti-Panzica et al., 1992, 1994; Panzica et al.,
1996a). All of these studies demonstrated a prominent
effect of testosterone, but it is not known at present
whether this steroid needs to be aromatized into an
estrogen in order to exert its effects, as shown previously in
mammals (De Vries and Duetz, 1984; De Vries et al., 1986,
1994b; Brot et al., 1993). This may be the case, because
numerous estrogen receptors containing cells are present
in the area (Watson and Adkins Regan, 1988; Balthazart et
al., 1989). However, we do not know at this point whether
these estrogen receptors are colocalized specifically with
VT. The VT-ir innervation of these regions decreases
whenever a drop in circulating testosterone occurs, either
after surgical castration (Viglietti-Panzica et al., 1992,
1994), after exposure to a short-day photoperiod, or during
aging (Viglietti-Panzica et al., 1992; Panzica et al., 1996a).
This effect can be reversed completely by testosterone
replacement therapy or by exposure to a long-day photoperiod (Viglietti-Panzica et al., 1992, 1994; Panzica et al.,
1996a).
The location of VT-ir cells that give rise to the steroidsensitive fibers innervating the lateral septum, the BSTm,
and the POM is unknown. In rat, the vasopressinergic
innervation of the lateral septal area is also sexually
dimorphic, testosterone-sensitive, and affected by aging
(for reviews, see De Vries et al., 1994a; De Vries, 1995).
These aspects of the septal vasopressinergic innervation
correlate qualitatively with those of VP-ir or VP geneexpressing cells in the BST and in the medial amygdala, so
that these two nuclei are supposed to be the major source
of the septal vasopressinergic innervation (De Vries et al.,
1984, 1994a). Based on the available data in quail, it is
impossible to identify the cell bodies that are responsible
for the VT-ir innervation of the POM, lateral septum, and
BSTm. VT-ir cells are present in large numbers in the
caudal part of the BSTm and, to a lesser extent, in the
rostral part of this nucleus and in the POM. Tract-tracing
studies have demonstrated a reciprocal connection between the POM and the lateral septum (Panzica et al.,
1992b; Balthazart et al., 1994; Balthazart and Absil,
1997), but no evidence is available so far for the existence
of projections from the BSTm to the POM and septum.
Additional work should be performed to answer this
question.
The sex differences and steroid-induced changes in VT
immunoreactivity closely parallel changes of male sexual
behavior that are observed in the same situations. These
correlations may suggest that VT is actually implicated in
the control of copulatory behavior, as also indicated by
hodological and recent pharmacological evidence (Panzica
N. ASTE ET AL.
et al., 1992b; Balthazart et al., 1994; Balthazart and Absil,
1997; Castagna et al., 1998). The specific part of the quail
vasotocinergic system that is implicated in behavior control, however, has not been identified so far. Electrolytical
lesions or testosterone implantation in the POM exert
potent effects on male copulatory behavior in quail, but the
same manipulations aimed at the anterior part of the
BSTm do not appear to have major behavioral effects
(Balthazart and Ball, 1997). In mammals, the BSTm is
implicated in the regulation of several behavioral systems,
including male copulatory behavior and maternal behavior. This nucleus receives sensory inputs mainly from the
olfactory centers and projects to the medial preoptic area.
This projection is supposed to modulate the motivational
aspects of reproductive activities (Emery and Sachs, 1976;
Valcourt and Sachs, 1979; Claro et al., 1995). However, the
specific role of the VP circuitry originating in the BST in
the control of these behaviors still remains to be demonstrated.
In quail, the presence of afferent connections from the
archistriatum to the BSTm (Balthazart and Absil, 1997),
together with the functional and morphological data collected in mammals, suggests a possible participation of the
BST in the elaboration of limbic information. The archistriatum, specifically, the nucleus taeniae (the avian homologue of the medial amygdala of mammals), is known to
receive olfactory inputs, at least in pigeon (Reiner and
Karten, 1985). The significance of putative olfactory and/or
pheromonal inputs to the quail BST, however, remains to
be assessed. Although the importance of the olfactory
perception in birds is still a matter of discussion, some
studies support the hypothesis that olfaction may play a
modulatory role in the control of avian reproductive activities or other behaviors (Balthazart and Schoffeniels, 1979;
Papi, 1989; Papi, 1990; Burne and Rogers, 1996; Jones and
Roper, 1997).
In conclusion, this paper provides a clear anatomical
definition and neurochemical characterization of the medial portion of the BST in the quail brain and supports the
notion that this nucleus is homologous to the mammalian
BSTm. In view of the involvement of the mammalian
BSTm in the control of different aspects of reproductive
activities, it will be important now to determine whether
this structure plays a similar role in the control of quail
reproduction.
ACKNOWLEDGMENTS
N.A. was a 3-month fellow of ESF in Celle.
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