Chem. Senses 24: 127-136,
1999
© Oxford University Press 1999
The Vomeronasal Organ of the Male Ferret
1 Department of Neurobiology and Physiology, Northwestern University, 2153 North Campus Drive, Evanston, IL 60208-3520, USA 2 Eberhard-Karls-Universität Tübingen, Tierphysiologie, Auf der Morgenstelle 28, 72076 Tübingen, Germany
Correspondence to be sent to: Dr Albert I. Farbman, Department of Neurobiology and Physiology, Northwestern University, 2153 North Campus Drive, Evanston, IL 60208-3520, USA. e-mail: afarbman{at}nwu.edu
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Abstract |
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The vomeronasal organ (VNO) is known to play a major role in sexual behavior in many mammals. This study is the first report that the adult male ferret has a VNO, which is considerably smaller and morphologically different from the usually crescentshaped epithelium in several mammalian species, particularly rodents. There were no differences in the size or structure of the ferret VNO between the mating season in spring and the sexually quiescent season in autumn, although plasma testosterone, testis size and brain size are dramatically increased in spring and behavior changes significantly. The histological data suggest that the VNO might be not as important a structure in male ferret sexual behavior as in rodents.
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Introduction |
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TopAbstractIntroductionMaterials and methods ResultsDiscussionAcknowledgementsReferences |
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The vomeronasal organ (VNO) plays a major role in the perception of stimuli related to social and/or reproductive behavior in many species of vertebrates (for review see Estes, 1972
; Wysocki, 1979, 1989; Meredith, 1983; Halpern, 1987). The morphology
of the VNO has been investigated in some detail in rodents (Gratiolet, 1845; Addison and Rademaker, 1927; Vaccarezzaet al., 1981), dogs (Klein, 1881; Read, 1908; Ramser, 1935; Adams and Wiekamp, 1984), cats (Harwey, 1882; Schwink, 1888; Herzfeld, 1889; Broom, 1900; Read,
1908; Seifert, 1971; Wöhrmann-Repenning, 1989; Wöhrmann-Repenning and
Ciba, 1989; for reviews see Zuckerkandl, 1910; Dawley, 1998) and minks (Salazar et al., 1994).
The VNO, also known as Jacobson’s organ because it was first described by Jacobson in 1811, is a paired, nonconnected, unbranched tube-shaped
structure located in the anterior region of the nose within the ventral end of the nasal septum. It is
generally enclosed in a bony or cartilaginous capsule. In carnivores it opens at its anterior end
into the incisive or nasopalatine duct (Starck, 1978), thus connecting with
the oral and nasal cavity. At its posterior extent it ends blindly (Adams and Wiekamp,
1984). The VNO consists of a sensory and a non-sensory epithelium lining the
medial and lateral side of the tube respectively. The sensory epithelium in mammals is usually
crescent-shaped (Addison and Rademaker, 1927; Adams and
Wiekamp, 1984; for review see Farbman, 1992) and is an
arrangement of a pseudostratified epithelium, containing the microvilli-bearing sensory neurons
(for review see Menco, 1997), basal cells and supporting cells with nuclei
in the apical compartment (Vaccarezza et al., 1981; Garrosa and Coca, 1991). The axons of the sensory neurons collect in the lamina
propria beneath the epithelium into a small number of nerve bundles which ascend in the nasal
septum and pierce the cribriform plate, then project along the medial aspect of the main olfactory
bulbs to their target, the accessory olfactory bulbs (McCotter, 1912).
The European polecat (Mustela putorius L.) is a mammalian carnivore which lives a
solitary life except during the annual spring mating season (Marshall, 1905). In the polecat and its domesticated form, the European ferret (Mustela putorius
f. furo L.), the reproductive cycle is reflected in the seasonal variations of many anatomical,
behavioral and physiological parameters (Kästner and Apfelbach, 1987; Weiler, 1992). In spring the testes in males become
significantly enlarged and produce spermatozoa (Neal et al., 1977). Male ferrets have to find their mating partners and—as nocturnal
animals—are known to depend predominantly on olfactory cues (Wheeler,
1978; Apfelbach, 1986). The main olfactory system is very
well developed and has been intensively studied (Apfelbach and Weiler, 1985; Apfelbach, 1986; Rehn et al., 1986; Weiler, 1986, 1993; Voigt, 1987; Apfelbach and Schmidt, 1989; Schmidt, 1989). In contrast, the accessory olfactory system has not been intensively
investigated in this species. Although a very small accessory olfactory bulb was reported to be
present (Lockard, 1982, 1985; Fox,
1988), a VNO has not, to our knowledge, been described in the adult male ferret.
The purpose of the present study therefore was to determine whether a VNO is present in adult male ferrets and, if so, whether it undergoes morphological changes between sexually active and quiescent seasons. In addition, the serum testosterone was measured during the two seasons to verify that the males were primed for sexual activity. The histological studies revealed that a rudimentary VNO is present and does not undergo morphological changes seasonally although there is a dramatic increase in plasma testosterone in the mating season.
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Materials and methods |
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Animals
All ferrets investigated in the present study were taken from the breeding colony of the University of Tübingen (Germany). Animals were kept under natural light and temperature conditions, and cared for by specially trained animal-care personnel.
‘Adult’ refers in this study to animals 1-3 years of age. Body weight changes
seasonally (Weiler, 1992).
Testosterone quantification
Blood collected from the tail vein was analyzed to determine the plasma concentration of testosterone by radioimmunoassay. In the spring 54 ferrets were used, and in the autumn, 38. The antiserum reacted 100% with testosterone whereas the cross-reactivity with dihydrotestosterone (DHT) was 54%. In order to obtain sufficient sensitivity, it was necessary to remove the sex steroid-binding proteins from the samples. Ether was used for extraction of steroids. After addition of the tracer (3H-labeled DHT) and reaction with the antibody until equilibrium was achieved, free and bound androgens were separated by adsorption of the free steroids by dextran-coated charcoal followed by centrifugation. Chemicals were obtained from Mallinckrodt Diagnostica, Dietzenbach, Germany.
Histological preparation and analysis
For the histological studies adult male ferrets were used in spring (high testosterone level)
and autumn (low testosterone level); in addition newborns were investigated for developmental
aspects (see Table 1). Ferrets were injected i.p. with a lethal dose of
Nembutal®. Under deep anesthesia, ferrets were perfused intracardially with a
physiological saline solution at room temperature to clear the vessels of blood, followed by a
fixative solution containing 2.5% glutaraldehyde and 1% paraformaldehyde in 0.1 M phosphate
buffer (Karnovsky, 1965). Heads were skinned and postfixed overnight.
As much as possible of the skull bones was removed before decalcifying the noses in 5% EDTA
in 0.1 M Sørensens phosphate buffer for several days. Snouts were embedded in
Paraplast
® and sectioned at 10µm in a frontal plane from the tip of the snout to the posterior
end of the olfactory epithelium. Each section was preserved; every 10th section was placed on
silane-treated slides and stained with hematoxylin and eosin. For the newborns every section was
stained. Sections were examined with a lightmicroscope at a magnification of x400 and
measurements performed with a calibrated ocular micrometer.
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The sections were screened to note two landmarks: (i) the anterior end of the VNO where it opens into the nasopalatine duct; and (ii) the posterior end where the VNO ends in a one-cell-deep epithelium as the duct of glands. The sensory epithelium was defined by the clear distinction of a supporting cell nuclear layer from a neuronal nuclear layer and the number of sections containing sensory epithelium was used to measure its anterior–posterior extent.
The thickness of the sensory and non-sensory epithelia, from the basement membrane to the luminal surface, was measured in each section half way along their length. In addition, in sections with sensory epithelium, the thickness occupied by neuronal nuclei was measured and the percentage of the whole thickness was calculated.
The length of lateral (non-sensory) and medial (sensory) epithelium in its dorso-ventral
extent was measured in each section. Because the epithelial thickness around the tube in a section
was nearly constant from dorsal to ventral, the area was calculated by multiplying the epithelial
thickness by the length. The volume of the VNO was then calculated by multiplying the extent
by
the area. The volumes of the sensory and non-sensory epithelium were calculated separately. In
addition the volume of the lumen was determined by measuring the length (a) and width
(b) of the oval-shaped space and calculating the area in each section using the formula
/4ab (Segovia et al., 1984).
For the newborns we used the analySIS morphometric system connected to a CCD camera on a Zeiss microscope at a magnification at x400; this allowed us to measure area and thickness semiautomatically.
For statistical analysis to determine whether there was a significant difference between the
values of spring and autumn we used the Mann–Whitney U test (Lienert, 1973).
OMP immunohistochemistry
Paraplast® sections were deparaffinized, rehydrated in phosphate-buffered
saline (PBS) and incubated sequentially at 37°C in a blocking solution of normal rabbit
serum and PBS 1:1 (30 min), the antibody against OMP (goat 
-OMP, dilution 1:500, 60
min; a gift from Dr F. Margolis, University of Maryland, Baltimore, MD), the Vectastain Kit
(Vector Labs, Burlingame, CA) containing biotinylated rabbit anti-goat antibodies (30 min) and
the avidin–biotin complex (ABC) reagent (45 min). Each antibody treatment was
followed by a 15 min wash with PBS at room temperature. Specimens were then incubated for 5
min at room temperature in a freshly made solution containing 0.01% H2O2 and 0.05% 3,3'-diaminobenzidine (DAB) in 0.1 M Tris–HCl buffer, pH
7.5, to visualize the immunoreactivity. PBS was substituted for the primary antibody in the
negative control slides.
BrdU immunohistochemistry
For proliferation studies, some animals were injected i.p. with a single dose (50 mg/kg body
wt) of 5-bromo-2'-deoxyuridine (BrdU; Sigma B 5002, Sigma-Aldrich Chemie GmbH,
Deisendorf, Germany) 1 h before perfusion. The fixative was 4% paraformaldehyde in 0.1 M
Sørensen's phosphate buffer. Following standard histological procedures, sections
were placed under a UV light for 2 h (to enhance the BrdU signal; Weiler and
Farbman, 1997),
deparaffinized and rehydrated. Endogenous peroxidase was inactivated by incubation of the
slides in 3% H2O2 in methanol for 30 min at room temperature. After
several washes in PBS, sections were treated with trypsin (0.1% trypsin, Sigma T-8642, 0.1%
CaCl2 in 0.05 M Tris buffer for 5 min at room temperature) to increase the signal of
the antibody reaction (Hayashi et al., 1988), then washed several
times in PBS. Sections were then incubated at 37°C in a 1:1 mixture of normal horse serum
and 0.1 M PBS to block non-specific binding (60 min), then overnight at 4°C in an antibody
against BrdU (Amersham anti-bromodeoxyuridine solution, containing mouse monoclonal
antibody and a
nuclease, Amersham RPN 202, Amersham Life Science, Arlington Heights, IL) diluted 1:10 in
PBS, and sequentially at 37°C with the Vectastain Elite Kit for mouse antibodies (Vector
Labs) containing biotinylated horse anti-mouse secondary antibody (30 min) and the ABC
reagent (45 min). Each antibody treatment was followed by a 15 min wash with PBS at room
temperature. Specimens were then incubated as above in a solution containing H2O2 and DAB in Tris–HCl buffer to reveal the BrdU immunoreactivity. To stop
the reaction, specimens were placed in distilled water, washed several times and dehydrated in
increasing concentrations of ethanol before being mounted with Permount® and
coverslipped.
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Results |
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TopAbstractIntroductionMaterials and methods ResultsDiscussionAcknowledgementsReferences |
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Hormonal data
Quantification of the testosterone level was performed in plasma of males between 1 and 3 years of age in spring and in autumn. There were no differences among the ages, therefore the values were taken together. However, there was a dramatic seasonal difference. In spring the testosterone plasma concentration was 2072 ± 215 pg/ml (mean value ± SE) while in autumn the concentration was only 397 ± 28.4 pg/ml. The difference between spring and autumn is statistically highly significant (P< 0.001).
Histological observations and data
Location, orientation, gross morphology and histological structure
A small VNO can be detected in adult male ferrets (Figure 1). As in other mammals, the VNO of the ferret is a paired, non-connected, elongated, unbranched tubular organ, located in the anterior part of the nose within the ventral septal wall (Figure 2A). Partially encapsulated by a layer of cartilage, it opens anteriorly via a narrow duct into the incisive canal (ductus nasopalatinus), as in other carnivores. Posteriorly it ends in a duct-like structure which branches to the ducts of caudally located glands.
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In contrast to other mammals, the VNO of the male ferret does not appear crescent-shaped in a frontal section but is more tubular. The epithelium lining the medial wall is thicker than that lining the lateral wall (Figure 2B). The anterior end of the tube, where it opens into the nasopalatine duct, is between 11.5 and 13.5 mm from the tip of the nose and lined by a stratified squamous epithelium. The medial side (which more posteriorly will become the presumptive sensory epithelium) always shows a thicker epithelium than the lateral, non-sensory aspect (Figure 3). About 1 mm posterior to the nasopalatine opening, the medial epithelium has changed from a stratified squamous epithelium to a pseudostratified columnar epithelium, and an apical supporting cell layer can be distinguished from the neuronal nuclear layer beneath (Figure 2C). The surface of this sensory epithelium changes from a smooth to a ‘hairy’ appearance. The epithelium on the lateral side also becomes columnar (Figure 2D) and remains columnar throughout most of the length of the VNO. On the posterior end of the VNO the epithelium becomes a single layer of cuboidal cells which represents the common duct of posteriorly located glands. The sensory epithelium is located on the medial wall throughout its extent; it does not shift posteriorly to a ventral position, in contrast to other mammals, where a 90° rotation in the orientation is seen (Zuckerkandl, 1910
; Barber and Raisman, 1978;
Vaccarezza et al., 1981). The extent of the VNO from anterior
to posterior is on average
2.73 ± 0.32 mm.
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Epithelium thickness, area and volume
The values for epithelial thicknesses, areas and volumes are listed in Table 1. There were no significant differences between the right and left sides (with one exception; see below, Unusual features) of the animals for any measured parameter. Therefore the individual adult VNOs were combined in the table. No significant differences between males at different hormonal status (spring, autumn) could be detected in the averages of most of the measured parameters (Table 1).
In the sensory epithelium only ~60% of the thickness is occupied basally by neuronal nuclei. The remainder consists of two zones, the elongated nuclei of supporting cells which span a very dense band and a small nuclear free zone in the apical region (Figure 2C, E). The non-sensory epithelium is organized differently: there are no rows of neuronal nuclei (Figure 2D, F).
From anterior to posterior the epithelium on both sides of the VNO-tube increases in thickness even before a sensory epithelium is distinguishable on the medial side (Figure 3), and further posteriorly the thickness remains relatively constant before it drastically decreases on its posterior end to become a one-cell layer epithelium of a glandular duct. The proportion of epithelium thickness occupied by neuronal nuclei to the whole sensory epithelial thickness is constant throughout the anterior–posterior extent (Figure 3). The non-sensory epithelium also increases in thickness from anterior to posterior but then decreases faster, commencing from the anterior third of the organ to the posterior end (Figure 3).
The area of sensory and non-sensory epithelium per section (Figure 4) increases from anterior to posterior rapidly but then decreases because of the decrease in lumen size.
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Histological observations
In the sensory epithelium mitotic figures were observed infrequently and were randomly
distributed, close to the basement membrane. The distribution of BrdU-immunoreactive cells was
similar (Figure 5). Condensed nuclei (probably apoptotic cells) were also
seen, but higher in the
epithelium (Figure 2E). We did not observe intruding capillaries into the
epithelium nor piercing
glands through the epithelium as has been reported in the rodent VNO (Weiler et
al., 1999).
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In the non-sensory epithelium cells with round nuclei were interspersed with cells having an elongated spindle-shaped nucleus; polymorphonuclear leucocytes were frequently observed (Figure 2F).
Developmental aspects
The morphometric parameters in the newborns are listed in Table 1. Notably the thickness ratio of non-sensory to sensory epithelium in newborns was ~28%. During postnatal development, the thickness of non-sensory epithelium increases more than that of the sensory epithelium so that the non-sensory epithelium reaches ~60% that of the sensory epithelium in adults. In the newborn VNOs it is very difficult to distinguish a borderline between neuronal and supporting cell rows and therefore no data are included in the table for neuronal layer thickness.
OMP staining
Mature sensory cells of the VNO in mammals usually express olfactory marker protein
(OMP) (Farbman and Margolis, 1980; Johnson et al.,
1993; Tarozzo et al., 1998). The OMP
immunohistochemical reaction was positive in some cells of the sensory
epithelium although it appeared weak (Figure 6). Non-sensory epithelium
and the negative control were not stained.
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BrdU labeling
The sensory and non-sensory epithelium of the VNO showed BrdU-positive nuclei (Figure 5). Basal cells and supporting cells were stained. The staining appeared to be randomly distributed in contrast to the adult rodent VNO, where most proliferating cells appear in the edges of the sensory epithelium adjacent to the non-sensory epithelium. The non-sensory epithelium seemed to contain even more BrdU-positive nuclei than the sensory epithelium and seemed to be more basally located. In the sensory epithelium, sometimes clusters of labeled cells are found; this was never observed in the non-sensory epithelium.
Unusual features
In one animal in spring we observed on one side that the epithelium lining the vomeronasal tube appeared to be sensory epithelium all around (Figure 7A). No non-sensory epithelium faced the sensory epithelium opposite. OMP staining confirmed this observation (Figure 7B). However, this pattern was seen only in the middle part of the organ. Anteriorly and posteriorly there was non-sensory epithelium in its typical location and extension. The VNO of the other side of that particular animal was typical, with sensory epithelium on the medial side and non-sensory epithelium on the lateral side.
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Discussion |
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TopAbstractIntroductionMaterials and methods ResultsDiscussionAcknowledgementsReferences |
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This study is the first to describe the existence of a VNO in the adult male ferret. Our results show that it is a small, rudimentary structure, compared with that of rodents. Moreover, there are no apparent morphological differences between the mating and the sexually quiescent seasons, although there are significant differences in physiological parameters [the testosterone level and the metabolic rate (Kästner and Apfelbach, 1987
)], as well as in
morphological parameters, e.g. brain size and weight and testis size and weight (Weiler, 1992), and in behavior (Mauz, 1985). Is the VNO in the ferret functional?
An adult male ferret has a body wt of >1 kg, but the length of its VNO is only 2.7 mm,
comparable to the length of the VNO in a 10 day old 10 g hamster (Taniguchi et
al., 1982) and far less than the 7 mm VNO of the albino rat (Addison and Rademaker, 1927; Weiler et al., 1999)
or the 6 mm VNO of the chinchilla (Oikawa et al., 1994).
Correlated with the smaller length, the volume of the sensory epithelium in the male ferret VNO
is 0.14 mm3, much less than that of a rat and even less than the VNO in a mouse of
25–30 g body wt (Wilson and Raisman, 1980). It is also smaller
compared with other carnivores (for review see Dawley, 1998).
In addition to its small size, several other histological facts suggest that the VNO in ferrets is rudimentary compared with that of other animals.
- The epithelium is very thin, approximately the thickness of the VNO of a 13 day
rat embryo (Yoshida et al., 1993).
- Only about three rows of neurons are seen.
- The ratio of the volumes of sensory to non-sensory epithelium is ~1.7:1, comparable to
that described for the immature VNO in rat embryos (Garrosa et al., 1986, 1992; Yoshida et al., 1993). The ratio is considerably higher in the adult rat.
- Proliferating cells in the developing VNO in the mouse and rat are found throughout the
epithelium (Cuschieri and Bannister, 1975; Weiler et al., 1999) but are concentrated on the edges of the sensory epithelium adjacent to
the non-sensory epithelium in the mature VNO (Barber and Raisman, 1978; Weiler et al., 1999). In the ferret, mitotic figures as
well as BrdU-labeled cells were found infrequently, but were distributed near the basement
membrane, again similar to an immature stage.
- We did not observe intruding capillaries in the sensory epithelium of the ferret VNO as
described for other mammals (Cuschieri, 1974; Barber and
Raisman, 1978; Wilson and Raisman, 1980; Breipohl et al., 1981; Vaccarezza et al., 1981; Taniguchi and Mochizuki, 1983; Garrosa et
al., 1986, 1992; Mendoza and Szabo, 1988; Szabo and Mendoza, 1988; Yoshida et al., 1993; Berghard and Buck, 1996; Weiler and
Farbman, 1998). Intruding capillaries usually reflect a high metabolic activity (Cuschieri, 1974; Vaccarezza et al., 1981). Their absence suggests a low metabolism and is described in species with a thin epithelium in
which the VNO seems not to play an important role in behavior (Schilling, 1970; Jordan, 1972; Loo and Kanagusuntheram, 1972; Bhatnagar, 1980; Mendoza et al., 1994). In species with a functionally important VNO, capillaries usually intrude
prenatally
when the VNO has reached a certain developmental stage (Breipohl et al.,
1981).
- In the newborn ferret a rudimentary VNO can be detected (Kabioll, 1989). During postnatal development the volume of non-sensory epithelium increases
more than the sensory volume. However, compared with the body size increase of ~200 times
between newborn and adult, the VNO volume increases only about 60 times.
- An accessory olfactory bulb, the target of the vomeronasal nerve, has been reported to be
very small in the ferret (Lockard, 1982, 1985; Fox, 1988).
- In contrast, the main olfactory system in the ferret is very well developed, the olfactory
bulbs comprising about 5% of the whole brain (Weiler and Apfelbach, 1995). In male ferrets, seasonal, hormone-dependent changes occur in the total brain
weight (Weiler, 1992) whereas the VNO shows no major differences
between spring and autumn. The epithelium in spring seems to be even thinner and the volume of
the lumen slightly bigger. The number of neurons and of OMP-positive neurons are relatively
small compared with those seen in rodents.
Thus, the overall relative size and rudimentary appearance of the male ferret VNO compared with that of animals in which the VNO plays a role in sexual behavior suggest it has a more limited function.
Male ferrets show signs of agitation as well as an increase in exploratory behavior and
vocalization when placed in an open field in which a female ferret in estrous had been previously
introduced and then removed (Cowley, 1978). But male ferrets have to
learn the odor of estrous females; only sexually experienced males prefer the odor of estrous
versus non-estrous or male odor (Mauz, 1985). Therefore there might be
no preprogrammed chemical signal for pheromones detected by the VNO as proposed in the
hamster (Keverne et al., 1986), where the VNO
is very well developed (Winans and Powers, 1977) and plays a critical
role in mediating sexual
behavior (Powers and Winans, 1975). In the present study on the ferret
VNO and in an earlier study on its main olfactory organ we discerned no distinguishable
morphological changes
between spring and autumn (Weiler and Bensemann-Ryvkin, 1995). If
the VNO plays a role in male ferret sexual behavior it is not reflected in discernible
morphological changes in the mating season, comparable to the dramatic increases in brain and
testis sizes associated with mating in this species.
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Acknowledgements |
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TopAbstractIntroductionMaterials and methods ResultsDiscussionAcknowledgementsReferences |
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We are thankful to Dr Dagmar Kästner and Mr Robert Winkler for helping in the hormonal analysis. The antibody against OMP was generously provided by Dr Frank Margolis. This study was supported in parts by grants from the Deutsche Forschungsgemeinschaft DFG Ap 14/8 and NIH Grants P01 DC 00347 and R01 DC 02126.
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Accepted November 3, 1998
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