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Serotonin-containing projections to the mesencephalic trigeminal nucleus of the cat.

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THE ANATOMICAL RECORD 241:136-142 (1995)
Serotonin-Contai ning Projections to the M esenceph alic TrigeminaI
Nucleus of the Cat
Department of Anatomy, Histology, and Embryology, Medical University,
Stara Zagora, Bulgaria
Background: It is well known that the mesencephalic
trigeminal nucleus (MTN) neurons transmit somatosensory information
from proprioceptors in the oral-facial region. Several mechanisms of sensory transduction in these specialized receptors have been proposed, but
the neurotransmitters which are responsible for mediating proprioceptive
information are still unknown. The current study concentrates on the distribution of one putative neurotransmitter system, serotonin (SER),in the
cat MTN. A second objective was to clarify the location and sources of
serotoninergic projections on the MTN neurons.
Methods: To determine whether SER was localized in the MTN, the peroxidase-antiperoxidase (PAP) immunocytochemical technique was applied
at light and electron microscopic levels in colchicine-treated animals. The
origin of SER-containing fibers in the MTN was studied using a doublelabeling method combining retrograde transport with wheat germ agglutinin conjugated to horseradish peroxidase (WGA-HRP)and SER immunocytochemistry.
Results: There were no SER-containing neurons in the MTN. The cell
bodies of immunonegative MTN neurons were closely surrounded by fine
SER-positive fibers and terminals. The labeled fibers were in most cases
very thin and sometimes varicose. Ultrastructurally, direct synaptic contacts between SER-containing terminals and perikarya of MTN neurons of
all sizes could be seen. The majority of SER-labeled structures were synaptic terminals in which the immunoreactive material was located within
the small round clear as well as the small granular vesicles (diameter 50-80
nm) and a few large dense-cored vesicles (up to 150 nm). Retrograde tracing
demonstrated that most of cells in the nuclei raphe dorsalis, pontis and
magnus were WGA-HRP-labeled.
Conclusions: These results indicated that MTN neurons received serotoninergic projections from the raphe nuclei of the brainstem. In light of
these morphological data, it is concluded that the MTN of the cat is under
the influence of SER-containing axons and this serotoninergic input may
modulate MTN neuronal activity at the first synaptic relay.
0 1995 Wiley-Liss, Inc.
Key words: Mesencephalic trigeminal nucleus, Serotonin, WGA-HRP, Retrograde tracing, Immunocytochemistry, Cat
The mesencephalic trigeminal nucleus (MTN) is a
unique sector of the central nervous system. The cell
bodies of primary sensory neurons composing this IIUcleus are situated within the rostra1 pons and all rostro-caudal levels of the entire midbrain.
A characteristic peculiarity of the MTN in the cat is
that about 40% of mesencephalic neurons are multipolar and only 60% of the population of first-order sensory neurons are (pseudo)unipolar (Walberg, 1984; Nomura et al., 1985). The peripheral processes of MTN
neurons, running in the trigeminal nerve, reach the
spindles of the masticatory muscles and periodontal
mechanoreceptors (Shigenaga e t al., 1988a,b).
Therefore, morphologically and functionally MTN
neurons are considered to be very similar or identical
to the cranio-spinal ganglion cells. In contrast to sensory ganglia, however, where no synaptic contacts on
somata and processes of primary sensory neurons have
been detected, axosomatic and axodendritic synapses
Received December 29, 1993; accepted July 8, 1994.
Address reprint requests to Christo N. Chouchkov, Department of
Anatomy, Histology, and Embryology, Medical University, 11 Armejska Street, 6003 Stara Zagora, Bulgaria.
have been found in the MTN (Nomura et al., 1985). into the fourth ventricle. These animals were allowed
Recently, Liem et al. (19921, examining the distribu- to survive for 24 h. A fifth cat was used a s control
tion of synaptic boutons in the MTN of the rat, sug- (without colchicine). Under pentobarbital anesthesia
gested that these synaptic boutons contained peptider- (30-40 mg/kg, i.p.1, the animals were fixed by perfugic, dopaminergic, or serotoninergic vesicles. The sion through the ascending aorta with 600 ml of hepexistence of a synaptic input to the primary sensory arinized phosphate buffered saline (PBS), immediately
ganglion cells would suggest a n integrative function followed by 3 I of fixative-4% paraformaldehyde in 0.1
for the MTN to proprioceptive information carried by M phosphate buffer (PB) at pH 7.4 for light microscopy
primary trigeminal afferents.
(LM) and a fixative mixture containing 4% paraformalSeveral studies have dealt with the chemical content dehyde, 0.08% glutaraldehyde, and 0.15% picric acid in
of MTN neurons of the rat, and some neurotransmit- 0.1 M PB, pH 7.4, for electron microscopy (EM). The
ters and neuropeptides have recently been suggested brainstems were separated from the brains and placed
(Copray et al., 1990a,b, 1991; Ginestal and Matute, for 4-24 h in the same fixative (without glutaralde1993). Information about the serotoninergic innerva- hyde for EM). They were then washed in a series of cold
tion of MTN neurons is available for the rabbit a s well sucrose solutions overnight. Serial frontal sections
(Kolta et al., 1993).Unfortunately, studies on the neu- (20-40 pm) were cut on a Vibratome (Lancer Series
rotransmitter distribution in the MTN of the cat are 1000) and processed for LM and EM immunocytochemlacking, and the neurotransmitters which are respon- ical staining, respectively, using the conventional persible for mediating proprioceptive information are still oxidase-antiperoxidase (PAP) technique (Sternberger,
unknown. There is only a light microscopic study 1986).
(Tashiro et al., 1989) which has demonstrated that
The sections were incubated with a 1:1,000 dilution
perikarya of MTN neurons of the cat are often in direct of rabbit primary antiserum to serotonin, purchased
contact with axonal varicosities showing enkephalin-, from INCSTAR (Stillwater, Mn; lot no. 8832021), for 24
substance P-, or serotonin-like immunoreactivity. h a t room temperature and 24 h at 4°C. As a second
However, the source of these fibers and the physiolog- antibody a n anti-rabbit IgG (1:50) and in the third
ical significance of these findings for the functioning of step of the staining a rabbit PAP (1:200) (both from
MTN neurons has remained unclear. As the available Dakopatts, Glostrup, Denmark) were applied. The perdata on the distribution of neurotransmitter candi- oxidase activity was demonstrated by incubating the
dates in the cat MTN are scanty, we have started to sections in 0.4 mg/ml 3,3'-diaminobenzidine tetrahyelucidate the potential neurotransmitters and the drochloride (DAB) and 0.01% H,O, in 0.05 M Tris-HC1
source of synaptic connections.
buffer, pH 7.54, for 10 min. Between the separate steps,
In the present study, we have described the origin of the sections were rinsed with cold PBS t 0.3% Triton
the serotonin (SER)-containing axons in the MTN of X-100. Some of them were mounted on gelatin-coated
the cat. For this purpose, we used a very sensitive ret- glass slides, dried, dehydrated, coverslipped with Enrograde tracing technique (that can be combined with tellan, and examined in a Zeiss research microscope.
SER immunocytochemistry) with horseradish peroxiFor ultrastructural analysis, after the DAB incubadase a s a retrograde tracer in colchicine-treated ani- tion, some sections were postfixed for 30 min in 0.5%
mals. A preliminary report has been published in ab- OsO, buffered with 0.1 M PB, dehydrated through a
stract form (Lazarov and Chouchkov, 1993).
graded ethanol series, and f lat-embedded in Durcupan
ACM (Fluka). Ultrathin sections were cut on a
Reichert-Jung ultratome. Lightly counterstained with
Eight adult cats of either sex weighing 2-3 kg pro- Uranyl acetate and lead citrate, they were viewed with
vided data. Five of them were treated for SER immu- an OPTON EM logelectron microscoPe.
noreactivity only, and the other three were treated for
Retrograde Labeling
both immunoreactivity and retrograde tracing a t light
Wheat germ agglutinin conjugated to horseradish
and electron microscopic levels.
peroxidase (WGA-HRP) (lot no. 0390; Sigma. St. Louis,
MO) was used as a retrograde tracer to-determine the
lrnrnunocytochernical Studies
Four cats received 1,000 pl colchicine (Merck, Darm- origin of the serotoninergic axons in the MTN. Three
cats were anesthetized with intraperitoneal sostadt, FRG) in 200 p1 saline injected stereotaxically adult
dium pentobarbital (40 mg/kg b.wt.1, placed in a stereotaxic apparatus (Kopf Instruments Co., Tujunga,
CA, USA), and given a single microinjection of the
tracer (2 pl of 2.5% WGA-HRP, dissolved in 0.9% NaC1)
into the MTN. The injection was made by iontophoresis
A bbreuiations
over a period of 30 min through a glass micropipette
cerebral aqueduct
(tip diameter 10-20 pm) which was attached to a 2 pl
central gray
dorsal parabrachial nucleus
Hamilton microsyringe. Two days later, all the aniDR
dorsal raphe nucleus
mals were deeply re-anesthetized and perfused tranLC
locus coeruleus
scardially with 3 1 of a fixative composed of 2.5% gluMnR
median raphe nucleus
taraldehyde and 0.5% paraformaldehyde, containing
mesencephalic trigeminal nucleus
periaqueductal gray
4% sucrose in 0.05 M PB, pH 7.4. After the perfusion,
raphe pontis nucleus
the brains were immediately removed, saturated with
superior cerebellar peduncle
30% sucrose in the same buffer a t 4"C, and then cut
ventral parabrachial nucleus
serially into frontal sections of 40 pm thickness on a
4 v
fourth ventricle
freezing microtome. The sections were stained for the
histochemical demonstration of WGA-HRP according
to the tetramethylbenzidine (TMB) method of Mesulam
(1978). To demonstrate the serotoninergic nature of
WGA-HRP-labeled neurons in the brainstem raphe
nuclei and the percentage frequency of immunoreactive cells giving rise to serotoninergic input to the cat
MTN, the sections were treated for immunocytochemistry as described above, and those projecting to the
MTN were identified by a retrograde tracer transport.
Double-labeled neurons which contained SER immunoreactivity and WGA-HRP reactive granules were
identified by the presence of both black and brown reaction product within their cytoplasm (cf. Fig. 8A-C).
WGA-HRP was demonstrated, resulting in a black
granular intracellular reaction product. On the other
hand, SER immunoreactivity was visualized by a light
brown cytoplasm staining.
Control sections were processed in the same way, but
the specific antibody was omitted from the incubation
medium. As other controls, primary antiserum was replaced with normal (nonimmune) rabbit serum. In addition, the specificity of the immunostaining was
checked by preabsorbing serotonin antiserum a t working dilution with a n excess (200 km/ml) of synthetic
SER overnight at 4°C.
sented a small number, approximately 5 t 1%,of the
total retrogradely labeled cell population. Incubation of
control sections without primary or secondary antisera
resulted in elimination of the immunocytochemical
staining, a s in sections incubated with normal rabbit
serum or antiserum preabsorbed with synthetic antiserum.
This paper has described for the first time in detail
the serotoninergic innervation of primary sensory neurons in the cat MTN. In addition, we have demonstrated that serotoninergic terminals form synaptic
contacts with cell bodies of MTN neurons. This observation is in agreement with the studies carried out on
the distribution of SER-immunoreactive terminals
within the rat mesencephalic trigeminal nucleus (Liem
e t al., 1993). The serotoninergic input to the MTN appears to be part of a SER-positive fiber plexus covering
the neighboring parabrachial nucleus and locus coeruleus. The present data have shown that serotoninergic
fibers form a pericellular basket-like network around
MTN neurons. In accordance with the previous reports
on other species (Copray e t al., 1990b, 1991; Kolta et
al., 1993), no perikaryal immunostaining has been
seen in the MTN of the cat. Similarly, such encircled
nonreactive neuronal somata have been identified in
the cat trigeminal ganglion, as were described elsewhere (Chouchkov et al., 1988). Furthermore, our results have confirmed the observations in a n earlier re-
Peroxidase immunoreactivity for SER was localized
in fine and sometimes beaded nerve fibers of the MTN
of the cat. None of the neurons within the MTN showed
any specific immunoreactivity. The serotoninergic
plexus extended over the adjacent locus coeruleus and
nucleus parabrachialis (Fig. 1).The cell bodies of large
1. SER-immunostained frontal section through the caudal level
immunonegative MTN neurons were closely sur- of Fig.
the MTN. The MTN is located in between the LC and VPB. Note the
rounded by SER-positive thin fibers and terminals high density of thin, varicose SER-positive fibers extending over the
(Figs. 2, 3). On rare occasions, the axonal varicosities adjacent LC and VPB. x 100.
covered the neuronal surface of small unstained MTN
Fig. 2. Photomicrograph illustrating the distribution of SER-immucells. At higher magnification, some of these immuno- noreactive
cell bodies and fibers in the brainstem of the cat at the
reactive varicosities appeared to be in close proximity level of the rostra1 pons. Immunoreactive perikarya can be seen in the
LC and VPB. A cluster of large unstained neurons in the MTN is
to profiles of MTN neurons of all sizes (Fig. 3).
At the ultrastructural level, fine labeled axonal pro- surrounded by thin serotoninergic fibers with intensively stained varfiles were in close apposition to the mesencephalic cell icosities and terminal boutons. x 160.
bodies (Fig. 4),and direct axosomatic contacts could be
Fig. 3. Higher magnification of the area inside the rectangle in Fig.
seen (Fig. 5). Furthermore, some axodendritic (Fig. 6) 2 showing a plexus of varicose fibers (arrows) forming basket-like
and synapses en passant (Fig. 7) were documented. The structures around five large immunonegative MTN neuron cell bodlabeled profiles were filled with small vesicles. In the ies. The SER-immunoreactive fibers pass to the LC and DPB. x 400.
nerve terminals, electron-dense DAB reaction product
Fig. 4. A perisomatic serotoninergic profile in the MTN. N o synaptic
was located within numerous small clear round vesi- contact between the perikaryon and the labeled fiber is visible. The
cles (diameter 50-80 nm) and a few small granular membranes are closely apposed and show some densification in some
points (arrows). The reaction product is distributed in the axoplasm
vesicles and was associated with the outer boundaries between
the vesicles and inside some of the small vesicles. Mitochonof the mitochondria. A few immunolabeled large dense- drial profiles are also labeled. x 12,000.
cored vesicles (up to 150 nm diameter) were also found
Fig. 5. Electron micrograph of a synaptic contact between a SERin serotoninergic terminals.
immunoreactive terminal and a MTN cell body (M).Note the presence
The sites of WGA-HRP injection were restricted to of
vesicles that are surrounded and only occasionally filled with DAB
the MTN in the cats. Retrograde tracing with WGA- reaction product. X 50,000.
HRP demonstrated that afferents of the MTN origiFig. 6. Demonstration of an axodendritic synapse between a SERnated from cells in serotoninergic areas (i.e., in the
terminal and a small dendrite (D). The site of the contact
brainstem raphe nuclei, mainly from the dorsal raphe containing
is marked by an arrow. The axon terminal contains small clear and
nucleus) (Fig. 8A-E). A few WGA-HRP-labeled cells granular (dense-cored) vesicles. Note the close membrane apposition
were also found in the median and pontine raphe nu- (indicated by an open arrow) between the labeled terminal and a MTN
cleus. After processing the sections for immunocyto- cell body (MI. x 50,000.
chemistry, some of the SER-immunostained neurons in
Fig. 7. Serotoninergic axon (Ax) making a synaptic contact with the
the nucleus raphe dorsalis of the cat were also WGA- dendritic shaft en passant. Note the different synaptic vesicle conHRP-labeled. These double-labeled neurons repre- tents with small round and large dense-cored vesicles. x 50,000.
Figs. 1-7
Fig. 8. A Coronal section of the brainstem a t the level of the rostra1
pons showing DR and RPn. Note a large number of SER-containing
raphe nerve cells. Some of these raphe neurons are retrogradely labeled with a WGA-HRP applied to the MTN. Arrows point to the
double-labeled cells and the arrowheads to SER-positive cells. x 100.
B High magnification LM micrograph of the double-labeled (arrows)
and single-labeled (arrowheads) neurons in the dorsal raphe nucleus
as shown in A. Single-labeled neurons were easily identified by the
presence of either a black granular reaction product (WGA-HRP-
labeled neuron) or a brown reaction (SER-immunoreactive neuron)
throughout the cytoplasm. Double-labeled neurons were demonstrated by the presence of both black and brown reaction product
within their cytoplasm. x 630. C:Section of the DR at the level of the
mesencephalon. Both magnifications x 100. D,E: Schematic drawing
of the same sections as in A,C according to the stereotaxic atlas of
Berman (1968).Injection sites of WGA-HRP and retrogradely labeled
cells in the pons and mesencephalon as indicated in A and C, respectively. Each star represents one labeled neuronal cell body.
port (Tashiro e t al., 1989) that SER-immunoreactive
axonal varicosities are often seen in direct contact with
profiles of MTN neurons. While the light microscopic
analysis cannot demonstrate synaptic contacts, it is
likely that the observed contacts represent sites of synaptic contacts.
In the sensory ganglia, no synaptic contacts between
a n axon terminal and a ganglion cell body or process
have as yet been demonstrated (Lieberman, 1976).
Only Yamamoto and Kondo (1989)have reported finding rare synaptic contacts on somata of primary afferent neurons in the rat trigeminal ganglion. Moreover,
the axonal varicosities were immunoreactive to calcitonin gene-related peptide.
Our electron microscopical analysis has revealed
that MTN neurons have synaptic contacts with SERcontaining terminals. However, the serotoninergic fibers engage only rarely in synaptic contacts. Serotonin-containing terminals form both axodendritic and
axosomatic synapses. According to the classical observations of Hinrichsen and Larramendi (1968, 1970)
and our own investigation of SER-labeled terminals,
most of the synaptic profiles in the cat MTN contain
numerous small round vesicles and several granular
vesicles. In agreement to the data given by Maley et al.
(1990), we could also find large granular vesicles in the
SER-containing terminals of the cat MTN. The axosomatic contacts are rare and are formed by fine axons. It
is likely that these correspond to the perisomatic serotoninergic fibers observed in this study.
In addition, retrograde tracer studies combined with
immunocytochemistry have demonstrated that MTN
received serotoninergic afferents exclusively from the
nuclei raphe dorsalis, pontis, and medianus. The first
reported distribution of monoamine-containing neurons in the raphe system of the rat given by Dahlstrom
and Fuxe (1964) has lately been confirmed in the cat
(Poitras and Parent, 1975, 1978). More recently, SER
has been localized a t the ultrastructural level in the
nucleus raphe dorsalis of the cat (Chazal and Ralston,
1987), and direct projections from the brainstem raphe
nuclei to the trigeminal sensory complex have been
documented (Li et al., 1993b,c,d).The nuclei of origin of
serotoninergic afferent fibers in the rat trigeminal motor, facial, and hypoglossal nuclei have earlier been
described by Li et al. (1993a). This study has revealed
that the SER-containing neurons project directly, except for the dorsal lateral geniculate nucleus (De Lima
and Singer, 1987), to the MTN of the cat. Thus, the
serotoninergic fibers revealed by immunocytochemistry in the MTN are most likely arising from the serotoninergic cells in the dorsal raphe nucleus. On the
other hand, the double-labeled method has shown that
in the cat, SER-containing raphe neurons contact with
axonal varicosities exhibiting noradrenalin-, substance
P-, and enkephalin-like immunoreactivity (Pretel and
Ruda, 1988).
The physiological significance of these findings for
the functioning of the MTN neurons, however, is obscure and still remains to be determined. The activity
of MTN neurons is modulated in different way (for review, see Cody et al., 1972, 1975; Inoue et al., 1981).
Similar studies carried out on MTN in the r a t (Copray
et al., 1991) and rabbit (Kolta et al., 1993) have suggested that SER can modulate the transmission of action potentials from muscle spindle receptors during
mastication. Although until now the functional role of
serotoninergic system has remained unknown, the results of a previous investigation (De Montigny and
Lund, 1980) have shown that SER has a depressant
effect on MTN spindle afferents in the cat.
As direct projections from the brainstem raphe nuclei to the MTN of the cat have been observed in the
present study and most of the double-labeled raphe
neurons have shown SER immunoreactivity, it may be
speculated that serotoninergic input modulates MTN
neuronal activity. As in the rat, SER-containing raphe
neurons may modulate the proprioceptive information
in the cat MTN by directly sending axon collaterals to
this region. This is supported by our findings in earlier
works on the neurochemical organization and the connections of the cat trigeminal sensory nuclear complex
(Lazarov, 1991, 1994, Chouchkov and Lazarov, 1993,
1994). Besides the fact that the cell bodies of primary
afferent neurons are SER-immunonegative, it is reasonable to assume that SER is not a transmitter candidate for MTN neurons of the cat.
In conclusion, it seems t h a t in the MTN of the cat
SER is likely to be involved not a s a classical neurotransmitter but as a pure neuromodulator. If i t is so,
then other substances may act as transmitters, and
only further investigations could clarify the neurotransmitter content of the cat MTN.
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containing, mesencephalic, cat, projections, serotonin, trigeminal, nucleus
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