Brain Research Bulletin. Vol. 31, pp. 279-285,
1993
Printed in the USA. All rights reserved.
Copyright
0361-9230/93 $6.00 + .OO
0 1993 Pergamon Press Ltd.
Distribution of Neurokinin A in the Cat
Diencephalon: An Immunocytochemical Study
A. VELASCO,* M. DE LEeN,*, R. COVE&AS, *’ P. MARCO&* J. A. NARVxkEZ,t G. TRAMU,$
J. A. AGUIRREt AND S. GONZALEZ-BAReN?
*Universidad de Salamanca, Facultad de Medicina, Dpto. Biologia Celular y Patologia,Avda. Camp0 Charro s/n,
37007~Salamanca, SpainfUniversidad de MLtlaga,Facultad de Medicina, Dpto. Fisiologia, Ma’laga, Spain
$Laboratoire de Neurocytochimie Fonctionelle, CNRS, URA 339, Universitt de Bordeaux I, France
Received 3 1 July 1992; Accepted 6 October 1992
VELASCO, A, M. DE LE6N, R. COVERAS, P. MARCO& J. A. NARVAEZ, G. TRAMU, J. A. AGUIRRE AND. S. GONZALEZ-BARON. Distribution of neurokinin A in the cat diencephalon: An immunocytochemical study. BRAIN RES BULL
31(3/4) 279-285, 1993.-The distribution of neurokinin A-like immunoreactive cell bodies and fibers in the diencephalon of the
cat was studied using an indirect immunoperoxidase technique. A high or moderate density of immunoreactive neurons was
observed in the nuclei habenularis lateralis, medialis dorsahs, parafaxicularis, hypothalamus posterior, area hypothalamica dorsalis,
hypothalamus lateralis, periventricularis hypothalami, above the corpus mamillare, and in the perifornical area, whereas scarce
immunoreactive perikarya were visualized in the nuclei reuniens, hypothalami ventromedialis, hypothalamus dorsomediahs, and
mamillaris lateralis. The highest density of fibers containing neurokinin A was found in the nuclei periventricularis anterior,
rhomboidens, centralis medialis, periventricularis hypothalami, and supraopticus. In the regio praeoptica, area hypothalamica
dorsalis, hypothalamus posterior, and in the perifornical area a moderate density of immunoreactive fibers was observed, whereas
the nuclei habenularis lateralis, medialis dorsalis, mamillaris lateralis, parataenialis, reuniens, habenularis medialis, tiliformis,
hypothalamus dorsomedialis, hypothalami ventromedialis, arcuatus, and suprachiasmaticus showed a low density of neurokinin
A immunoreactive fibers.
Neurokinin A
Diencephalon
Immunocytochemistry
Cat
NEUROKININ A (NKA) is a member of the family of the
mammalian tachykinin peptides, as well as substance P (SP) and
neurokinin B (NKB) (22). These tachykinins have a common
C-terminal amino acid sequence and they have been reported
to be involved in several physiological roles such as the regulation
of smooth muscle contraction, salivation, depolarization of central neurons, central pressor action, hyperactivity, as well as interacts with dopaminergic A- 10 neurons mediating behavioral
activation (3,12,24,26). In addition, NKA and SP may be neurotransmitters of the baroreceptor reflex in the nucleus tractus
solitarii of the rat, and NKB may be a neuromodulator on cardiovascular responses in the same nucleus (25). Finally, NKA
and NKB may have a neurotransmitter/neuromodulator
role in
the cat substantia nigra (10). It is also known that SP and NKA
are derived from the preprotachykinin A gene, whereas NKB is
derived from the preprotachykinin B gene.
In general, the distribution of tachykinins in the mammalian
CNS has been characterized using immunocytochemistry
and
radioimmunoassay techniques (1,2,8,11,13,18,2 1,23,27,29-3 1).
However, these studies have been carried out on the distribution
of SP in the CNS of the rat, cat, monkey, and humans, whereas,
for example, the anatomical localization of NKA and NKB has
been carried out mainly in rats. In the cat, the data available on
the NKA show that the peptide enhances the depression of spinal
nociceptive neurons caused by cutaneously applied vibration
and that NKA is released in the spinal cord following injection
of a knee joint with kaolin and carrageenan ( 16).
In the cat diencephalon, we have studied the anatomical distribution of the neuropeptides methionine-enkephalin,
SP, neuropeptide Y, somatostatin-28 ( 1- 12) and neurotensin (2,47,19,20), but no data are available on the distribution of fibers
and cell bodies containing NKA in this region of the feline brain.
Thus, in the present work we attempted to study the distribution
of NKA in the cat diencephalon using an immunoperoxidase
technique and to compare our findings with the distribution of
the above-mentioned neuropeptides previously describe in the
feline diencephalon.
METHOD
Eight male adult cats (2-3 kg) were used. Three animals,
under deep ketamine anesthesia (40-50 mg/kg), received unilateral intraventricular injections of colchicine in the lateral
ventricle (300 pg in 5 ~1 of distilled water). The other five cats
’ To whom requests for reprints should be addressed.
279
VELASCO ET AL.
280
were not treated with the drug. Two days after the injection, the
treated animals as well as the untreated ones were anesthetized
with ketamine and perfused via the ascending aorta with 4 1 of
4% ~rafo~aldehyde
in 0.15 M phosphate buffer (PB) (pH 7.2).
The brains were removed, the diencephalon dissected out and
postfixed in the same solution for 12 h. With a Vibratome, 60
pm frontal sections were cut and processed for immunostaining.
The sections were incubated in PB containing 1%normal sheep
serum and 0.3% Triton X-100 for 30 min. The sections were
then placed overnight in the same PB solution containing NKA
antiserum diluted l/l~.
After a 30 min wash with PB, the
sections were incubated for 60 min with sheep antirabbit IgG
coupled to horseradish peroxidase as the second antibody, diluted
l/250 in PB. Finally, the sections were washed in PB and the
peroxidase was revealed by the 33’ diaminobenzidine method.
The antiserum used in the present work was purchased from
Bachem (Swi~erland). It was raised in rabbits against immunogens prepared by coupling the peptide to a carrier protein
(human serum albumin) with giutaraldehyde. The specificity of
the immunostaining was controlled by the preabsortion of the
primary antiserum with synthetic NKA antibody and by omitting
the NKA antibody in the first incubation bath. No residual immunoreactivity was found in either case. Moreover, possible interference by endogenous peroxidase was ruled out by staining
some sections beginning with the diaminobenzidine
step. No
reaction was visualized. Immunohistochemical crossreactivities
were performed by incubating NKA antiserum with an excess
of SP, NKB, eledoisin, or kassinin. In no case was any significant
reduction in immunoreactivity observed. Mapping was carried
out according to the stereotaxic atlas of Jasper and AjmoneMarsan ( 17). The same atlas was used for the terminology of
the diencephalic nuclei. Finally, the term neurokinin A-like immunoreactive (NKA-ir) was used to described the staining results
in our material.
RESULTS
Figure 1 shows the dist~bution of NKA-ir fibers and cell
bodies in the diencephalon of the cat. The hypothalamus showed
a higher density and a more widespread distribution of NKA-ir
structures than the thalamus. Thus, in the thalamus, NKA-ir
perikarya were found in the nucleus (n.) habenularis lateralis,
n. medialis dorsalis, n. parafascicularis and in the n. reuniens,
whereas in the hypothalamus, immunorea~ive
neurons were
visualized, e.g., in the n. mamillaris lateralis, n. hypothalami
ventromedialis, n. periventricularis hypothalami, area hypothalamica dorsalis, hypothalamus posterior, hypothalamus dorsomedialis, above the corpus mamillare, and in the perifomical
area. Moreover, NKA-ir fibers were mainly located in the thalamus in the midline nuclei or in nuclei located near the midline,
being absent in the lateral thalamic regions, whereas in the hypothalamus, immunoreactive fibers were found in almost all the
nuclei.
At anteriority (A) 5.0 and A 7.0 (not shown in Fig. I), respectively, was found a very low density of NKA-ir fibers in the
dorsal and lateral parts of the corpus geniculatum mediale and
a moderate densitv of both immunoreactive fibers and cell bodies
in the n. pamfa~~cula~s (Fig. 2A).
At A 7.5 (Fig. 1A), a high density of NKA-ir cell bodies was
observed in the n. habenularis lateralis (Fig. 2B) and a moderate
density in the n. medialis dorsalis (below the n. habenularis lateralis), below the n. subparafascicularis, and between this latter
nucleus and the ventricle. A scarce number of NKA-ir fibers
was observed in the stria medullaris, n. habenularis medialis, n.
ha~nuia~s lateralis, and n. medialis dorsalis, whereas a high
density of immunoreactive fibers was visualized in the n. periventricularis anterior. In addition, NKA-ir fibers were also located ventrally along the midline (moderate density) and extending towards the substantia nigra. In this, a large number of
NKA-ir processes was observed.
At A 8.5 (Fig. IB) NKA-ir cell bodies were observed above
the corpus mamillare (Figs. 2C, D) and in the n. mamillaris
lateralis. In these regions a high and a low density, respectively,
of NKA-ir cell bodies was visualized. Moreover, a large number
of immunoreactive cell bodies was visualized above the commissura supramamilla~s. Scarce immunoreactive fibers were
observed extending from the corpus mamillare towards the pedunculus cerebralis. Dorsally, a few immunoreactive fibers were
found in the region of the n. lateralis dorsalis nearest to the
midline, in the n. habenularis medialis, in the stria meduliaris,
in the n. habenularis lateralis, as well as in the midline and
dorsal regions of the n. medialis dorsalis, and in the same nucleus
in the region placed below the n. habenularis lateralis. Finally,
a high density of NKA-ir fibers was found in the n. centralis
medialis and above the corpus mamillare and a low density in
the n. interventricularis and in the n. mamillaris lateralis and
in the midline region extending from this latter nucleus to the
commissura supramamiiaris.
At A ii .O (Fig. I CT),a low density of NKA-ir cell bodies was
found in the thalamus in the n. reuniens. In the hypothalamus
(Fig. 3A), a high density of NKA-ir cell bodies was observed in
the hypothalamus posterior, the perifornical area (Fig. 2E), and
in the region extending ventrally from this area to the n. hypothalami ventromedialis. A moderate density of immunoreactive cell bodies was also found in the area hypothalamica dorsalis
(Fig. 2F) and in the hy~thalamus
lateralis (Fig. 3B), whereas
in the n. hypothalami ventromedialis, a few NKA-ir cell bodies
were visualized. In the thalamus, immunoreactive fibers were
found in the midline region. Thus, a low density of immunoreactive fibers was located in the stria medullaris, n. parataenialis,
and n. reuniens, whereas a high density was visualized in the n.
periventricuiaris anterior, n. rhomboidens, and in the n. centralis
medialis. In the hy~thalamus. scarce immunoreactive processes
were found in the n. filiformis and in the n. hypothalami ventromedialis. The perifornical area, the hypothalamus lateralis.
area hypothalamica dorsalis, and the hypothalamus posterior
showed a moderate density of NKA-ir fibers.
At A 12.5 (Fig. 1D), a low density of NKA-ir cell bodies was
found in the n. reuniens. A high density of immunoreactive
perikarya was visualized below the h~othalamus dorsomedialis
and close to the ventricle, a moderate density in the hypothalamus lateralis and in the n. periventricularis hypothalami, and
a low density in the hypothalamus dorsomedialis. At the same
level, scarce immunoreactive fibers were visualized in the stria
medullaris, n. parataenialis, n. reuniens, n. fiiiformis, hypothalamus dorsomedialis, and n. arcuatus, whereas a high density
of NKA-ir fibers was found in the n. ~~vent~cula~s
anterior
(Fig. 3C), n. periventt-icularis hypothalami, and n. supraopticus.
In addition, in the hypothalamus lateralis, in the region situated
near the ventricle and below the hypothalamus dorsomedialis,
as well as in the regions surrounding the n. filiformis and the
fornix and in the regions extending from the n. supraopticus to
the midline and from the same nucleus to the cap&a intema,
a moderate density of NKA-ir fibers was found.
At A 13.5 (Fig. 1E) a high density of NKA-ir neurons was
found near the ventricle between (Figs. 3D, E) the n. periventricularis hypothalami, and the n. suprachiasmaticus, and
a moderate density in the n. periventricularis
hypothalami.
In addition, at this level two clusters of immunoreactive
cell
bodies (moderate density) were found laterally. A high density
NKA IN THE CAT DIENCEPHALON
A
281
A7.5
FIG. 1. Distribution of NRA-ir fibers and cell bodies in frontal planes
of the diencephalon of the cat corresponding to the posteroanterior stereotaxic plane levels A 7.5 to A 13.5 of the Jasper and Ajmone-Marsan
(17)stereotaxic atlas. Immunoreactive fibers are represented by continuous lines, whereas cell bodies are indicated by closed circles, their shape
being related to the density of perikarya. (large filled circle, high density:
> IO cell bodies; medium filled circle, middle density: S-IO cell bodies;
small filled circle, low density: <5 cell bodies). The anterior&y (A), in
mm with respect to the zero stereotaxic point of each section is indicated
at the lower right. AHD, area hypothalamica dorsalis; AM, n. anterior
medialis; ARC, n. arcuatus; AV, n. anterior ventralis; CH, chiasma opticum; CI, capsula intema; CL, n. centralis lateralis; CM, n. centrum
medianum; FIL, n. filiformis; FX, fomix; GL, corpus geniculatum laterale; GM, corpus geniculatum mediale; HA, hypothalamus anterior;
HBL, N. habenularis lateralis; HBM, n. habenularis medialis; HDM,
hypothalamus dorsomedialis; HL, hypothalamus lateralis; HP, hypothalamus posterior; IV, n. interventricularis; LD, n. lateralis dorsalis; LP,
n. lateralis posterior, MD, n. medialis dorsalis; ML, n. mamillaris lateralis;
MM, corpus mamillare; NCM, n. centralis medialis; NHVM, n. hypothalami ventromedialis; PED, pedunculus cerebralis; PUL, n. pulvinar;
PVA, n. periventricularis anterior; PVH, n. periventricularis hypothalami;
R, n. reticularis; RE, n. reuniens; RH, n. rhomboidens; S, stria medullaris;
SCH, n. suprachiasmaticus; SMX, commissura supramamillaris; SN,
substantia nigra; SO, n. supraopticus; VA, n. ventralis anterior; VL, n.
ventralis lateralis; VM, n. ventralis medialis; VPL, n. ventralis posterolateralis; VPM, n. ventralis postero-medialis.
VELASCO
ET AL.
FIG. 2. NKA immunoreactivity in the diencephalon of the cat. (A) Anteriority 7.0. Immunoreactive fibers (small arrows) and cell bodies (large
arrows) in the n. parafascicularis. V: ventricle (X85). (B) Anteriority 7.5. NKA-ir cell bodies (large arrows) and fibers (small arrows) in the n.
habenularis lateralis (X85). (C) Anteriority 8.5. Clusters of immunoreactive neurons above the corpus mamillare. Note NKA-ir perikarya (arrows)
located medially. HP: h~thalamus
posterior: MM: corpus mamiliare; SMX: commissura supramamiila~s; V: ventricle (X 17). (D) Anteriority 8.5.
High power image of the delimited area in C (X85). (E) Anteriority 11.0. NKA-ir cell bodies and fibers (arrows) near the fomix (FX) (X85). (F)
Anteriority 10.0. Fibers and cell bodies (arrows) containing NKA located in the area hypothalamica dorsalis. TMT: tractus mamillo-thalamicus; V:
ventricle (X34).
NKA IN THE CAT DIENCEPHALON
283
FIG. 3. NKA-ir fibers and cell bodies in the cat thalamus and hypothalamus. (A) Anteriority 11.0. A low magnification of the hypothaiamus.
Immunoreactive cell bodies (arrows) showing a widespread distribution. AHD: area hypothalamica dorsalis; F’Xzfomix; HP: hypothalamus posterior;
NHVM: n. hy~thalami ventrom~ialis; V: ventricle (X34). (B) Anterior&y 11.0. Immunomacti~e fibers and cell bodies (arrows) located in the
hypothalamus lateralis. CI: cap&a intema; FX: fomix (X34). (C) Anteriority 12.5. NKA-ir fibers (arrows) in the n. periventricularis anterior (X85).
(D) Anteriority 13.5 . Clusters of NKA-ir cell bodies located near the ventricle (V) (X34). (E) Anteriority 13.5. High power image of the area
delimits in D (X85).
of NKA-ir fibers was found in the n. periventricularis
anterior, n. periventricularis hypothalami, and n. supraopticus,
whereas a low density of immunoreactive
fibers was observed in the n. suprachiasmaticus
and in the hypothalamus
anterior. Moreover, a moderate density of NKA-ir fibers was
visualized above the chiasma opticum, along all the midline
and surrounding the n. periventricularis
hypothalami and
the fornix. Finally, in the region praeoptica (not shown in
Fig. 1) a moderate density of immunoreactive
fibers was
found.
284
VELASCO
DISCUSSION
The present work is the first report that shows in detail the
distribution of NRA-ir structures in the mammalian diencephalon, using an indirect immunoperoxidase
technique.
In comparison with a study on the cellular localization of SP
and NRA-encoding
preprotachykinin
(PPT) mRNA in the female brain (13), our results are in agreement in some features.
Thus, Harlam et al. (13) observed, in the rat, PPT neurons in
the n. hypothalami ventromediahs, hypothalamus dorsomedialis,
the perifomical area, and above the corpus mamillare, in which
we found NRA-ir cell bodies in the feline. Moreover, these authors observed neurons containing PPT in the n. arcuatus but
no PPT cell body in the n. periventricularis
hypothalami. However, we have visualized in the cat immunoreactive
cell bodies
in the latter nucleus but none in the former. Moreover, Harlam
et al. (13) did not find labeled neurons containing PPT in the
rat thalamus; however, we found NRA-ir perikarya in the cat
in the n. habenularis lateralis, n. medialis dorsalis, and n. reuniens. These observations reveal that there are some differences
on the distribution of neurons expressing the PPT gene in the
rat diencephalon
in comparison with the distribution of NKAir cell bodies observed in the same region in the cat. These discrepancies could be due to technical considerations
and/or species differences.
In addition, our results are in agreement with other studies
in which radioimmunoassay
techniques has been used. In this
sense, using these techniques NRA has been described in the
thalamus and hypothalamus
of both rat and golden hamster
(9,29), as we found using immunocytochemical
techniques in
the cat diencephalon.
In addition, more NRA was found in the
rat hypothalamus than in the thalamus (28). In the cat, we have
also observed more immunoreactive
structures in the hypothalamus than in the thalamus.
The distribution of fibers and cell bodies containing methionine-enkephalin,
neurotensin,
somatostatin,
SP, and neuropeptide Y has been described in the cat diencephalon
(2,47,19,20). An anatomical relationship between NRA and SP can
be suggested for the diencephalon ofthe cat. Thus, both peptides
have been found, for example, in the following nuclei: habenularis lateralis, periventricularis
anterior, parataeniahs,
rhomboidens, centralis medialis, reuniens, area hypothalamica
dorsalis, hypothalamus
posterior,
perifomical
area, filiformis,
suprachiasmaticus,
and supraopticus. This finding is consistent
with the results observed by Helke et al. (14) on the distribution
of NRA and SP in the spinal cord, because in this region these
authors found the same distribution patterns of both peptides.
Our data also suggest a possible colocalization of NRA and SP
in the cat diencephalon,
as has been demonstrated
in sensory
neurons and in neurons of the medullary raphe nuclei ( 14,lS).
ET AL.
However, future studies are needed in order to corroborate this
hypothesis.
In addition, an anatomical relationship between NRA and
neurotensin,
somatostatin,
or methionine-enkephahn
can be
pointed out, because, for example, the four peptides have been
found in the n. habenularis lateralis, n. medialis dorsalis, n. periventricularis anterior, n. rhomboidens,
n. centralis medialis, n.
reuniens, area hypothalamica
dorsalis, and hypothalamus
posterior (4,6,19,20). Finally, the mentioned
neuropeptides
and
neuropeptide
Y were found in the n. rhomboidens,
n. centralis
medialis, n. reuniens, n. medialis dorsalis, and n. periventricularis
anterior (4,5,19,20). These data also suggest a possible colocalization of such neuroactive substances in the cat diencephalon,
as well as a possible interaction among some of the above-mentioned neuropeptides
and an elaborate modulation of functions
in which these diencephahc nuclei are involved. The distribution
of NRA-ir structures in the diencephalon
of the cat suggest that
the peptide could be involved in several physiological functions.
Thus, for example, the presence of NRA-ir fibers in both n.
periventricularis
hypothalami and n. supraopticus suggests that
NRA might regulate neuronal activity in both nuclei. Moreover,
the localization of NRA in the n. suprachiasmaticus
could indicate a possible role in the control of circadian rhythms and/
or in visual processes, whereas the presence of immunoreactive
fibers in the midline thalamic region could be related with motivational or affective aspects of the sensory transmission.
In
sum, the physiological significance of NRA in the cat diencephalon remains to be elucidated.
Until now, we have no data indicating whether the NRA-ir
perikarya observed in the hypothalamus
of the cat are local or
projecting neurons. However, according to the morphological
data obtained in the cat, it appears that the NRA-ir neurons
found, for example, in the n. habenularis lateralis send distant
NRA-ir projections, because a high density of NRA-ir perikarya
was found in this region as well as a low density of immunoreactive fibers, whereas the neurons containing NRA located in
the area hypothalamica
dorsalis, hypothalamus
lateralis, and in
the n. parafascicularis could be interneurons, because a moderate
density of both immunoreactive
cell bodies and fibers was observed in these regions. Alternatively, these neurons may send
distant NRA projections, whereas NRA-ir fibers may be NRA
afferents. Finally, it also appears that the n. periventricularis
anterior, n. rhomboidens,
n. centralis medialis, n. supraopticus,
and the regio praeoptica could recive NRA-ir afferents because
in all these nuclei a high or moderate density of NRA-ir fibers
was observed but no NRA-ir cell body. In sum, the origin of
the NRA-ir fibers and knowledge of whether the immunoreactive
neurons found in the cat diencephalon
are local or projecting
neurons should be investigated in future research.
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