Neuropeptides in the cat diencephalon: I. Thalamus - Eur J Anat

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R E V I E W
Eur J Anat, 5 (3): 159-169 (2001)
Neuropeptides in the cat diencephalon:
I. Thalamus
R. Coveñas1, M. de León1, M. Belda1, P. Marcos2, J.A. Narváez3, J.A. Aguirre3,
G. Tramu4 and S. González-Barón3
1- Instituto de Neurociencias de Castilla y León (INCYL), Laboratorio de Neuroanatomía de los Sistemas Pep-
tidérgicos,Salamanca,Spain
2- Un i v e r sidad de Castilla-La Mancha,Facultad de Medicina,De p a r tamento de Ciencias de la Salud,Al b a c e t e ,
Sp a i n
3- Universidad de Málaga,Facultad de Medicina,Departamento de Fisiología,Málaga,Spain
4- Un i v e r sité de Bordeaux I,Laboratoire de Neurocytochimie Fon c t i o n e l l e , C. N . R . S . , U.R.A. 339,Tal a n c e , Fra n c e
SUMMARY Abbreviations used: AD, N. anterior dorsalis;
AM, N. anterior medialis; AV, N. anterior ven-
In this paper we review the distribution and tralis; CL, N. centralis lateralis; CM, N. centrum
functions of neuropeptides in the cat thalamus. medianum; GL, Corpus geniculatum laterale;
We focus our review on the following topics: 1) GLv, Corpus geniculatum laterale (pars ven-
the distribution of neuropeptides in the cat thal- tralis); GM, Corpus geniculatum mediale; Hbl, N.
amus; 2) the coexistence of neuropeptides in the habenularis lateralis; Hbm, N. habenularis medi-
cat thalamus; 3) the anatomical relationships alis; IAM, N. interanteromedialis; IV, N. interven-
between neuropeptides in the cat thalamus; 4) tricularis; LD, N. lateralis dorsalis; Lim, N. limi-
the peptidergic pathways in the cat thalamus; 5) tans; LP, N. lateralis posterior; mc, pars
a comparison of the distribution of neuropep- magnocellularis; MD, N. medialis dorsalis; NCM,:
tides in the mammalian thalamus; and 6) the N. centralis medialis; P, N. posterior; Pc, N. para-
physiological functions of neuropeptides in the centralis; Pf, N. parafascicularis; Prt, Praetectum;
cat thalamus. Although in recent years our Pt, N. parataenialis; Pul, Pulvinar; PVA, N.
knowledge of the distribution of neuropeptides periventricularis anterior; R, N. reticularis; RE, N.
in the cat thalamus has increased considerably, reuniens; Rh, N. rhomboidens; S, Stria
there still remains much to do in this feline brain medullaris; SG, N. suprageniculatus; Sm, N. sub-
region in order to know the distribution of other medius; Spf, N. subparafascicularis; THP, Tractus
ne u r opeptides, the physiological interactions habenulo-peduncularis; VA, N. ventralis anterior;
among them, the afferent and efferent peptider- VL, N. ventralis lateralis; VM, N. ventralis medi-
gic pathways, and the physiological roles of such alis; VPL, N. ventralis postero-lateralis; VPM, N.
neuropeptides. In the future, other methods ventralis postero-medialis; ZI, Zona incerta.
(e.g., in situ hybridization, tract-tracing…) in
addition to immunocytochemical methods
should be used in the cat thalamus to increase INTRODUCTION
our knowledge of the neuropeptides in this
diencephalic region. The thalamus is located in the central part of the
encephalon, belongs to the diencephalon, and is
Key Words: Neuropeptides – Thalamus – Dien- an important relay area between the spinal
cephalon – Cat cord/brainstem and the basal ganglia/cerebral
Correspondence to:
Dr. R. Coveñas. Instituto de Neurociencias de Castilla y León (INCYL),Laboratorio de Neu-
roanatomía de los Sistemas Peptidérgicos, Facultad de Medicina,C/ Alfonso X El Sabio
Submitted: July 17, 2001 s/n,37007,Salamanca,Spain.
Accepted: October 26,2001 Phone: [phone] est. 1856; Fax: [phone]. E-Mail: [email protected]
159
R. Coveñas,M. de León,M. Belda,P. Marcos,J.A. Narváez,J.A. Aguirre,G. Tramu and S. González-Barón
cortex. The thalamic nuclei receive somatosen- ly, into the concentration of neuropeptides and
sorial, nociceptive, visual, auditive, vestibular, the presence of neuropeptides receptors in the
taste and olfactory inputs (see van Dongen and cat thalamus (O’Donohue et al., 1979; Dietl et
Nieuwenhuys, 1998). In addition, this brain al., 1990). As can be observed, only ten neu-
region is involved in motor and speech mecha- ropeptides have been studied in detail in the cat
nisms and is a region in which functional asym- thalamus (Sugimoto et al., 1984; Conrath et al.,
metry has been described, since one side pre- 1986; Coveñas et al., 1986, 1990, 1996a,b,c; Rao
dominates over the other. Thus, the left side of et al., 1986, 1987; Burgos et al., 1988; de León et
the thalamus predominates over the right side in al., 1991a, b; Battaglia et al, 1992; Velasco et al.,
mechanisms involved in speech and in mechan- 1993; Belda et al., 2000), although there are par-
ical processes (e.g., respiration…), whereas the tial data for another two neuropeptides (Obata-
thalamic right side predominates over the left Tsuto et al., 1983; Sugimoto et al, 1985; Wahle
side in visual and spatial processes. Moreover, and Albus, 1985). Moreover, scarce or very
the thalamus has been implicated in several dis- scarce data are available concerning the distrib-
eases. For example, a loss of 50% of the small ution of another four neuropeptides (not shown
neurons located in the pulvinar nucleus has in Table 1): somatostatin-14, somatostatin-28,
been observed in schizophrenia, and a decrease avian pancreatic polypeptide and delta sleep-
in the number of neurons located in the nucleus inducing peptide. In the cat, immunoreactive
ventralis lateralis has been described in Hunting- fibers containing somatostatin-14 have been
ton’s disease (see Ohye, 1990). found in the nuclei habenularis lateralis, centralis
Based on topographic criteria, the thalamic medialis, reuniens, medialis dorsalis, subparafas-
nuclei have been grouped into several nuclear cicularis and zona incerta, and somatostatin-14-
gr oups (posterior, ventral, medial, midline, containing cell bodies have been observed in the
intralaminar) and complexes (lateralis posterior- cat nucleus reticularis (Graybiel and Elde, 1983).
pu l v i n a r , geniculate), as well as into the In this species, the same authors described
ephithalamus and dorsal and ventral thalamus immunoreactive cell bodies, but no fibers con-
(see Macchi, 1983; Jones and Hendry, 1989). In taining somatostatin-28 in the nucleus reticularis
this review, we will follow that classification (see and no immunoreactive structures containing
Table 1). avian pancreatic polypeptide in the same thala-
Knowledge of the distribution and functions mic nucleus (Graybiel and Elde, 1983). In addi-
of the neuropeptides present in the mammalian tion, fibers containing delta sleep-inducing pep-
thalamus has increased considerably over the tide have been described in the cat nuclei
last twenty years. The distribution of many neu- habenularis medialis, periventricularis anterior,
ropeptides belonging to several peptidergic fam- reuniens and lateralis dorsalis (Charnay et al.,
ilies has been studied in the rat, dog, monkey 1990). Finally, the localization of calcitonin-bind-
and human thalamus (see, for example, Smith et ing sites has been demonstrated in the medial
al., 1985; Palkovits, 1988; Pioro et al., 1990; and intralaminar thalamus of the cat (Guidobono
Pego-Reigosa et al., 2000). The cat has been et al., 1987) and, with radioimmunoassay meth-
used in the laboratory as an experimental animal ods, a moderate level of kassinin has been
model in order to investigate several scientific described in the cat thalamus (Hunter et al.,
issues related to neuroanatomy, neurophysiolo- 1985).
gy, neuropharmacology and behaviour. Howev-
In general, the immunoreactive fibers con-
er, until 1983 the distribution of neuropeptides in
taining neuropeptides in the cat thalamus are
the cat central nervous system had received little
located in the nuclei of the midline and in thala-
attention. Over the past eighteen years, howev-
mic nuclei close to the midline (see Table 1),
er, knowledge of their distribution has increased
although the presence of immunoreactive fibers
notably. The aim of this paper is to review, in containing, for example, neuropeptide Y, b -
the cat, the currently available morphological endorphin or a -melanocyte-stimulating hormone
and physiological data concerning neuropep-
has been described in thalamic nuclei located
tides in one of the most complex areas of the
laterally, such as the corpus geniculatum medi-
central nervous system: the thalamus.
ale, corpus geniculatum laterale, pars ventralis of
the corpus geniculatum laterale or lateralis pos-
terior (Coveñas et al., 1990; 1996a,b). The distri-
NEUROPEPTIDES IN THE CAT THALAMUS bution of cell bodies containing neuropeptides
in the cat thalamus is shown in Figure 1.
Table 1 shows the presence of fibers and cell The neuropeptide methionine-enkephalin
bodies containing neuropeptides in the thalamus (MET-E) shows the most widespread distribu-
of the cat detected using immunocytochemical tion, since of the 36 nuclei of the cat thalamus
methods. The table also shows a few studies in fibers and/or cell bodies containing MET-E have
which radioimmunoassay or autoradiographic been observed in 31 of them (see Table 2). How-
techniques were used to gain insight, respective- ever, neurokinin A (NKA) has the lowest distrib-
160
Neuropeptides in the cat diencephalon: I. Thalamus
161
R. Coveñas,M. de León,M. Belda,P. Marcos,J.A. Narváez,J.A. Aguirre,G. Tramu and S. González-Barón
Fig. 1.- Distribution of cell bodies containing neuropeptides in frontal planes of the cat thalamus corresponding to the anteroposterior stereo -
taxic plane levels from anteriority 5.0 to anteriority 11.5 of the Jasper and Ajmone-Marsan (1966) stereotaxic atlas. The anteriority (A),
in mm with respect to the zero stereotaxic point of each section, is indicated at the lower right. For a nomenclature of the thalam-
ic nuclei, see list of abbreviations. Cell bodies are represented by: : cholecystokinin-8; : methionine-enkephalin; : neurokinin
A; : neuropeptide Y; : neurotensin; : somatostatin-28 (1-12); : somatostatin-28; : somatostatin-14; : substance P; :
vasoactive intestinal peptide. Scale bar: 1.54 mm.
162
Neuropeptides in the cat diencephalon: I. Thalamus
Table 1.-Distribution of neuropeptides in the nuclei of the cat thalamus.
MET-E SP NT SOM NPY b -END a -MSH ACTH LH-RH NKA CCK-8 VIP
F CB F CB F CB F CB F CB F CB F CB F CB F CB F CB F CB F CB
EPITHALAMUS
Hbl - + + + + - + - + - + - + - + - + - + + -
Hbm + - - + + - - - - - + - + - + - + - + - -
PVA + - + + + + + - + - + - RIA - + - + - + - + -
+
MIDLINE GROUP
IAM - - + - + - + - + - + - + - + - - - - - +
IV + + - - + - - - - - + - + - + - + - + -
NCM + + + - + + + - + - + - + - + - + - + - + - +
RE + + + - + + + - + - + - + - + - + - + + -
Rh + - + - + - + - + - + - + - + - - - + - + -
MEDIAL GROUP
MD + + + - + + + - + + + - + - + - + - + + -
Pt + - - - + - + - + - + - + - + - + - + - + -
INTRALAMINAR GROUP
CL - - + - - - - - + - + - - - - - - - - - +
CM + + - + + - - - + - + - + - - - - - - -
Pc - + - - - - + - + - - - - - - - - - - + +
Pf + + + + + - - - + + + - + - + - - - + +
Spf + + - + - - - + - - - - + - - - + - - -
VENTRAL GROUP
Sm + + - - - - - - - - - - - - - - - - - -
VA + - - - - - - - - - + - - - - - - - - - +
VL - + - - - - - - - - - - - - - - - - - - +
VM - + - - + - + - - - + - + - - - - - - - +
VPL + + - - - - - - - - - - - - - - - - - - -
VPM - + - - - - - - - - - - - - - - - - - - - R
POSTERIOR GROUP
Lim - + - - - - - - - - + - - - + - - - - -
P - + - - - - - - - - - - - - - - - - - -
Prt - + + - + - - - + - - - - - - - + - - -
SG - + + - - - - - - + - - + - - - - - - -
LATERAL POSTERIOR
PULVINAR COMPLEX
LP - + + - + - + - + + + - + - + - + - - - -
Pul - + - - - - - - + - - - + - - - - - - - - R
DORSAL THALAMUS
AD - - + - - + + - + - - - + - - - - - - - +
AM + - - - - - - - + - - - RIA - - - + - - -
-
AV - - - - - + - - + - - - RIA - - - - - - -
+
LD + + + - + + + + + - + - + - + - + - + - - +
GENICULATE COMPLEX
GL - + - - - - - - + - + - + - - - - - - - - R
GLv - - + - - - - - + + + - + - - - - - - -
GM - + - - - - - - - - + - + - + - - - + -
VENTRAL THALAMUS
R + - - - - - - - - - - - - - - - - - - -
ZI - - - - - - - - + - + - + - + - - - - -
TRACTUS
S + - + - + - + - - - + - - - + - + - + -
THP + - - - - - - - - - - - - - - - + - - -
ACTH: ad r en o c o r t i c o t r opin hormone (18-39) or (1-39);b -E N D : b -endorphin (1-27); CC K - 8 : cholecystokinin-8; LH-RH: luteinizing hormo n e -
releasing hormone; ME T -E : methionine-enkephalin; a -M S H : a -melanocyte-stimulating hormone; NK A : ne u r okinin A; NP Y :ne u r opeptide Y; NT :
ne u r otensin; R: receptors; RI A : radioimmunoassay; SO M : somatostatin-28 (1-12); SP : substance P; VI P : vasoactive intestinal peptide. For a
no m e n c l a t u r e of the thalamic nuclei, see list of abbreviations. CB : im m u n o r eactive cell bodies; F: im m u n o r ective fibers; +: pr esence; - :ab s e n c e ;
no sign:not studied.
ution, since immunoreactive structures (fibers nuclei, such as the lateralis dorsalis, periventric-
and/or cell bodies) are only observed in 12 ularis anterior and reuniens, twelve neuropep-
nuclei of the cat thalamus. Moreover, in almost tides are seen in each of them.
all the thalamic nuclei of the cat (except in the
nuclei posterior, submedius, ventralis postero-
lateralis and postero-medialis) the presence of COEXISTENCE OF NEUROPEPTIDES IN THE CAT
two or more neuropeptides can be detected (see THALAMUS
Table 3). The thalamic nucleus in which the
highest number of neuropeptides (thirteen) has The presence of several diffe r ent neurop e p -
been observed in fibers and/or in cell bodies is tides in the same thalamic nuclei suggests the
the nucleus centralis medialis, whereas in other possibility that two or more neuropeptides may
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R. Coveñas,M. de León,M. Belda,P. Marcos,J.A. Narváez,J.A. Aguirre, G. Tramu and S. González-Barón
Table 2.- Percentages of thalamic nuclei of the cat that contain a neuropeptide located in fibers and/or cell bodies (F and/or CB), in fibers
(F) or in cell bodies (CB).
90%
80%
70%
60%
50%
F and/or CB
F
40% CB
30%
20%
10%
0%
MET-E MSH NPY END SP NT ACTH SOM LH-RH NKA
For a nomenclature of the neuropeptides, see Table 1. CB:immunoreactive cell bodies; F:immunoreactive fibers. The total number of thal-
amic nuclei is 36.
coexist in the same neuron. In this sense, it has et al., 1986), since somatostatin-28 was detect-
been demonstrated in the cat that in the nucle- ed in the cell bodies and somatostatin-28 (1-
us centralis medialis 70-80% of the immunore- 12) in fibers, suggesting that somatostatin-28 is
active neurons containing vasoactive intestinal cleaved within the neuronal somata to form
peptide also contain cholecystokinin (Sugimo-
to et al., 1985). The same authors also rep o r t -
ed the coexistence of cholecystokinin and neu- Table 3.-Presence of neuropeptides in the cat thalamic nuclei.
rotensin in cell bodies located in the nucleus
anterior dorsalis, and the coexistence of NCM 13/13 100%
vasoactive intestinal peptide and neurot e n s i n LD, PVA, RE 12/13 92,30%
has been also described in the rostral part of Hbl, MD 11/12 91,66%
Pt, Rh 10/12 83,33%
the nucleus lateralis dorsalis (Sugimoto et al.,
LP 9/11 81,81%
19 8 5 ) .
Pf, S 8/10 80%
In some cases, it has been described that Hbm 9/12 75%
the distribution in the central nervous system IAM 8/11 72,72%
of neuropeptides arising from the same pre- IV 7/10 70%
CM 6/10 60%
cursor is diffe r ent. Thus, in the cat thalamus
AD, Spf, VM 6/11 54,54%
the distribution of the diffe r ent forms of
GM, Prt 5/10 50%
somatostatin (somatostatin-28, somatostatin-14 Pc 5/12 41,66%
and somatostatin-28 (1-12), which originate AM, GL, GLv, SG 4/10 40%
fr om the precursor prosomatostatin (Fitz- ZI 5/13 38,46%
CL 4/11 36,36%
patrick-McElligott et al., 1988), shows several
AV, Lim 3/10 30%
di f fe r ences (de León et al., 1991b). These dis-
Pul, VA 3/11 27,27%
cr epancies in the localization of the diffe r en t R 3/13 23,07%
fo r ms of somatostatin could be due to intra- THP 2/10 20%
ne u r onal transport of the neurop e p t i d e s VL 2/11 18,18%
P, Sm 1/10 10%
(Lechan et al., 1983; Morrison et al., 1984;
VPL, VPM 1/11 9,09%
Lewis et al., 1986). In keeping with this, a
complete intraneuronal segregation of somato- For a nomenclature of the thalamic nuclei, see list of abbrevia-
tions. For example, 12/13: indicates that of 13 neuropeptides stud-
statin-28 and somatostatin-28 (1-12) has been
ied, 12 were found in fibers and/or cell bodies in the nucleus LD.
described in the cortex of the monkey (Lewis Their percentages are also indicated.
164
Neuropeptides in the cat diencephalon: I. Thalamus
somatostatin-28 (1-12), which is then rapidly POSSIBLE PEPTIDERGIC AFFERENCES TO THE CAT
transported into neuronal processes. In addi- THALAMIC NUCLEI
tion, it is also possible that a diffe r ent kind of
pr ocessing of somatostatin precursor may Some of the results shown in Table 1 suggest
oc c u r , since it has been reported that the that several nuclei of the cat thalamus receive
intensity of staining for somatostatin-28 (1-12) peptidergic afferences. In this sense, a high or
and somatostatin-28 in the same region is moderate density of immunoreactive fibers and
quite diffe r ent (see de León et al., 1991b). no immunoreactive cell bodies have been
observed in such nuclei. Table 5 shows the thal-
amic nuclei of the cat in which peptidergic fibers
ANATOMICAL RELATIONSHIPS AMONG THE NEU- but no cell bodies have been observed. In all
ROPEPTIDES IN THE CAT THALAMUS cases, the observation indicates that such thala-
mic nuclei could receive peptidergic afferences
Table 4 shows the anatomical rel a t i o n s h i p s arising from neurons located inside and/or out-
among the neuropeptides in the cat thalamus. side the thalamus.
For example, in the case of substance P and b -
endorphin the Table indicates that in 89.47% of
the cat thalamic nuclei in which substance P- Table 5.- Possible peptidergic afferents to the cat thalamic nuclei
immunoreactive fibers and/or cell bodies are (F: +++/++; CB: -).
found, b -e n d o r p h i n - i m m u n o r eactive fibers
and/or cell bodies have also been observed. The ACTH NPY
percentage was calculated taking the total num-
IAM: (++) PVA (+++)
ber of the cat thalamic nuclei in which substance
IV: (++) NT
P-immunoreactive fibers and/or cell bodies were Lim: (++) Pf: (++)
MD: (++) SOM
visualized as 100%. The lowest perce n t a g e
NCM: (++) Hbl: (+++)
observed was 39.13% (neuropeptide Y/neu- Pf: (++) Pc: (++)
rokinin A). PVA: (+++) PVA: (+++)
Rh: (+++) SP
MET-E AD: (++)
HBM: (+++) IAM: (++)
Pt: (++) LD: (+++)
PVA: (+++) MD: (+++)
Rh: (++) NCM: (+++)
Table 4.- Anatomical relationships among the neuropeptides in a -MSH Prt: (+++)
the cat thalamus. PVA: (++) RE: (++)
NKA Rh: (++)
NCM: (+++)
% PVA: (+++)
SP/b -END 89.47 Rh: (+++)
NPY/a -MSH 86.95
SOM/b -END; SOM/a -MSH; SOM/ ACTH; SOM/NPY 85.71 For a nomenclature of the neuropeptides and the thalamic nuclei,
NT/a -MSH; SP/NPY; SP/a -MSH; NT/b -END 84.21 see respectively, Table 1 and list of abbreviations. CB:immunore-
SP/NT; NT/NPY; NT/ACTH 78.94 active cell bodies; (- : absence); F:immunoreactive fibers (+++:
b -END/a -MSH; b -END/ACTH 78.26 high density; ++: moderate density).
ACTH/NKA 72.22
SOM/LH-RH 71.42
NPY/b -END 69.56
NT/SOM 68.42 POSSIBLE PROJECTING PEPTIDERGIC THALAMIC
LH-RH/ NKA 66.66
NEURONS IN THE CAT
SOM/NKA 64.28
SP/SOM; SP/ACTH; NT/LH-RH; NT/NKA 63.15
a -MSH/ACTH 62.15 Unlike what has been reported above, there are
ACTH/LH-RH 61.11 thalamic nuclei in the cat in which a high or
MET-E/b -END; MET-E/a -MSH 59.37
moderate density of immunoreactive cell bodies
SP/LH-RH 57.89
b -END/NKA 56.52 has been observed, but no immunoreactive
MET-E/NPY 53.12 fibers. This finding indicates that such neurons
SP/NKA 52.63 could be projecting neurons, which send projec-
NPY/ACTH 52.17 tions to other thalamic nuclei and/or to other
MET-E/ACTH; a -MSH/LH-RH; a -MSH/NKA 50
parts of the central nervous system (see Table 6).
NPY/LH-RH; b -END/LH-RH 47.82
MET-E/NT; MET-E/LH-RH 46.87
MET-E/SP 43.75
MET-E/SOM; MET-E/ NKA 40.62 PEPTIDERGIC PATHWAYS IN THE CAT THALAMUS
NPY/NKA 39.13
Few peptidergic pathways have been demon-
For a nomenclature of the neuropeptides, see Table 1. strated in the cat thalamus, although the follow-
ing pathways have been described:
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R. Coveñas,M. de León,M. Belda,P. Marcos,J.A. Narváez,J.A. Aguirre,G. Tramu and S. González-Barón
Table 6.-Possible peptidergic projecting neurons in the cat thala- a high density of immunoreactive cell bodies
mic nuclei (F: -; CB: +++/++). containing neuropeptide Y has been found in
the thalamic nucleus, and neuropeptide Y-
MET-E NPY im m u n o r eactive fibers, but no immunorea c t i v e
cell bodies, have been observed in the hypo-
GL (+++) SG (++)
thalamic nucleus (Ueda et al., 1986). However,
GM (+++) SOM
Hbl (+++) Spf (+++) some of the neuropeptide Y-i m m u n o r ea c t i v e
LP (+++) SS-14 ne u r ons located in the pars ventralis of the cor-
P (+++) Ret (+++)
pus geniculatum laterale could be interne u r on s ,
Pc (+++) SS-28
Pul (+++) Ret (+++) since in that nucleus a moderate density of
VL (+++) fibers containing neuropeptide Y has also been
VM (+++)
observed. Alternatively, that nucleus could
VPM (+++)
receive affe r ences with neuropeptide Y from
SS-14: Somatostatin-14; SS-28:somatostatin-28. For a nomencla- ne u r ons located outside the pars ventralis of
ture of the other neuropeptides and the thalamic nuclei, see the corpus geniculatum laterale. Moreo v e r , the
respectively, Table 1 and list of abbreviations: CB:immunoreactive
ne u r ons containing neuropeptide Y in this
cell bodies; (+++: high density; ++: moderate density); F:
immunoreactive fibers (- : absence). nucleus could be projecting neurons that send
their axons to other thalamic nuclei such as the
lateralis posterior and pulvinar (Edwards et al.,
a) From the rostral region of the intralaminar
1974; Rodrigo-Angulo et al., 1988), since in the
nuclei to the striatum: containing cholecys-
cat horseradish peroxidase-labelled cell bodies
tokinin-8 or vasoactive intestinal peptide
have been visualized after injections of the
(Sugimoto et al., 1985; Adams and Fisher,
enzyme into the nuclei lateralis posterior and
1990).
pu l v i n a r , in the pars ventralis of the corpus
b)From the nuclei centralis lateralis, paracen-
geniculatum laterale; this is the same thalamic
tralis and centralis medialis to the proreus
nucleus in which neurop e p t i d e - i m m u n o r ea c -
gyrus: cholecystokinin (Sugimoto et al.,
tive cell bodies have been found (Coveñas et
1985).
al., 1990).
c) From the nucleus lateralis dorsalis to the
presubiculum: neurotensin or vasoactive
intestinal peptide (Sugimoto et al., 1985). COMPARATIVE STUDY ON THE DISTRIBUTION OF
d)From the nuclei anterior dorsalis and ante- THE NEUROPEPTIDES IN THE MAMMALIAN THAL-
rior ventralis to the presubiculum: chole-
AMUS
cystokinin or neurotensin (Sugimoto et al.,
1985).
Table 7 shows that the fibers and cell bodies that
e) From the nuclei centralis medialis, centralis
contain the neuropeptides that have been most
lateralis, paracentralis and rhomboidens to
extensively studied in the mammalian thalamus
cerebral areas 5, 6, 17, 18 and 19: chole-
show a greater or lesser degree of distribution in
cystokinin-8 (Whale and Albus, 1985).
the species studied (rat, cat, monkey, human).
f) From laminae I and V of the spinal cord to
Thus, in the cat thalamus, the distribution of
the thalamus: substance P (Battaglia and
im m u n o r eactive fibers is widespread for neu-
Rustioni, 1992).
ropeptide Y and luteinizing hormo n e - r el e a s i n g
g) From the superior colliculus to the nuclei
ho r mone in comparison with the distribution
lateralis posterior: substance P (Hutsler
observed for these neuropeptides in the rat/mon-
and Chalupa, 1991).
h) From the nuclei centrum medianum and
parafascicularis to the caudate: substance P
(Sugimoto et al., 1984). Table 7.- Comparative study of the distribution of fibers and cell
bodies containing neuropeptides in the thalamus of mammals.
i) From the nucleus arcuatus to the nucleus
periventricularis anterior: adren o c o r t i -
cotropin hormone (Kitahama et al., 1986). F CB
MET-E C = R > H C = R > M > H
Other works have also indicated the possi- SP C = R > H C = R > H
bility of peptidergic pathways. In order to NT C = R = H C > R > H
SOM C = R = H R > C > H
demonstrate these pathways, the use of both
NPY C > M > R C > M = H
immunocytochemical and tract-tracing tech- b -END C = R C = R
niques is req u i r ed. Thus, a possible pathway a -MSH C = R C = R
ACTH C = R = H C = R = H
containing neuropeptide Y from the pars ven-
LH-RH C > R C > R
tralis of the corpus geniculatum laterale to the
nucleus suprachiasmaticus could be prop o s e d ,
For a nomenclature of the neuropeptides, see Table 1. C:cat; CB:
since this anatomical pathway has been
distribution of immunoreactive cell bodies; F: distribution of
described in the cat (Swanson et al., 1974) and immunoreactive fibers; H: human; M: monkey; R:rat.
166
Neuropeptides in the cat diencephalon: I. Thalamus
key. Moreo v e r , immunoreactive cell bodies con- alis dorsalis indicates that this neuropeptide
taining neurotensin, neuropeptide Y or luteiniz- could be involved in vigilance and attentive
ing hormo n e - r eleasing hormone show a more behaviour (Bouyer et al., 1992). Moreover, the
wi d e s p r ead distribution in the cat thalamus than presence of immunoreactive fibers containing
that found for the same neuropeptides in the methionine-enkephalin in the nucleus sub-
thalamus of other mammals (Hökfelt et al., 1977; medius suggests the involvement of the opiate in
Ljungdahl et al., 1978; Sar et al., 1978; Finley et analgesic mechanisms (Conrath et al., 1986;
al., 1981; Haber and Elde, 1982; Jennes et al., Miletic and Coffield, 1988). Finally, other data
1982; Bouras et al., 1984, 1986, 1987; Johansson indicate that the thalamus is a potent source of
et al., 1984; Barry and Dubois, 1985; Chronwall et ne u r opeptides (e.g., neurotensin, vasoactive
al., 1985; Khachaturian et al., 1985; Nakagawa et intestinal peptide, cholecystokinin…) in the
al., 1985; Smith et al., 1985; Vincent et al., 1985; afferent systems to the cerebral cortex and stria-
Bennett-Clarke and Joseph, 1986; Mai et al., 1986, tum (Sugimoto et al, 1985), and that the intralam-
1987; Palkovits, 1988; Léger et al., 1990; Zaphi- inar thalamic nuclei mediate quite sophisticated
ropoulos et al., 1991). control mechanisms necessary to organize spe-
The discrepancies found as regards the dis- cific types of motor behaviour (Wahle and Albus,
tribution of fibers and/or cell bodies containing 1985).
ne u r opeptides in the mammalian thalamus
could be due to species variations and/or tech-
nical considerations (e.g., antisera used, injec- FUTURE RESEARCH ON NEUROPEPTIDES IN THE
tions of colchicine…). Accordingly, in order to
CAT THALAMUS
know the origin of such discrepancies, addi-
tional experiments (e.g., using the same
In the light of the above, it is clear that there is
methodology in all the species studied…)
much to be done if we are to elucidate the dis-
should be carried out.
tribution and functions of the neuropeptides in
the cat thalamus. The distribution of more neu-
ropeptides should be studied in depth using
PHYSIOLOGICAL FUNCTIONS OF NEUROPEPTIDES immunocytochemical methods. In addition,
IN THE CAT THALAMUS radioimmunoassay and in situ hybridization
techniques should be implemented in order to
The presence of numerous neuropeptides in the know the distribution and quantity of the neu-
same nuclei of the cat thalamus (see Table 3) ropeptides in the cat thalamus, as well as the
and the anatomical relationship between the distribution of the cell bodies containing
neuropeptides present in the cat thalamus (see mRNAs of the neuropeptides and/or their pre-
Table 4) suggest a possible interaction among cursors. Moreo v e r , there are no data rep o r t i n g
them and an elaborate modulation of functions the presence of neuropeptidases in the cat thal-
in which the thalamic nuclei are involved. Thus, amus and descriptions in the same region of
for example, an interaction between enkephalins receptors for neuropeptides are very scarce .
and substance P could be possible in the cat Both types of study must be carried out in the
thalamus, since it is known that enkephalins fu t u r e. Finally, other res e a r ch fields warranting
inhibit the release of substance P and cholecys- development in the future are: a) demonstra-
tokinin from hypothalamic slices (Micevych et tion of the peptidergic pathways, by combining
al., 1982). In addition, it has been demonstrated immunocytochemical and tract-tracing meth-
that methionine-enkaphalin is released by b - ods; b) knowledge of the synaptic connections
endorphin (Tseng, 1989) and that the neuropep- in the thalamic nuclei, using immunocytochem-
tide Y could act as a melanocyte-stimulating hor- ical and electron microscopic methods; c)
mo n e - r elease inhibiting factor (Ver b u r g- V an coexistence of neuropeptides in the cat thala-
Kemenade et al., 1987). Also, the release of mus, using immunofluorescence methods; and
luteinizing hormone-releasing hormone is mod- d) microinjections of the neuropeptides into
ulated by neuropeptide Y (McDonald, 1990). the cat thalamic nuclei in which the neurop e p -
As shown in Table 1, the presence of the neu- tides have been previously described in order
ropeptides studied in many different sites of the to know the physiological functions in which
cat thalamus implies that such neuropeptides such neuropeptides are involved. In sum,
serve different functions. Thus, the presence of although in the last eighteen years our knowl-
immunoreactive fibers containing methionine- edge about the distribution of the neurop e p -
enkephalin in the thalamic midline region indi- tides in the cat thalamus has increased thanks
cates that the neuropeptide could be involved in to the advent of immunocytochemical methods,
a motivational or affective aspect of sensory in the future other methodologies must be
transmission (Coveñas et al., 1986), and the pres- applied in order to gain further insight into the
ence of b -endorphin and luteinizing hormone- distribution and functions of neuropeptides in
releasing hormone in the thalamic nucleus medi- the cat thalamus.
167
R. Coveñas,M. de León,M. Belda,P. Marcos,J.A. Narváez,J.A. Aguirre,G. Tramu and S. González-Barón
ACKNOWLEDGEMENTS COVEÑAS R, DE LEÓN M, NARVÁEZ JA, TRAMU G, AGUIRRE JA
and GONZÁLEZ-BARÓN S (1996b). Mapping of alpha-
melanocyte-stimulating hormone-like immunoreactivity
This work has been supported by the
in the cat diencephalon. Peptides, 17: 845-852.
D. G . I . C . Y .T . (PB 96/1467; PM 99/0159; PM COVEÑAS R, DE LEÓN M, NARVÁEZ JA, TRAMU G, AGUIRRE JA
99/0160). The authors wish to thank N. Skinner and GONZÁLEZ-BARÓN S(1996c). An immunocytochemi-
for stylistic revision of the English text. cal mapping of ACTH/CLIP in the cat diencephalon. J
Chem Neuroanat, 11: 191-197.
CRONWALL BM, DIMAGGIODA, MASSARI VJ, PICKEL VM, RUG-
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