ACTA NEUROBIOL. EXP. 1989, 49: 239-241
NUCLEUS LIMITANS THALAMI - COMPARATIVE ANATOMICAL
STUDY
\
Janusz MORYS,Jerzy DZIEWIqTKOWSKI, Maciej BOBINSKI and
Olgierd NARKIEWICZ
Department of Anatomy, Medical Academy
1 Debinki St., 80-211 Gdansk, Poland
Key words: nucleus limitans, thalamus, comparative anatomy
Cyto- and myeloarchitectonics as well as acetylcholinesterase activity
of the nucleus limitans thalami - a n important part of the nociceptive
system - were studied in insectivora (Sorex araneus, Erinaceus europaeus, Talpa europaeus), rat, rabbit, cat, monkey and man. Our results
suggest that nucleus limitans is phylogenetically a rather new structure.
In insectivora and in the rat we could not find any evident group of
neurons resembling nucleus limitans. I n the rabbit and cat nucleus limitans is composed of few layers of elongated cells. In macaca and man
it is a larger, more complicated structure possessing various types of
neurons, and arranged into many layers.
INTRODUCTION
Nucleus limitans is the most ventromedial part of the thalamus. It is
limited medially by the anterior pretectal nucleus.
Neuroanatomical studies have revealed connections of the nucleus
limitans with numerous somatosensory areas of the cortex in primates
(27, 34, 45) and cats (8, 38, 46). Our studies using the retrograde axonal
transport method have shown the presence of connections between the
nucleus limitans and the insuloclaustral area (26). In man and primates
the connections of the nucleus limitans with the pallidum have also been
found (18).
According to some clinical studies the nucleus limitans is a subcortical
somatosensory area related to pain. This hypothesis is supported by the
fact that low-frequency stimulation of the nucleus lirnitans during a stereotaxic operation in man causes discomfort or unbearable pain (18).
Phylogenesis of the nucleus limitans has never been studied, and
there is a disagreement on the structure, size and even existence of this
nucleus in various animals (7, 10, 16-18).
In the present study we compare architectonics of this area in various
species in order to find whether it is a phylogenetically new or old structure.
METHODS
Brains of insectivora: Sorex araneus (3 animals), Erinaceus europaeus
(2 animals), Talpa europaeus (2 animals), and of rat (5 animals), rabbit
(3 animals), cat (3 animals), monkey (Macaca mulatta - 3 animals) and
of 4 humans brains were used for cyto- and myeloarchitectonic studies.
Some animals (rat, rabbit, cat) were anesthetized with Thiopental injected intraperitoneally in the dose of 200 m g k g body weight and perfused
transcardially according to the Rosene and Mesulam method (41). The
brains of insectivora and monkey were removed without perfusion from
the skull immediately after the death of the animals, and fixed in 4O/o
formalin solution, The human brains were removed from the skull during postmortem examination, 24-36 h after patients' death, and also
fixed in 4O/0 formalin solution. After the fixation, the brains or their
parts were embedded in paraffin. Forty micrometer paraffin sections
were stained with cresyl violet or Weil standard technique.
Six animals (2 cats, 2 rats, 2 monkey) were anesthetized with Thiopental
and perfused transcardially with 0.9Vo NaCl solution followed by aO/o
formalin with CaC1, (1 g CaC1, per 100 ml solution). Two human brains
were removed from the skull during the autopsy, 24 h after the death,
cut into pieces and fixed in 2,000 ml of 8O/o formalin with 20 g CaC12. All
brains were stored overnight in a fixative. 60 pm thin frozen sections
were cut in the coronal plane and each of them was incubated according to the Gerebtzoff method (12). There were designated comparatively
three degrees of acetylcholinesterase activity: low, middle and high.
RESULTS
Nucleus limitans is characterized by some topographical and morphological features: (i) It lies between the medial part of the lateral
posterior nucleus of the thalamus (pulvinar) and the anterior pretectal
nucleus. (ii) It passes into the parafascicular and suprageniculate nuclei
(Fig. 1). (iii) In Nissl preparations neurons of the nucleus limitans are
Fig. 1. Diagram of transverse sections through the pretectothalamic border area in: A, rat; B, cat; C, monkey; D, man.
The schematic drawings were plotted typical transverse sections.
Fig. 2. Microphotographs of transverse sections showing neurons of the nucleus
limitans in cat ( A , B), monkey (C, D) and man (E, F). Cresyl violet. A, C and E,
lower; B, D and F, higher magnifications.
darkly stained, mainly elongated, of medium size with a clearly demarcated nucleus (Fig. 2C and D). (iv) In Weil standard technique the nucleus
limitans is poorly myelinated and well separated from the pretectum
by strongly myelinatd lamina medullaris pretectothalamica. (V) Nucleus
limitans is characterized by a rather low acetylcholinesterase activity.
Nucleus limitans in insectivora
In all the insectivora under study we could not find any structure
which could be regarded as the nucleus limitans. Organization of the
posterior thalamus is simple and comprises the lateral posterior and the
suprageniculate nuclei, both structures lying laterally to the lamina medullaris pretectothalarnica. Medially to this lamina the pretectal complex
is situated.
Nucleus limitans in the rat
As in the insectivora we could not find in the rat any evident structure similar to the nucleus limitans. Only in places, laterally to the lamina medullaris pretectothalamica, we abserved a few elongated darkly
stained neurons, which might form an anlage of the nucleus lirnitans.
The posterior part of the thalamus shows a simple organization (Fig. 1A).
We found here two parts of the lateral posterior nucleus: the medial
part - adjoining the lamina medullaris pretectothalamica, and the lateral one.
Nucleus limitans in the cat
Nucleus limitans in the cat is situated medially to the medial part of
the lateral posterior nucleus of the thalamus (Fig. 1B). Rostrally it passes into the parafascicular nucleus and ventrally into the suprageniculate
nucleus. Medially it adjoins the lamina medullaris pretectothalarnica,
which shows strong myelinization in Weil technique. The nucleus limitans encompasses many darkly stained and elongate neurons of medium
size (Fig. 2B). These neurons are localized in 3-4 parallel layers situated
close to the lamina medullaris pretectothalamica (Fig. 2A). They partly
resemble neurons of the medial part of the lateral posterior nucleus of
the thalamus and the parafascicular nucleus. The nucleus limitans contains a small number of unmyelinated and myelinated fibers which run
in ventrodorsal direction. The acetylcholinesterase activity of this area
is low.
Nucleus limitans in the rabbit
The nucleus limitans of the rabbit is clearly separated from neighbouring areas. Its structure and topography a r e similar to those found
in the cat. However there are only 2
area.
layers of neurons in this
-Nucleus limitans in the monkey
The nucleus limitans of the monkey forms a band of densely packed,
oval or elongated, dark neurons that are lying on the dorsolateral surface
of the anterior pretectal nucleus. Laterally nucleus limitans is bordered
by the pulvinar (Fig. 1C). Contrary to the previously described animals,
we observed a small number of microneurons (neurons, with perikarya
less than 10 pm in diameter). They are dispersed among larger cells.
Neurons of the nucleus limitans are arranged mostly in 7-10 layers,
parallel to the lamina medullaris pretectothalamica (Fig. 2C). A dense
network of fine fibers runs in this area parallelly to the lamina medullaris pretectothalamica. Neurons of the nucleus limitans resemble those
of the suprageniculate nucleus. The acetylcholinesterase activity is low
and similar to that in the medial part of the pulvinar.
Nucleus limitans in man
The rostra1 margin of the nucleus limitans surrounds the caudal portion of the medial nuclear complex. The central part of the nucleus limitans is delineated rostrally and dorsally by the nucleus parafascicularis
and centromedian nucleus. Laterally to the nucleus limitans there is the
medial part of the pulvinar and ventromedially - the suprageniculate
nucleus. The nucleus limitans contains numerous, darkly stained, densely
packed neurons (Fig. 2E and F), mainly oval and medium sized. They
form many parallel layers (more than 10). In the central part of the
nucleus we found microneurons which, as in the monkey, form about
1O0/o of all neurons in this region. In the caudal part of the nucleus limitans the percentage of microneurons increases to lgO/o. The nucleus
limitans contains a loose feltwork of single fibers, which becomes denser
laterally. fe he acetylcholinesterase activity of the nucleus limitans is low.
DISCUSSION
Our observathns suggest that the nucleus limitans is a phylogenetically young structure. In basal insectivora, showing a very simple organization of the posterior thalamus, we could not find any structure,
which could be regarded as nucleus limitans. In the rat we were not
able to discern nucleus limitans. In this area we found some elongated
neurons, which could be taken into account only as the anlage of the
nucleus limitans. In other animals, in parallel to the development of the
neocortex, the nucleus limitans increases in size forming layers of neurons.
I n the rabbit there are mainly 2 neuronal layers in this area, in the cat
3-4, in the monkey about 10, and in man much more.
The fact that in our morphological investigations we could not find
the nucleus limitans in the insectivora and in the rat, corresponds to the
observatiools of some authors (7, 14, 24, 32, 36, 39, 43). The nuclear complex however composed of the nucleus limitans and the suprageniculate
nucleus has been previously described in the rat (2). According to our
investigations this complex consists of the suprageniculate nucleus and
the most lateral part of the lateral posterior thalamic nucleus.
In the rabbit the nucleus limitans has not been described yet (23, 40).
In the cat various areas of the thalamus have been designated as nucleus
limitans. Some authors have suggested that it is situated laterally to the
parafascicular or centromedian nuclei and medially to the suprageniculate nucleus (13, 19, 20). In other descriptions the nucleus limitans has
been replaced with the suprageniculate nucleus (21, 8), or it has not been
found in this region (3, 35, 37, 40, 44). Updyke (46) describes the nucleus
lirnitans as a posterior part of the intralaminar nuclear complex of the
cat.
In the monkey the location of the nucleus limitans, described by us
is s~milarto that found by other authors (6, 7, 9, 11, 16, 22, 27, 30,
31, 42).
In man the nucleus limitans has been described by Percheron et al.
(33), Dewulf (10) and Hassler (17, 18). Hassler has distinguished its three
parts: nucleus limitans medialis, nucleus limitans opticus and nucleus
lirnitans portae. According to our results, Hassler's nucleus limitans portae corresponds to our suprageniculate nucleus. Microneurons of the
nilcleus limitans have been described only in man (10). It has been
suggested that small neuronal elements might correspond to inhibitory
interneurons, which have been observed also in other thalamic nuclei
(10). In our material microneurons were present only in primates (man
and macacca) but not in other species.
The connectivity pattern previously f o m d by us (26), suggests a sirn~iaritybetween the nucleus limitans and the paralamellar part of the
anterior pretectal nucleus. Both structures receive projections of long
somatosensory ascending tracts (5, 1) and both project to the somatosensory part of the claustrum (25, 26, 28, 29), which possesses connections
with various cortical areas. From our experiments (25, 26, 28, 29) it
seems that the nucleus limitans is an intermediate structure situated between the lateral posterior thalamus which projects to the insular cortex
(4, 14, 46) and the anterior pretectum.
The question from which part of the diencephalon or mesencephalon
the nucleus limitans derives is still open. According to Le Gros Clark (7)
244
!
the nucleus limitans originates from the large-celled nucleus of the
optic tract of the pretectal area. On the basis of morphological similarities Olszewski (31) has suggested that the nucleus limitans derives from
the suprageniculate nucleus. One may also suppose, that it either arises
from the lateral posterior thalamus a s a separate somatosensory structure, or originates from the posterior intralaminar nuclei.
We would like to thank Miss Sylwia Scislawska for preparation of the drawings.
This investigation was supported by Project CPBP 04.01 of the Polish Academy
of Sciences.
ABBREVIATIONS
C1
CM
DM
GI
GM
Hb
Lam
Lim
LPM
rnc
NPAC
NPA
Pf
Pul
Rh
sg
claustrum
centromedian nucleus
dorsomedial nucleus
granular insular cortex
medial geniculate nucleus
nuclei habenulae
lamina medullaris pretectothalamica
nucleus limitans
medial part of the lateral posterior nucleus
magnocellular part of the medial geniculate nucleus
anterior pretectal nucleus (pars compacta)
anterior pretectal nucleus
parafascicular nucleus
pulvinar
rhinal sulcus
suprageniculate nucleus
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Accepted 7 March 1989
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