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ACTA NEUROBIOL. EXP. 1977, 37: 247-252
THE ORGANIZATION OF AMYGDALOPETAL PROJECTIONS FROM
THE LATERAL HYPOTHALAMUS AND PREOPTIC AREA IN THE
RAT
Liliana NITECKA, Olgierd NARKIEWICZ and Czeslaw JAKIEL
Department of Anatomy, Institute of Medical Biology, School of Medicine
Gdahsk, Poland
In the light of physiological data it is certain that there is a close
functional correlation between the amygdaloid body and the hypothalamus and preoptic area. These areas are vital for emotional reactions
and affect drives and endocrinal functions. A damage of amygdaloid
nuclei causes changes in behavior very similar to those following partial
lesions of the hypothalamus and preoptic area (7, 8).
As various investigations have shown, there are numerous connections
running from the amygdaloid nuclei to the preoptic area and hypothalamus (3-5, 9, 11). They run both in stria terminalis and in the
ventral amygdalofugal (amygdalar) pathway. The stria terminalis is
a compact bundle of fibers, which divides near the anterior commissure
into several components running in various directions (4, 5, 10); we
distinguish, according to de Olmos (4), its dorsal, ventral and commissural
component. The ventral amygdalofugal pathway assumes a compact
bundle form only in the higher mammals, but is rather dissipated in the
rat (15).
In contrast to the fairly well-known amygdalofugal connections we
havz only some data on amygdalopetal axons emerging from the diencephalon (1-3, 12-14, 16), while their topographical and physiological
organization is almost unknown.
For our studies on amygdalopetal connections we used 110 Wistar
rats of both sexes, weighing 200-250 g. Various parts of the hypothala-
mus, preoptic and neighboring areas were coagulated by direct current
of 1 mA lasting 15-30 s. In several cases the stria terminalis was partly
or wholly damaged in its supracapsular part. Postoperative survival
time of animals was 3-5 days. Frozen sections of the brain were prepared according to the ' ~ a u t a - ~ y g a and
x Fink-Heimer methods. Location and extent of lesion were determined on specimens stained by the
Kliiver-Barrera method.
Various lesions in the anteromedial part of the hypothalamus, in its
posterior part, in the ventromedial and dorsomedial hypothalamic nuclei
and in the medial preoptic area have not produced any marked degenerative changes in the amygdala. Massive terminal and preterminal
degenerations in its nuclei were found in rats following lesions of the
most lateral parts of the lateral preoptic area and lateral hypothalamus
in its rostra1 segment, above the optic chiasma (Fig. 1 and 3). The whole
area was defined by us as the preopticohypothalamic lateral area.
Fig. 1. Localization of lesions causing degenerations in the amygdala. Extent of
lesions is marked in black. A : Lesion in the lateral preoptic area (LP) causing
severe degeneration of axons in the lateral amygdalopetal pathway of the stria
terminalis. B: Lesion situated more caudally, in the rostrolateral part of the lateral
hypothalamus (LH)resulting in degeneration of axons in the medial amygdalopetal
pathway of the stria terminalis and in the ventral amygdalar pathway.
After damage to the lateral preopticohypothalamic area, we found
three bundles of fibers passing from that area to the amygdala, seen
microscopically as bands of degenerating axons. Two bundles ran in the
ventral component of the stria terminalis, occupying in its supracapsular
part the lateral (lateral amygdalopetal pathway of the stria) and medial
area (medial amygdalopetal pathway of the stria) (Fig. 2). The third
pathway comprised fibers running directly to the amygdala (without
entering the stria terminalis) in the ventral amygdalar pathway. They
ran dispersed in a fan-like pattern. We named them as "ventral amygdalopetal pathway" (Fig. 2C).
Fig. 2. Localization of degenerations in the amygdala following lesions in the lateral
preopticohypothalamic area. In each row sections of the amygdaloid body from
rostra1 to caudal. The broken lines indicate degenerating fibers of passage, the dotspreterminal and terminal degenerations. A: Degeneration of the lateral amygdalopetal pathway of the stria terminalis. B: Degeneration of the medial amygdalopetal
pathway of the stria terminalis. C: Degeneration of the ventral amygdalopetal
pathway (both, orsal and ventral component). At the upper left corner localization
of the lateral and medial amygdalopetal pathways show11 on the cross-sectional
schema of the components of the stria terminalis, Abbreviations: A, anterior
amygdaloid area; BD, basal dorsal nucleus of amygdala; BV, basal ventral nucleus
of amygdala; BN, bed nucleus of stria terminalis; C, commissural component of
stria terminalis; Ce, central nucleus of amygdala; Co, cortical nucleus of amygdala;
D, dorsal component of stria terminalis; L, lateral nucleus of amygdala; LH, lateral
hypothalamus; LO, nucleus of lateral olfactory tract; LS, lateral amygdalopetal
pathway of stria terminalis; M, medial nucleus of amygdala; MS, medial amygdalopetal pathway of stria terminalis; ST, stria terminalis; V, ventral component of
stria terminalis.
Fig. 3. Terminal degenerations in the anterior amygdaloid area (A), and in the medial nucleus of amygdala (B) following
a lesion in the rostrolateral part of the lateral hypothalamus. C: Terminal degenerations in the basal dorsal nucleus of
amygdala following a lesion in the rostra1 part of the lateral preoptic area. Nauta, Gygax. (>: 240).
1. The lateral amygdalopetal pathway of the stria terminalis begins in the cells lying rostrally in the preoptic lateral area (Fig. 1A).
The fibers of this tract initially pass through the lateral area of bed
nucleus of the stria terminalis. Farther on they penetrate the ventral
component of the stria terminalis and in its supracapsular part lie laterally
to the comrnissural component (Fig. 2). They enter the amygdala posteriorly, passing mainly through the medial part of the central nucleus.
Terminal and preterminal degeneration was found, above all, in the
medioventral area of the medial and posterior segment of the basal
dorsal nucleus and, in a lesser degree in the medial part of the central
nucleus (Fig. 2A). If the area of lesion was small and occupied only the
rostra1 part of the preopticohypothalamic lateral area, there was no definite degeneration in the other amygdalopetal pathways nor in the rest
of the amygdaloid nuclei.
2. The medial amygdalopetal pathway starts in the neurons of the
preopticohypothalamic lateral area more caudally mainly in the lateral
hypothalamus (Fig. 1B).The amygdalopetal fibers of this pathway enter
the stria terminalis after passing through the lateral area of the bed
nucleus of the stria terminalis more caudally than the fibers of the
lateral amygdalopetal pathway. In the supracapsular part of the stria
terminalis the fibers of the medial amygdalopetal pathway are situated
in the ventral component of the stria, medially to its commissural component (Fig. 2). They are slightly less numerous and penetrate the
amygdaloid body more medially than the former fibers. They end mainly
dorsally, in the posterior and intermediate portions of the medial nucleus
of amygdala (Fig. 2B).
After cutting the supracapsular part of the stria terminalis we found
degenerating fibers in the stria between the site of lesion and the
amygdaloid body. These fibers, located mainly in the ventral portion
of the stria, lay in two bundles medially and laterally similar to those
after damage to the preopticohypothalamic lateral area. Following the
lesion of the stria the extent of degeneration in the amygdaloid nuclei
was generally similar to that of the preopticohypothalamic lateral lesion.
The only definite difference was the additional degeneration in the
ventroposterior part of the cortical nucleus of the amygdala.
3. The ventral amygdalopetal pathway similarly to the medial one,
begins in the neurons lying for the most part caudally in the hypothalamic lateral area. Its fibers are slightly finer than the amygdalopetal
axons of the stria terminalis. Owing to the location of the terminal degeneration in the amygdala (Fig. 2C) as well as to the course of the
amygdalopetal fibers, it is possible to distinguish two not clearly separated components in the ventral amygdalofugal pathway: the ventral
and the dorsal. The fibers of the ventral component run as a rule transversally to the medial part of the anterior amygdaloid area and to the
anterior part of the medial nucleus. Here the terminal degeneration is
very massive. In the medial nucleus of amygdala the projection area of
the ventral amygdalopetal pathway partly overlaps the one caused by
lesion in the stria terminalis. It was comparatively easy to distinguish
the degenerating fibers of both systems, as the fibers of the ventral
amygdalopetal pathway generally finer and their course is transversal,
while the fibers of the stria terminalis, enter the medial nucleus of
amygdala from the dorsocaudal side.
The fibers of the dorsal component run not only in a lateral direction
but also posteriorly. They pass through the dorsal part of the anterior
amygdaloid area, through the central nucleus and terminate a t the
neurons of the anterior pole of the basal dorsal nucleus.
The above shows that the lateral amygdalopetal pathway of the stria
and dorsal component of the ventral amygdalopetal pathway terminate
in the basal dorsal nucleus, partly in the central nucleus, i.e., in the
areas of a high AChE activity. On the other hand, the medial pathway
of the stria and the ventral component of ventral amygdalopetal pathway end in the nucleus medialis and in the anterior amygdaloid area,
where the AChE activity is low. Some terminals of these pathway can
be found in the cortical nucleus and rarely in the basal ventral nucleus,
although our data do not provide sufficient evidence of the latter suggestion. Neither we found degenerations in the lateral nucleus.
The area where according to our findings, the amygdalopetal axons
begin may be defined as the most lateral part of the hypothalamus.
Here the characterjstically large neurons of high AChE activity can be
found. From them emerge axons rich in AChE, which, after passing
through the lateral part of the bed nucleus of stria terminalis, appear
mainly in the lateral area of the ventral portion of the stria and run
towards the amygdaloid body. Some data seem to favor the idea that
these axons connect the lateral preopticohypothalamic area with the
amygdaloid body. Naturally cells of high AChE activity are not the only
nerve cells of this area and amygdalopetal connections may in a great
part begins in other types of neurons as well. On the other hand, experiments with horseradish peroxidase ( 6 ) show that large cells of this
area send axons to the cortex and to the reticular formation.
Conrad and Pfaff (I, 2) found some fibers projecting from the medial
preoptic area and anterior hypothalamus to the medial amygdaloid
nucleus. Observations of Swanson (14) and our results show the localization of amygdalofugal neurons in a more lateral region. Data concerning
the localization of terminals arising from neurons of the lateral preoptic-
ohypothalamic region in the amygdaloid body are also somewhat contradictory. Cowan et al. (3), following the lesions of the lateral hypothalamus,
found terminal degenerations in all nuclei of the rat amygdala except
its central nucleus. Swanson (14), using autoradiographic techniques,
traced in the rat an amygdalopetal projection from the lateral preoptic
area; axons of that projection terminate in most of the amygdala, but
they were not found in its lateral nucleus and the nucleus of the lateral
olfactory tract. The above-mentioned authors observed no striking differences in the supply of various areas of the amygdaloid nuclei by axons
arising from the preopticohypothalamic area. In our material, massive
terminal degenerations almost equally distributed in all areas of the
amygdala (except the nucleus of the lateral olfactory tract) were observed
only in those cases where a lesion localized in the lateral preopticohypothalamic region encroached, even slightly, on the anterior amygdaloid
area. If a lesion was localized exactly in the preopticohypothalamic region
without touching the neighboring structures, degenerating axons running
in all the above amygdalopetal pathway terminated in defined areas of
the amygdaloid body.
The investigation was supported by Project 10.4.1.01 of the Polish Academy
of Sciences.
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Accepted 21 February 1977
Liliana NITECKA, Olgierd NARKIEWICZ and Czeslaw JAKIEL, Institute of Medical Biology. School of Medicine, Dqbinki 1, 80-211 Gdafisk, Poland.