Download connections of the hypothalamus and preoptic area with nuclei of

ACTA N E U R O B I O L . EXP. 1081, 4 1 : 53-67
CONNECTIONS OF THE HYPOTHALAMUS AND PREOPTIC AREA
WITH NUCLEI OF THE AMYGDALOID BODY IN THE RAT;
HRP RETROGRADE TRANSPORT STUDY
Liliana NITECKA
Department of Anatomy, Institute of Medical Biology, Sch,ool of Medicine
Debinki 1, 80-211 Gdalisk, Poland
Key words: amygdaloid-hypothalamic connections, rat, horseradish peroxidase
Abstract. Horseradish peroxidase (HRP) was injected into various
nuclei of the amygdala in 50 rats. The retrograde axonal transport of
HRP showed various connections arising from the hypothalamic nuclei
and the basal forebrain. Neurons of the magnocellular preoptic nucleus
send out amygdalopetal axons to all amygdaloid nuclei except the lateral
nucleus. The amygdalopetal projections emerge from the large neurons
situated dorsally in the most lateral preoptic area (probably substantia
innominata) and terminate in the basal donsal and the central amygdaloid nuclei. Neurons in the lateral division of the hypothalamus (the
lateral hypothalamic area proper and the perifarnical region) send out
axons which terminate in the medial and central nuclei and in the
posterior part of the cortical amygdaloid nucleus. Axons emerging from
the ventromedial hypothalamic nucleus end mainly in the medial nucleus and in the central amygdaloid nucleus. Amygdalopetal fibers
arising from neurons of the ventral premammillary and dorsal hypothalamic nuclei reach the medial amygdaloid nucleus and perhaps a few of
them end in the posterior part of the cortical amygdaloid nucleus. Neurons of the bed nucleus of the stria terminalis project to the medial, the
posterior part of the cortical and probably to the basal dorsal amygdaloid nuclei.
INTRODUCTION
Experimental results and clinical observations indicate that both the
hypothalamus and the amygdaloid body control many autonomic functions, influence the endocrine glands and also affect the emotional
behavior and drives (11, 12, 15).
Neuroanatomical observations showed that the nuclei of the amygdaloid body receive projections from and send out axons to the hypothalamus and to some prosemcephalic structures (4-6, 8, 9, 16, 18, 19, 20,
26, 27, 33-36, 38, 39). The distribution of amygdalopetal pathways which
arise from the hypothalamus and preoptic area has been partly established in some experimental animals (4-6, 19, 20, 26, 27, 33-36, 38, 39).
However, few data are available concerning the exact distribution of
hypothalamic neurons sending amygdalopetal axons in the rat (33, 38).
This is due partly to the fact that the hypothalamic nuclei in the rat
are relatively small. It is difficult, therefore, to make selective lesions
or to inject labeled aminoacids strictly limited to a single nucleus.
Moreover, various pathways run through the lateral hypothalamus
(37) and their damage affects the results. It seems that experiments
carried out by the HRP retrograde transport method should be helpful
in establishing the precise location of the hypothalamic neurons projecting to various amygdaloid nuclei in the rat brain.
Our investigation was an attempt to find the precise origin of amygdalopetal axons in the hypothalamic and preoptic neurons by means of
the HRP retrograde transport method. The observations presented below
include the distribution of neupons sending amygdalopetal axons not
only in the hypothalamus and preoptic area but also in the bed nucleus
of the stria terminalis. This seemed uwful because the hypothalamus,
the preoptic area and the bed nucleus of stria terminalis-structures
derived according to Broadwell and Bleier (3) from a common embsiological anlage - are functionally interrelated and form an important
link of the limbic system. The nomenclature of the amygdaloid nuclei is
based on the results of our investigation on the cytoarchitectonics and
acetylcholinesterase (AChE) activirty in the amygdaloid nuclei of the
rat and other experimental animals (22, 28).
The nomenclature of the hypothalamic and preoptic nuclei is based
mainly on the results of cytoarchitectonical and embriological studies
by Bleier (2), Broadwell and Bleier (3), Gurdijan (13) and Swanson (36).
MATERIAL AND METHODS
Our material con~ist~s
of the brains of 50 Wistar rats of both sexes,
weigh 200-250 g. Injections of 0.05-0.5 p1 of 30°/o solution of horseradish
peroxidase (Sigma VI) were made in the nuclei of the amygdala through
a glass micropipette within 5-10 min. The postoperative survival time
was 24-48 h. The brains were subsequently perfused through the heart
with a 0.4O/o solution of paraformaldehyde and a 1.25OIo glutaraldehyde
in the 0.1 M phosphate buffer of pH 7.2. After removal from the skulls
the brains were fixed for 24 h in the perfusion solution. They were kept
for another 24 more hours in a 5OIo solution of sucrose in the 0.1 M
phosphate buffer'of pH 7.2. The brains were cut on a freezing microtome into 50 pm slices. Incubation was then carried out in 0.05O/o solution
of 3.3' - diaminobenzidine and afterwards, in the same solution plus
3OIo HzOz (0.3 m1/100 ml incubation solution).
The HRP was injected into the amygdaloid nuclei by two stereotactic approaches; the micropipette with the HRP solution was inserted
either (i) through the dorsal cerebral cortex and the striatum, or (ii)
through the piriform cortex. A detailed description of the histological
and surgical procedures was given in an earlier publications (24, 25).
RESULTS
CelLs containing HRP labeled granules were found in various nuclei
and areas of the hypothalamus. The examples of the results obtained
following HRP injecti'ons into the amygdaloid nuclei presented below
are chosen as the most characteristic ones.
Distribution of the H R P labeled neurons in the lateral
division of the hypothalamus and preoptic area
The HRP labeled cells were numerous here. They were found in
the most laterally situated parts of the lateral preoptic area and in
the lateral hypothalamic area proper (Fig. 2).
In the most lateral pireoptic area of rat numerous, large cells may
be seen. Their derivation is still controversial. Divac (10) defined them
as magnocellular nuclei of the basal forebrain. According to our own
observations and the results of cytoarchitectonic studies by Swanson
(36) in this most lateral region of the preoptic area two structures m a p
be differentiated: (i) magnocellular preoptic nucleus situated ventrally
and (ii) a dorsally situated area containing loosely scattered large cells
probably corresponding in some respect to the substantia innominata
of other animals.
The anterior pole of the magnocellular preoptic nucleus is found
in the frontal sections through the posterior portion of nucleus accumbens, while its posterior pole reaches the anterior hypothalamus. This
nucleus for the most part corresponds to Gurdijan's "nucleus intersti-
tialis septo-hypothalamicus" as well as Price and Powell's "nucleus of
the horizontal limb of the diagonal band" (13, 31, 32).
The substantia innominata cells are seen anteriarly at the level of
the posterior part of the nucleus accumbens; they are clearly visible
in all frontal sections through the preoptic area and the anterior pole
of the hypothalamus up to the level of the optic chiasma.
The HRP labeled cells in the ventral part of the most lateral region
of the preoptic area - magnocellular preoptic nucleus. In rat R-30 the
HRP injection involved nearly all the nuclei of the amygdala (Fig. 1).
1
2
3
Fig. 1. Localization of large H R P injection into t h e amygdala of t h e r a t R30. T h e
injection site is marked in black. Slight diffusion of t h e enzyme is indicated by
hatches. 1-3: Frontal sections i n t h e rostro-caudal order. Distribution of t h e H R P
labeled cells following injection is shown i n Fig. 2.
Rather numerous HRP labeled cells were observed in the preoptic
magnocellular nucleus (NPM; Fig. 2). They contained generally relatively few HRP labeled granules.
In almost all cases whe,re the HRP injections involved a single amygdaloid nucleus (Fig. 4) (the basal dorsal nucleus - rat R95, the basal
ventral nucleus - rat R94, the anterior parts of the basal ventral and
cortical nuclei - rat R45, posterior part of the cortical nucleus - rat R76,
the central nucleus - rat R60, the medial nucleus - rat R57) the HRP
labeled cells were observed in the preoptic rrlagnocellular nucleus.
Only after injections involving the la'teral numcleusof the amygdala rat R20, no HRP labeled cells were found in the preoptic magnocellular
nucleus (Fig. 5). Certain differences could be seen in the topographical
distribution of the labeled cells in the magnocellular preoptic nucleus
following injections of particular nuclei of the amygdaloid body. After
injections of the cortical nucleus and basal ventral nucleus labeled
cells appeared mainly in the vicinity of the anterior pole of the preoptic magnocellular nucleus (Fig. 4, rat R45). In the remaining cases the
distribution of the labeled cells was more unifotm. The magnocellular
preoptic nucleus in its rostra1 part abuts medially on the nucleus of
the horizontal limb of the diagonal band. Following the HRP injection
into various amygda1,oid nuclei, single labeled cells in the nucleus of
the horizontal limb of the diagonal band were sometimes observed.
Fig. 2. Distribution of t h e HRP labeled cells in the hypothalamus and preoptic
area in rat R30 following the injection shown i n Fig. 1. Dots represent labeled cells.
1-11: Frontal sections in the rmtro-caudal order.
The HRP labeled cells in the dorsal part of the most lat~eralregion
of th,e preop tic arela~substaatia innomi,nlata. Following a large in jection into the amygdaloid nuclei (Figs. 1 and 2, rat R30) the HRP labeled
cells were observed in the whole dorsal part of the most lateral preoptic area (SI, Figs. 2 and 3 A ) . They were comparatively more numerous
than in the magnocellular preoptic nucleus. The labeled neurons
were often clustered in the form of small islands consisting of
several average five cells. These were generally cells characte-
ristically round in shape. The labeled cells were comparatively most
numerous in the frontal sectio,ns passing through the anterior commissure. They were situated mainly inferolaterally to the bed nucleus of the
I
stria terminalis.
A similar localization of the HRP labeled cells was found in rats
R95 and R60 following the HRP injections into the basal dorsal nucleus
and into the medial and intermediate part's of the central nucleus
(Fig. 4, rats R95 and R60). In cases where the HRP injections involved
other nuclei of the amygdala (lateral, basal ventral, medial or cortical
nuclei) cells containing HRP labeled granules were not obse'rved in the
substantia innominata.
The HRP labeled neurons in the lateral hyp,othalamic area proper.
Following large injection into the amygdala HRP labeled cells were
observed in two regions 'of the proper lateral hypothalamic area: (HL,
Fig. 2) inferolaterally to the medial forebrain bundle and in the perifornical region. They appeared in the interm,ediate and posterior parts of
the hypothalamus; and p r e d o m i n a ~ t l yin the frontal sections passing
through the ventromedial hypothalamic nucleus. Cells lecated inferolaterally to medial forebrain bundle were most often of medium size
and contained many HRP labeled granules. There were a few of th,em
in one section.
In the perifornical region the HRP labeled oells were found in
various positions in relati,on to the column of fornix, sometimes above
and often below or medially. These were mostly quite large oval cells;
however, ~om~etimes
they were very elongated and fusiform. Generally
these neurons contained few HRP labeled granules. The number of
labeled neurons were slightly smaller here than in the immediate
vicinity of the medial forebrain bundle.
Similarly situated HRP labeled cells were observed following small
injections of the HRP into the posterior part of the cortical nucleus
(Fig. 4, rat R76) or the posterior portion of the medial nucleus (Fig. 4,
rat R57). In cases where injections involved other single amygdaloid
rluclei (the basal dorsal, basal ventral or the anterior part of the cortical nucleus) the labeled cells appeared rather sporadically (Fig. I ,
rats R95, R94 and R45) and they were regularly observed after 'injections involving selectively the central nucleus (Fig. 4, rat R60). The
labeled cells were not observed in the lateral hypothalamic area following injections into the lateral nucleus (Fig. 5, rat R20). In addition the
HRP labeled cells were found in the ventral tegmental area which is
sometimes considered as belonging to the lateral hypothalamus. Data
concerning the location of labeled cells in this area were presented in
another publication (25).
Distribufion of the HRP labeled neurons in the medial
division of the hypothalamus and preoptic area
After large injections of the HRP involving most of the amygdaloid
nuclei, labeled cells appeared in many structures of the medial hypothalamus, mainly in the ventromedial, ventral premammillary and the
posterior nucl'ei (Figs. 1 and 2, rat R30). Besides, labeled neurons appeared sporadically, in the supramammillary, the dorsal premammillary
nuclei, and also in other areas of the tuber cinereum.
The HRP labeled neurons in the ventromedial hypothalamic nucleus.
Iil rat R30 following a large injection of the HRP to the amygdaloid
nuclei labeled cells were p,rimarily found in the ventrolateral portion
of ventromedial nucleus (VM, Fig. 2). There were several of them in
each section. In the central and the doirsomedial portion of the nucleus
they appeared less frequ'ently. Labeled cells were located primarily
ip the peripheral part of the nucleus, more rarely appearing in its
central part. The labeled cells found here were small, oval, containing
comparatively few HRP lak'eled granul3s.
Similarly located labeled cells in the ventromedial hypothalamic
nucleus were found following injections selectively involving the medial nucleus, and mainly its posterior part (Fig. 4, R57). The HRP labeled cells in the ventromedial hypothalamic nucleus were clearly
visible, although much less numerous, after injections into the central
nucleus. The labeled c'ells were not observed in the ventromedial nucleus following inj,ections involving other amygdaloid nuclei: basal
dorsal, basal ventral, cortical or lateral (Fig. 4, rats R95, R94, R45,
R76 and Fig. 5, rat R20).
After large injections into the amygdala and smaller ones involving
only the medial nucleus the HRP labeled neurons were sometimes seen
in various areas of the tuber cinereum (Figs. 1, 2 and 3). They appeared
here in small numbers, rather sporadically and were 1,ocated anteriorly
in the area of tuber cinereum, lying above the ventromedial hypothalamic nucleus.
The HRP label'ed cells in the ventral premammillary nucleus. In the
rat R30 following a large injection of the HRP into the amygdala, significant numbers of labeled neurons were observed in the ventral premammillary nucleus (PV, Figs. 1 and 2). They were situated in the
central part of the nucleus, which contain )tightly packed medium size
cells. Labeled cells of the ventral premammillary nucleus were numerous and contained many distinct HRP labeled granules.
A similar location and distribution of the labeled cells in the ventral
-
premammillary nucleus was observed after injections involving only
the medial nucleus (Fig. 4, R57). Single labeled cells appeared here
following selective injeotions into the posterior part of the cortical
nucleus (Fig. 4, R76). After injections into other amygdaloid nuclei no
HlZP labeled cells were seen in the vent.r8al plremammillary nucleus
(F'ig. 4, R95, R94, R60 and Fig. 5, R20).
The HRP labeled cells in the posterior hypothalamic nucleus. In
the posterior hypothalamic nucleus only single HRP labeled cellls
were found, 1-2 in respective sections. They appeared after large injections of HRP to the amygdala (NP, Fig. 2, rat R30) and also in cases
of small injections involving the medial nucleus (Fig. 4, R57).
Moreover, after large injections of HRP to the amygdala (Figs. 1
and 2, R30) labeled cells appeared sporadically in the dorsal premammiliary nucleus and in the supramammillary nucleuls. Labeled neurons of
the latter contained many granules. In cases of small injectifons single
labeled cells in the dorsal premammillary nucleus were observed after
injections limited to the medial nucleus while in the supramammillary
nucleus after injections, selectively involving the medial nucleus or
posterior part of cortical nucleus, and sometimes after injections into
the rostra1 part of the cortical nucleus.
Distribution of HRP labeled neurons in the bed nucleus
of the stria terminalis
The HRP labeled cells following injections into the majority of
nuclei of the amygdala (Fig. 1, rat R30) were seen primarily in the
inferoposterior portion of the bed nucleus of the stria terminalis. They
were visib1,e in frontal seotions through the posterior region of thz
preoptic area and anterior hypothalamus; in the part of the nucleus,
which lies just above the lateral and medial portion of the preoptic
area and anterior hypothalamuis (NXT, Fig. 2). This area of t h e bed
nucleus of the stria terminalis corresponds to "medial preoptic hypothalamic junction al-ea" according to de Olmos and Ingren (9). The
labeled cells here were of medium size and oval shape, they contained
many HRP labeled granules. Besid,es, several HRP labeled cells appeared in the anterolateral a,rea of the bed nucleus of stria terminali~s;all
of them were located along the lateral edge of the nucleus.
Following small injeotions involving the medial nucleus (Fig. 4, R57)
or the posterior part of the cortical nucleus (Fig. 4, R76) HRP labeled
cells appeared in the above described posteroinferior portion of the
bed nucleus of the stria terminalis; whereas in the anterolateral portion
of this nucleus labeled cells were seen f'o'llowing injection involving
basal dorsal nucleus (Fig. 4, R95).
Fig. 3.
Dark field microphotographes of labeled cells from the substantia innominata
(A) and ventral premammillary nucleus (B) i n r a t R30.
Fig. 4. Localization of small HRP injections R60'
into single amygdaloid nuclei. Injections involve mainly: basal dorsal nucleus (rat - R95),
basal ventral nucleus (rat - R94), anterior
parts of the cortical and basal ventral nuclei
(rat-R45),
posterior part of the cortical
nucleus (rat - R76), central nucleus (rat - R60),
and medial nucleus (rat -R57). Denotations as
in Fig. 1.
Fig. 5. Localization of a small HRP
injection into the lateral amygdaloid
nucleus (rat -R%O). No labeled cells in
the preoptic-hypothalamic area following this injection were observed.
Fig. 6. Diagram showing the origin and termination of the amygdalopetal axons
arising from the ventral part of the most lateral region of the preoptic area
(preoptic magnocellular nucleus). Amygdaloid nuclei supplied by these axons are
indicated by hatches.
Fig. 7. Diagram of the origin and
termination of the amygdalapetal axons
arising from the dorsal part of the
most lateral region of the greoptic
area (probably substantia innominata).
Denotations as in Fig. 6.
Wig. 8. Diagram of the origin and
termination of amygdalopdal axons
arising from the lateral hypothalamus
(lateral hypothalamic area and perifornical region). Denotations as in
Fig. 6.
CONCLUSIONS AND DISCUSSION
The experimental results lead to the conclusion that all nucl.ei of
the amygdaloid body - excluding the lateral nucleus receive direct
afferent connections from the hypothalamus or from neurons of the
basal forebrain: the preoptic area and the bed nucleus of the stria
terminalis.
These clolnnectionls either terminate in a dispersed manner in most
of the nuclei of the amygdaloid body o'r end in one or more of its.
Amygdalopetal axons emerging from neurons of the magnocellular
preoptic nucleus seem to extend to most of the amygdaloid nuclei
(Fig. 6). The only exception is the lateral nucleus of the amygdala,
which probably also receive no afferent connections from the hypothalamus and other preoptic areas. The neurons of the magnocellular
preoptic nucleus seem to be the only 'source of the preoptic and hypothalamic projections running to th,e cortical and basal ventral nuclei.
The investigations by Beckstead (1) indicate that the magnocellular
preoptic nucleus sends also projections to the entorhinal cortex as well.
Acconding to results of Price and Powell (31, 32) and Swanson (36),
the magnocellular preoptic nucleus hais reciprocal connections with
the olfactory bulb, and projects to various areas of ,the limbic system,
including the amygdala. It may thus ,,be,supposed tha't the magnocellular
preoptic nucleus transmits impulses from the olfactory bulb to the
amygdaloid nuclei while receiving reciprocal projections from the amygdala.
Among the amygdalopetal axons which arise in the preoptic-hypothalamic area and project to particular amygdaloid nuclei, we may
distinguish connections which emerge from: (i) dorsal area of most
lateral region of the preoptic area, (ii) the proper lateral hypothalamic
area, (iii) the medial hypothalamus.
The neurons located in the dor,sal part of m80st lateral region of the
preoptic area seem to correspond well to the substantia irinominata,
althcugh according to Divac (10) no substantia innominata is present
in the rat's brain.
Amygd,alopet'al connections which arise from neunons situated in
the extreme dorso-lateral preoptic area end in the basal dor,sal nucleus
and in the medial and intermediate parts of the central nucleus (Fig. 7).
The pTesence of these amygdalopetal lconnections in the brain of the
rat was suggested by earlier experimental results carried out by silver
degeneration methods and autoradiography (26, 27, 36).
Amygdalofugal axons arising from (the basal dorsal and central nuclei of the amygdala have been found to terminate in the substantia
'
innominata (16, 36). Experimental data indicate that some profections
from the brainstem, among others from the taste and .auditory areas,
also termi'nate in the subst,ant'ia innominata of the primates (14, 29, 303.
Moreover, large neurons of substantia innominata, like the neurons of
other rnagnocellular nuclei of the basal forebrain, project abundantly
to various cortical areas (10). It is possible that the neocortex s e ~ d s
ont axons to the substantia innominata, from which, in turn, it receives
projeations. In this way, the neocortex may directly influence the
amygdala. The data on the function of the substantia innominata are
scanty, but some authors (7, 14) suggest that it may exert a n effect
on th,e emotional behavior and feeding activities. This would explain
the role of the amygdalopetal projections arising from this area.
The axons of the amygdalopetal projection from the subst'antia
innominata terminate mainly in the basal dorsal nucleus and the medial
part of the central nucleus. The basal dorsal nucleus according to our
data, in turn, send out short axonal projections to almost all the
remaining nuclei of th,e amygdala (23).
The neurons located in the lateral hypothalamic area proper project
mainly to the medial amygdaloid nuc1,eus and to the posterior part of
the cortical nucleus; and, to a lesser degree to the central nucleus and
may be to other nuclei of the amygdala (Fig. 8).
These connections have not been previously reported. They were
not apparent in our studies carried out by silver degeneration methods:
(26, 27). The amygdalofugal connections running to (the lateral hypothalamus were described by Krettek and Price (16). According to these
investigators, these paths begin in the medial, cortical and central
amygdaloid nuclei.
Studies on the lateral hypothalamus indicate that its function is
related to the control of some drives, and, predominantly, the control
of Ceeciirig activities and flight and defanse responses (11, 12, 15). It is
considered that the mcdial and cortical and perhaps the also basal
ventral amygdaloid nuclei, are functionally related Oo the la'teral hypothalamus (15). Stimulation of these nuclei may induce hyperphagia,
and hypophagia may result from their injury. Opposite alimentary
reactions are obtained from the basal dorsal amygdaloid nucleus. There
is no evidence that the basal dorsal tamygdlaloid nucleus is directly
connected to the lateral hypothalamus. Jt may, however, exert its effect
on the lrateral hypothalamus by acting through the medial amygdaloid
nucleus to which it projects by short intraamygdaloid connections (23).
An amygdalopetal projection, similar to that originating in the
neurons of the lateral hypqthalamus, seems to arise from the cells
located in the infero-posterior portion of the bed nucleus of the stria
krmindis. The fibers beginning here te~minaeein the !medial nucleus
and the posterior part of the costic~alnucleus.
Amygdalopetal connections emerging from the medial hypothalamus.
Several structures of the medial hypothalamus seem lto send out projections to amygdala. They arise mainly from the venbromedial, ventral
premammillary and the posterior nuclei. Some axons may also originate
in other areas of the tuber cinereum, in the dorsal premammillary
and the supramammillary nuclei. They terminate primarily in the
medial nucleus, and also in the central and the posterior part of the
cortical *amygdaloidnuclei (Fig. 9). With regard to the cortical a'mygda-
Fig. 9. Diagram of the origin and termination of amygdalopetal axons arising from
the nuclei of the medial hypothalamus. Amygdaloid nuclei supplied by these axons
are indicated by hatches; broken hatches indicate nuclei with probable projections
from the medial hypothalamus. Denotations as in Fig. 6.
loid nucleus we may assume that impulses from the medial hypothalamus are conducted there mainly indirectly via the medial nucleus,
w'hich sends out a large intraamygdaloid ,projection to the cortical
nucleus (8, 17, 23).
The amygdalopetal projections arising from the ventromedial hypo-,
thalamic nucleus, as established in this report, are in agreement with
aut'oradiographic studies by other authors (5, 34). Renaud and Hopkins
(33) who injected the HRP into t'he amygdala, also found labeled cells
in the ventromedial hypothalamic nucleus of the rat. The resultts of the
present report, however, do not fully agree with those .of the above
authors.
Our observations together with those of other investigators (8, 16)
show that connections between the amygdala, on one side, and the
I
ventromedial nucleus and the premammillary area, on other, are reciprocal.
The interconnected areas of the medial hypothalamus (the area of
tuber cinereum including the ventromedial nucleus) and the amygdala
(the medial and cortical nuclei) have, according to Kaada (15) an activating effect on the sexual behavior, e.g. they induce ovulation, release
of gonadotropins and uterine movements.
As mentio'ned before the amygdaloid lateral nucleus is the only
part of the amygdala which probably neither sends out nor receives
projections to
from the hypothalamus and the basal foreb~ain(nuclei.
Nevertleless, the lateral, amygdaloid nucleus receives direct projections
from the posterior-thalamic region and the peripeduncular nucleus (14,
21). The pulvinar-posterior system of the thralamus, as a whole is
involved in the integration of a variety of sensory imputs. This permits
an assumption that the impulses conducted by these projections are
related to sensory perception.
I
This investigation was supported by Project 09.4.1 of the Polish Academy of
Sciences.
REFERENCES
1. BECKSTEAD, R. M. 1978. Afferent connections of the entorhinal area in the
rat demonstrated by retrograde cell-labeling with horseradish peroxidase.
Brain Res. 152: 249-264.
2. BLEIER, R. 1961. The hypothalamus of the cat: A cytoarchitectonic atlas in
the Horsley-Clarke coordinate system. Johns Hopkins Press, Baltimore,
1-109.
3. BROADWELL, R. D. and BLEIER, R. 1976. A cytoarchitectonic atlas of mouse
hypothalamus. J. Comp. Neurol. 167: 315-340.
4. CONRAD, L. C. A. and PFAFF, D. W. 1976. Efferents from medial basal
forebrain and hypothalamus in the rat. I. An autoradiographic study of
the medial preoptic area. J. Comp. Neurol. 169: 185-219.
5. CONRAD, L. C. A. and PFAFF, D. W. 1976. Efferents from medial basal
forebrain and hypothalamus in the rat. 11. An autoradiographic study of
the anterior hypothalamus. J. Comp. Neunol. 169: 221-261.
6. COWAN, W. M., RAISMAN, G. and POWELL, T. P . S. 1965. The connections
of the amygdala. J. Neurol. Neurosurg. Psychiatr. 28: 137-151.
7. DE LONG, M. R. 1971. Activity of pallidal neurons during movement. J. Neurophysiol. 34: 414-427.
8. DE OLMOS, J. S. 1972. The amygdaloid projection field in the rat as studied
with the cupric silver method. In B. E. Eleftheriou (ed.), The neurobiology
of the amygdala. Plenum Press, New York, p. 145-205.
9. DE OLMOS, J. S. and INGRAM, W. R. 1972. The projection field of the stria
terminalis in the rat brain. J. cornp. Neurol. 146: 303-335.
10. DIVAC, J. 1975. Magnocellular nuclei of the basal forebrain project to neo-
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.
5
cortex, brain stem, and olfactory bulb. Review of some functional correlates.
Brain Res. 93: 385-399.
FONBERG, E. 1967. The role of the amygdaloid nucleus in animal behaviour.
Progr. Brain Res. 22: 273-280.
FONBERG, E. 1969. T h e role of the hypothalamus and amygdala; food intake,
alimentary motivation, and emotional reactions. Acta Biol. Exp. 29: 335-358.
GURDIJAN, E. S. 1927. The d i e n c e ~ h a l o nof the albino rat. Studies on t h e
brain of the rat. J. Com,p. Neurol. 43: 1-114.
JONES, E. G., BURTON, H., SAPER, C. and SWANSON, L. W. 1976. Midbrain,
diencephalic and cortical relationships of the basal nucleus of Meynert and
associated structures in primates. J. Comp. Neurol. 167: 385-420.
KAADA, B. R. 1972. Stimulation and regional ablation of the amygdaloid
complex with reference to functional representations. In B. E. Eleftheriou
(ed.),The neurobiology of the amygdala. Plenum Press, New Yor'k, p. 205281.
KRETTEK, J. E. a n d PRICE, J. L. 1978. Amygdaloid projections to subcortical
structures within the basal forebrain and brainstem in t h e rat and cat.
J. Comp. Neurol. 178: 225-254.
KRETTEK, J. E. and PRICE, J. L. 1978. A description of the amygdaloid
complex in the r a t and cat with observations on intra-amygdaloid axonal
connections. J. Comp. Neurol. 178: 255-280.
LEONARD, C. M. and SCOTT, J. W. 1971. Origin and distribution of the
amygdalofugal pathways in the rat. An experimental neuroanatomical
study. J. Comp. Neurol. 141: 313-331.
NAUTA, W. J. H. 1962. Neural associations of the amygdaloid complex in the
monkey. Brain Res. 85: 505-520.
NAUTA, W. J . H. and HAYMAKER, W. 1969. Hypothalamic nuclei and fiber
connections. In W. Haymaker, E. Anderson, and W. J. H. Nauta (ed.), T h e
hypothalamus. Charles C. Thomas, Springfield.
NITECKA, L. 1979. Connections of the posterior thalamus with the amygdaloid
body of the rat. Acta Neurobiol. Exp. 39: 49-55.
NITECKA, L. 1975. Comparative anatomic aspects of localization of acetylcholinesterase activity in the amygdaloid body. Folia Morphol. 34: 167-185.
NITECKA, L., AMERSKI, L. and NARKIEWICZ, 0. 1980. Organization of intraand inter-amygdaloid connections in the rat brain. J. F. Hirnforsch. (in
press).
NITECKA, L., AMERSKI, L., PANEK-MIKUEA, J. and NARKIEWICZ, 0. 1979.
Thalamoamygdaloid connections studied by the method ,of retrograde transport. Acta Neurobiol. Exp. 39: 585-601.
NITECKA, L., AMERSKI, L., PANEK-MIKUEA, J. and NARKIEWICZ, 0. 1980.
Tegmental afferents of the amygdaloid body in t h e rat. Acta Neurobio~l.
Exp. 40: 609-624.
NITECKA, L. anmd JAKIEL, C. 1978. Connections of the lateral preoptic-hypothalamic area with amygdaloid nuclei in the rat. Folia Morphol. 37: 13-31.
NITECKA, L., NARKIEWICZ, 0. and JAKIEL, C. 1977. The organization of
amygdalopetal projections from the lateral hypothalamus and preoptic
area in t h e rat. Acta Neurobio~l.Exp. 37: 247-252.
NITECKA, L., NARKIEWICZ, 0. and ZAWISTOWSKA, H. 1971. Acetylcholinesterase activity in the nuclei of the amygdaloid complex in the rat.
Acta Neurobiol. Exp. 31: 383-389.
- Acta
Neurobiol. Exp. 1/81
29. NORGREN, R. 1976. Taste pathways to hypothalamus and amygdala. J. Comp.
Neurol. 166: 17-30.
30. NORGREN, R. and LEONARD, CH. M. 1973. Ascending central gustatory
pathways. J. Comp. Neurol. 150: 217-238.
31. PRICE, J. L. and POWELL, T. P. S. 1970. An experimental study of the origin
and the course of the centrifugal fibers to the olfactory bulb in the rat.
J. of Anat. 107: 215-237.
32. PRICE, J. 0. and POWELL, T. P. S. 1970. The afferent connections of the
nucleus of the horizontal limb of the diagonal band. J. Anat. 107: 239-256.
33. RENAUD, L. P. and HOPKINS, D. A. 1977. Amygdala afferents from the
mediobasal hypothalamus: an electrophysiological and neuroaqatmical
study in the rat. Brain Res. 121: 201-214.
34. SAPER, C. B.,SWANSON, L. W. and COWAN, W. M. 1976. The efferent connections of the ventromedial nucleus of the hypothalamus of the rat. J. Comp.
Neurol. 169: 409-442.
35. SAPEX%,C. B., SWANSON, L. W., and COWAN, W. M. The efferent connections of the anterior hypothalarnic'area of the rat, cat and monkey.
J. Comp. Neurol. 182: 575-600.
36. SWANSON, L. W. 1976. An autoradiographic study of the efferent connections
of the preoptic region in the rat. J. Comp. Neurol. 167: 227-256.
37. UNGERSTEDT, U. 1971. Stereotaxic mmping of the monoamine pathways in
the rat brain. Acta Physiol. Scand. 81. Suppl. 367: 1-48.
38. VEENING, J. G. 1978. Subcortical afferents of the amygdaloid complex in the
rat. Neurosci. Lett. 8: 196-202.
39. WAKEFIELD, D. C. and HALL, E. 1974. Hypothalamic projections to the
amygdala in the cat. Cell. Tiss. Res. 151: 499508.
Accepted 15 September 1980
ABBREVIATIONS
Ac
ALH
nucleus accumbens
lateral hypothalamic area
BD
basal dorsal nucleus of the amygdala
BV
basal ventral nucleus of the amygdala
C
central nucleus of the amygdala
Ca
anterior commissure
CM
mammillary body
Co
cortical nucleus of the amygdala
Coa
cortical nucleus of the amygdala (anterior part)
COP cortical nucleus of the amygdala (posterior part)
dorsomedial nucleus of the hypothalamus
DM
F
fornix
FPM medial forebrain bundle
HA
anterior hypothalamic area
HL
lateral part of the hypothalamus
L
lateral nucleus of the amygdala
LM lemniscus medialis
M
medial nucleus of the amygdala
NP
posterior nucleus of the hypothalamus
NPM preoptic magnocellular nucleus
bed nucleus of the stria terminalis
NST
NTOL nucleus of the lateral olfactory tract
PD
dorsal premammillary nucleus
lateral preoptic area
PL
medial preoptic area
PM
ventral premammillary nucleus
PV
perifornical region
RP
substantia innominata
SI
supramammillary nucleus
SM
ventromedial nucleus of the hypothalamus
VM
ventral tegmental area
VT