Brain Research, 190 (1980) 347-368
© Elsevier/North-HollandBiomedicalPress
347
CORTICAL AND SUBCORTICAL AFFERENTS TO THE A M Y G D A L A OF
THE RHESUS MONKEY ( M A C A C A M U L A T T A )
J. P. AGGLETON, M. J. BURTON and R. E. PASSINGHAM
Department of Experimental Psychology, University of Oxford, South Parks Road, Oxford OX1 3UD
(U.K.)
(Accepted October 25th, 1979)
Key words: amygdala -- monkey -- horseradish peroxidase
SUMMARY
The afferent projections to the primate amygdala were studied using horseradish
peroxidase. The potential advantages of this technique are discussed compared with
those previously used to determine amygdaloid afferents. The findings indicate that
certain agranular or dysgranular cortical regions may project directly to the amygdala:
in particular, the orbital frontal cortex, anterior cingulate gyrus, subcallosal gyrus,
temporal pole and anterior insula. These projections probably terminate predominantly in either the lateral or accessory basal nuclei. Other cortical projections from
the inferotemporal and superior temporal gyri are described. Evidence was found for a
heavy projection from the superior temporal sulcus to the lateral nucleus. Subcortical
afferents were found from the hypothalamus, substantia innominata, diagonal band,
thalamus, periaqueductal central gray, peripeduncular nucleus and from a band of
cells extending medially from the peripeduncular nucleus to the midline, just ventral to
the thalamus. In the thalamus, labelled cells were restricted to the non-specific nuclei,
and were common in the rostral midline nuclei. No projection was observed from the
dorsomedial nucleus of the thalamus. We discuss the implications of these results for
interpreting the functions of the amygdala.
INTRODUCTION
It has frequently been supposed that the amygdala plays a role in the control of
emotion and motivation12,1L One clue to the function of the amygdala is provided by
knowledge of its anatomical connections, and by inference the classes of information it
receives. Since lesions of this area are made in the treatment of epileptic, hyperkinetic
and hyperaggressive disorders it is clearly of crucial importance that our understanding of these connections be as accurate and refined as possible.
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There are, however, problems in interpreting some of the relevant anatomical
evidence. Neuronographic studies a4,45 indicated that the amygdala was directly interconnected with the orbital frontal, subcallosal and cingulate cortex and with the
anterior insula and the temporal pole. Evidence that some fibre pathways do not
respond to strychnine 11,57 or can show transsynaptic synchronous conduction 57 leaves
these results inconclusive. More reliable information concerning afferents to the
amygdala has been obtained from anterograde degeneration studies 15,~9. Although
such studies have been successful in looking at cortical projections, subcortical
projections have been more difficult to elucidate by this technique. Interpretation is
difficult because fibres of passage may be damaged, as well as afferent axons projecting
from the area of the lesion. Thus Nauta a° made lesions of the dorsomedial nucleus of
the thalamus and reported terminal degeneration in the amygdala; but it is unclear if
this resulted from damage to fibres traversing the lesion site and not arising from it.
This technique is also inefficient if the aim is to delineate the precise boundaries of the
areas which project into a structure, or to produce an exhaustive list of its afferents.
These objections can be largely overcome by utilizing the retrograde axonal
transport of horseradish peroxidase (HRP) 31. Although there is evidence that H R P
can be taken up by severed fibres of passage 6°, the damage to such fibres may be
assumed to be far less than in a comparable lesion degeneration study. In the present
study, horseradish peroxidase was injected into the amygdala in a series of rhesus
monkeys and the brains then studied for evidence of retrograde cell labelling.
Injections were made into subareas of the amygdala, as defined cytoarchitectonically9.
There is evidence that the different amygdaloid areas may subserve different functions 23, and by making localized injections we hoped to discover not only which areas
project to the amygdala but also in which nuclei they terminate.
METHODS
Subjects
Nine rhesus monkeys (Macaca mulatta) were used. Of these, 5 had previously
been used for behavioural studies and had bilateral lesions. Two (nos. 182 and 113)
had lesions confined to the sulcus principalis in the prefrontal cortex. Two (nos. 103
and 105) had lesions of the dorsolateral prefrontal cortex, anterior to the arcuate
sulcus and including sulcus principalis and the cortex of the dorsal convexity. One had
the superior colliculi removed (no. 231). The extent of the cortical lesions is shown in
Figs. 3, 4 and 5.
Fig. 1. Diagram of the sites of the HRP injections, plotted on coronal sections taken through the
extent of the amygdala. The cross-hatched area indicates the extent of the HRP reaction product and
the blackened region marks the centre of the injection (see the section 'Analysis'). The large numerals
identify the animals. The small numerals refer to the number of microlitres of HRP (50 %) injected.
Abbreviations : A, anterior area of amygdala; Ab, accessory basal nucleus; AC, anterior commissure;
Bla, basolateral nuclei; C, central nucleus; CA, caudate; CL, claustrum; Co, cortical nucleus; GP,
globus pallidus; La, lateral nucleus; Lb, lateral basal nucleus; Mb, medial basal nucleus; Me, medial
nucleus; OC, optic chiasm; OT, optic tract; P, putamen; Pam, periamygdaloid nucleus; Pyr,
prepiriform cortex; RS, rhinal sulcus; SF, sylvian fissure; STS, superior temporal sulcus.
020
65
0-20
Fig. 2. Diagram of the site o f the H R P injections. Conventions as in Fig. I.
351
Injections
Operations were carried out under intravenous pentothal anaesthesia. A 1 #1
Hamilton syringe was used to inject 0.1-0.85 #1 of 50 ~ horseradish peroxidase (Sigma
Type IV) dissolved in a 0.9 ~o physiological saline solution. A single unilateral injection
was hydraulically delivered over a period of 10 rain. Where previously operated
animals were used, care was taken to match their injections with those made into
unoperated animals.
It was not possible to rely on the stereotaxic co-ordinates given by the atlas of
Snider and Lee 5°, since the animals varied considerably in size (5.0-8.3 kg) and the
stereotaxic co-ordinate of any structure differs with the size of the animal 55. In
previous investigations in the rhesus monkey we found that the amygdala maintains a
constant position with respect to the posterior margin of the sphenoid bone, despite
variations in brain and skull size. The sphenoid bone was visualised using X-ray
photographs taken during the course of the operation (typically 90 kV at 30 mA for
0.5 sec using Kodak X-ray plates). The anteroposterior and dorsoventral coordinates
were taken relative to the posterior tip of the sphenoid, whilst the lateral co-ordinate,
which is the least variable between animals 55 was calculated on the basis of previous
experiments.
The animals were sacrificed 24 h after the injection. Those animals which had
been previously operated upon and had lesions were kept under urethane anaesthesia
during the intervening period, to comply with U.K. Home Office regulations. All of
the animals were then given a lethal intravenous injection of barbiturate anaesthetic
(Nembutal) and perfused with a mixture of 2 . 5 ~ paraformaldehyde and 1.5~
glutaraldehyde in 0. I M phosphate buffer. The brains were blocked in the stereotaxic
vertical plane, as shown in Figs. 3, 4 and 5. The brains were kept in 30 ~ sucrose buffer
for the next 48-72 h at pH 7.2 at 4 °C. They were then cut in 50 #m coronal sections on
a freezing microtome and every section was retained. Two l-in-10 series of adjacent
sections were saved and these were reacted with diaminobenzidine (BDH) 14 and 0.4 9/00
o-dianisidine (Sigma) 7 respectively. The sections were mounted and the dianisidine
series was then counterstained with cresyl violet and the diaminobenzidine (DAB)
series with thionine. This material was studied microscopically with both bright- and
dark-field illumination. In one animal (no. 105) only a diaminobenzidine series was
prepared. The reaction proved to be significantly more sensitive with dianisidine than
DAB, both in the area of the injection site and in the degree of retrograde labelling.
The majority of the results were therefore derived from the dianisidine series, of which
every section was studied. The overall picture from the DAB series was similar in the
location of the cells found, and only differed quantitatively.
Analysis
The position and extent of the HRP injections were plotted on to a standardized
series of coronal sections, taken throughout the extent of the amygdala as shown in
Figs. 1 and 2. That part of the reaction product which was so dense that no underlying
cell structures could be discerned microscopically is shown in black. The remaining
extent of the reaction product is shown by the hatched lines. This is not meant to imply
352
that the area of HRP uptake is equivalent to the area shown in black, although there
is good evidence that the area of active HRP uptake is less than the full extent of the
reaction product 60.
Some indication of the extent of uptake could be inferred by reference to
previous studies of amygdala afferents 15, and by comparing the results of overlapping
injections in the present study. Despite partially overlapping regions of reaction
product, evidence of discrete zones of HRP uptake is supplied by the consistently
different distributions of labelled cells (nos. 113, 182 and 355). In animal no. 355 the
injection (Fig. 2), although centred on the lateral basal nucleus, extended into several
other nuclei; but the striking lack of labelled cells in the temporal lobe (Fig. 4) in this
animal suggests that the area of active HRP uptake was confined to the lateral basal
nucleus 15. In addition it was possible to assess the contribution of uptake from areas
outside the amygdala by comparing the largest with the more discrete injections.
Animals nos. 105 and 103 both showed the greatest spread of HRP from the injection
site into adjoining structures, in particular the putamen, claustrum and globus pallidus
(Fig. 1). In both animals label was found in caudal inferotemporal cortex, area 6,
posterior cingulate cortex, somatosensory area I1, and thalamic nuclei including
nucleus ventralis posteralis (VPM and VPLo) and nucleus ventralis lateralis (VLm and
VLo). These areas were not labelled with more restricted injections. This indicates
that the occasional striatal HRP reaction product seen in those animals with more
restricted injections did not contribute to the overall pattern of labelling. Thus active
uptake probably did not occur at the striatal periphery of the injection site in these
animals.
It was of some concern that HRP might be taken up by damaged fibres of
passage, especially as we often damaged the caudal end of the anterior commissure in
our approach to the amygdala. But the label seen in the contralateral hemisphere did
not correspond to the projections of the anterior commissure 62 except in animals 103
and 105. Also, animal 355 showed virtually no label in the temporal lobe, although
there was damage to the caudal part of the anterior commissure and the spread from
the injection extended up as far as the commissure and into the lateral white matter.
We therefore think it unlikely that, with the probable exceptions of animals 103 and
105, there was significant uptake of HRP by the fibres of the anterior commissure.
RESULTS
The position and extent of the cortical label in the ipsilateral hemisphere was
plotted on standardized diagrams (Figs. 3, 4 and 5). The sylvian fissure (Figs. 3, 4 and
5) and the superior temporal sulcus (STS) (Fig. 6) were opened up to allow the
representation of labelled cells found within them. Each dot in the diagram represents
one labelled cell. The concentration of label in other sulci is not represented on the
surface view, though its extent is shown by dots lying alongside the sulci (Figs. 3, 4 and
5). The vertical dashed lines mark the caudalmost sections that were saved and
studied. Where no labelled cells are reported, none were found. Though the contralateral hemisphere was scanned, the results reported here are almost exclusively for the
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Fig. 3. Diagram of cortical labelled cells. Each dot represents one labelled cell exceptfor certain sulci,
as explained in the section on 'Analysis". The blackened areas indicate the extent of removal of
prefrontal cortex. The sylvian fissure has been opened up to expose the insula. Sections were saved and
studied anterior to the vertical dashed line. The position and extent of the respective injections is
shown on the right. Abbreviations: CC, corpus callosum; CIN, cingulate sulcus; CS, central sulcus;
INS, insula; IP, intraparietal sulcus; IT, inferotemporal sulcus; OS, orbital sulcus; OT, occipitotemporal sulcus; RS, rhinal sulcus; SF, sylvian fissure; SP, sulcus principalis; STS, superior temporal
sulcus.
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Fig. 4. Conventions as for Fig. 3.
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ipsilateral hemisphere. The cortical nomenclature is based on Von Bonin and Bailey's
study 54, except for the prefrontal cortex where the more detailed description provided
by Walker s8 is used.
Temporal lobe
Evidence for temporal lobe afferents was first obtained after injections aimed at
filling the amygdala (nos. 103 and 105). In these animals, the basolateral nuclei were
comprehensively covered (Fig. 1), although some corticomedial areas were not
involved. As there was spread of H R P into adjoining structures we subsequently made
more discrete injections. In this way we could check that the projection was indeed to
the amygdala and provide more detailed evidence concerning its site of termination.
Injections involving the corticomedial areas (nos. 113, 231 and 65) provided a more
complete picture of temporal-amygdaloid afferents.
(a) lnferotemporal cortex. Injections centred on the lateral nucleus (nos. 104 and
182) produced the pattern of labelled cells shown diagrammatically in Fig. 4. A low
concentration of label was found in the anterior inferotemporal area (TE), which
continued ventrally into areas T H and TF. HRP-positive cells were found as far
posterior as the anterior portion of the occipitotemporal sulcus. The labelled cells in
the inferotemporal cortex were predominantly pyramidal, being confined to layers III
and V. On the ventral surface of the temporal lobe (TH and TF) the majority were
found in layer V, but as one moved more dorsally towards the superior temporal
sulcus (TE), an increasing proportion were in layer III. Inferotemporal label was not
seen after any other localized amygdaloid injections.
(b) Superior temporal sulcus. Extensive injections which included the basolateral
nuclei (nos. 103 and 105) (Fig. 1) resulted in high concentrations of labelled cells in
both banks and fundus of the superior temporal sulcus (STS) which in animal 103
extended posteriorly to a level with the caudal extent of the sylvian fissure (Fig. 3). A
similar distribution of label was found after injections centred on the lateral nucleus
(nos. 104 and 182) (Figs. 4 and 6). In animal 104, labelled cells were found in all subareas of the rostral half of STS, but no cells were found in the caudal half of the sulcus,
including most of OAa 4s. This sulcal area accounted for approximately one fifth of all
the label found in animals 104 and 182. Evidence for similar but lighter contralateral
labelling was found in those animals (nos. 104 and 182) with lateral amygdala
injections. The ipsilateral label was mainly restricted to pyramidal cells. These were in
layer III, especially in the deeper portion, and a few in layer V. The contralateral label
was solely in layer III.
Evidence for afferents to the medial nuclei of the amygdala were derived from
only one animal (no. 65). After an injection of the medial and central nuclei with involvement of the substantia innominata an occasional cell could be seen in the banks
of the STS (Fig. 3).
Fig. 6. Diagram of projection from superior temporal sulcus and temporal lobe to the amygdala. Each
dot represents one labelled cell. The sulcus has been opened up and shown in isolation to allow
visualization of the depths of the sulcus. Sections were saved and studied anterior to the vertical line.
Conventions as for Figs. 1 and 3.
358
(c) Superior temporal gyrus. The rostral half of the superior temporal gyrus
contained only a few labelled cells after the largest injections, which included all of the
basolateral nuclei (nos. 103 and 105) (Fig. 3). In both animals with injections centred
on the lateral nucleus (nos 104 and 182) a few HRP-positive cells were located in the
rostral portion of the superior temporal gyrus which merges with the temporal pole
(TG) (Fig. 4). This label was found in pyramidal cells in layers llI and V.
(d) Temporalpole (TG). Dense aggregations of labelled cells were observed after
injections centred in either the lateral (nos. 104 and 182) or the accessory basal nuclei
(no. 113) (Figs. 4 and 5). In animal 113 almost half of the labelled cells found outside
the amygdala were located in the temporal pole, and in animals 104 and 182 the
proportion was a fifth. In one animal (no. 355) where the injection was centred on the
lateral basal nucleus the labelled cells in TG were very much reduced as compared with
the more lateral and medial injections described above. Very light label was seen after
corticomedial injections, although this may have been due to involvement of the substantia innominata (no. 65) (Fig. 3). In all animals the label was mainly found in the
pyramidal cells of layer III, especially the deeper portions, with smaller numbers
present in layer V.
(e) Entorhinal andperirhinal areas. Few labelled cells were found in the entorhinal cortex after large amygdaloid injections (nos. 103 and 105) (Fig. 3), and even less
label was seen after more restricted lateral injections (nos. 104 and 182) (Fig. 4).
Injections filling the basolateral amygdala (nos. 103 and 105) produced a consistent
pattern of labelled cells along both banks of the rhinal sulcus, but with more restricted
lateral (nos. 104 and 182) and accessory basal nuclei (no. 113) injections this labelling
was reduced to a sparse scattering of cells (Figs. 4 and 5). In one animal (no. 65), with
an injection involving the central and medial nuclei and the area of the substantia
innominata, dense labelling was observed from the rostral rhinal area. Although the
perirhinal label was mainly found in subarea 35a, it was also present in Pr2 and 35b.
This label derived from pyramidal cells in layer V, with a smaller number present in
layer III.
(f) Insula. The anterior two-thirds of the insula was labelled after injections into
the basolateral nuclei. The caudal-third of the insula was only labelled following those
larger amygdaloid injections (nos. 103 and 105) which spread to surrounding
structures (Fig. 3). In animals with more restricted injections the insula and parainsula
were labelled after injections into the lateral (nos. 104 and 182) and lateral basal nuclei
(no. 355) (Fig. 4), while label was only found in the parainsular area following
injections into the accessory basal nuclear area (nos. 113 and 403) (Fig. 5). A few
scattered cells were observed in the insula after injections of the central nucleus and the
substantia innominata (no. 65). The labelled cells were pyramidal cells in layers 1II and
V. Some label was also observed in the contralateral rostral parainsula area in animal
104.
The frontal lobe
The considerations concerning injection size and placement, mentioned in the
preceding section on the temporal cortex, also apply to the frontal lobe. In addition,
359
when considering prefrontal cortex, only the results from the 5 animals without
prefrontal lesions are discussed.
(a) Orbital prefrontal cortex. An injection centred on the lateral nucleus (no.
104) produced labelled cells in area 13, especially in the more posterior portion, the
orbito-insula transition zone and in the orbital and frontomarginal sulci (Fig. 4). Injections into the lateral or accessory basal regions produced small amounts of label in
area 14 (nos. 104 and 403) (Figs. 4 and 5). This orbitofrontal label arose from
pyramidal cells in layers III and V. Many labelled cells were observed from all of area
13 and the caudal part of area 11 after an injection into the medial nucleus and the
adjacent region of the substantia innominata (no. 65) (Fig. 3).
(b) Dorsalprefrontal cortex. Injections into the basolateral nuclei (nos. 104, 355
and 403) (Figs. 4 and 5) failed to show any evidence of a projection from this region to
the amygdala apart from a few cells in sulcus principalis (no. 104). However, a significant quantity of label was found in sulcus principalis and the superior prefrontal
dimple 53, after an injection into the medial nucleus and substantia innominata region
(no. 65) (Fig. 3).
(c) Medialfrontal cortex. No label was observed in areas 10, 25 and 9 apart from
a few cells found in the animal (no. 65) with a medial nucleus and substantia innominata injection. The anterior cingulate, above the genu of the corpus callosum, was
significantly labelled but only after injections into the lateral nucleus (no. 104) (Fig. 4).
This label was restricted to pyramidal cells in layer III. The subcallosal (FL) gyrus,
however, was labelled after both basolateral (nos. 104 and 403) and medial amygdaloid injections (nos. 65 and 231) (Figs. 3, 4 and 5). It is of interest that, even though
animal 113 had a lesion of sulcus principalis, it had the heaviest labelling seen in the
subcallosal gyrus. This was after an injection centred in the accessory basal nucleus.
The injection into the lateral nucleus (no. 104) labelled primarily large pyramidal cells
in layer V. However, only small circular cells in the same layer were labelled after
injections into the accessory basal nucleus (no. 113). As the precise boundary between
areas 24 and 25 is unclear, some label in the most rostral cingulate or subcallosal
cortex may have belonged to posterior 25.
(d) Precentral cortex. The labelled cells found in precentral cortex in animals
103 and 105 almost certainly resulted from spread of H R P into the putamen (Fig. 3). It
is unclear how to interpret the cluster of labelled cells found around the most posterior
extent of the arcuate sulcus (no. 182) (Fig. 4).
Parietal cortex
The brains were blocked in such a way that in only one animal (no. 104) could
the full extent of parietal cortex be examined. No labelled cells were found in this
animal (Fig. 4). But in one of the animals with restricted injections (no. 182) a few cells
were found on either bank in the depths of the intraparietal sulcus (Fig. 4). The
difference between the results for animals 182 and 104 is difficult to explain given the
general similarity between their injections.
Subcortical structures
(a) The amygdala. In some animals the spread of label from the injection site
360
precluded analysis of intra-amygdaloid projections. However, with the more discrete
injections very dense label was present in the lateral portion of the lateral nucleus and
claustral area of the amygdala after an injection into the accessory basal region (nos.
113 and 403). Conversely, the magnocellular part of the accessory basal nucleus was
labelled following injections centred on the lateral nucleus (nos. 104 and 182). Both
animals (nos. 65 and 231) injected in the dorsal amygdaloid region showed a heavy
labelling in the caudal, lateral basal, and magnocellular accessory basal nuclei. These
labelled cells within the amygdala were the most numerous single source of afferents
found in the brains (nos. 113,403, 65 and 231) and it is highly probable that the spread
of HRP from the injection site obscured other intra-amygdaloid connections. The
interpretation of results for the amygdala is further clouded by the possible uptake of
HRP by severed axons which arise from areas of the amygdala other than the injection
site.
(b) Substantia innominata (SI). Every animal examined had labelled cells in the
SI area, which were very numerous in some cases. The SI was the major source of subcortical label in several animals (nos. 104, 182, 231 and 355). The greatest densities of
cells appeared after injections into the lateral basal nucleus (no. 355). In animals with
injections in the central or medial nucleus (nos. 65 and 231) the possibility that labelled
cells resulted from the passive spread of HRP from the injection site could not be
excluded. The horizontal limb of the diagonal band of Broca showed a similar, if less
dense, pattern of label. Only a few cells were observed in the vertical limb and no
labelled cells were found in the septal areas. No evidence of a topographic projection
to the amygdala was found.
(c) Hypothalamus. The hypothalamic area contained only a few scattered
labelled cells and there was no evidence that any of these groups of cells was associated
with any particular nuclear division of the amygdala. In animals with corticomedial
involvement (nos. 113, 231 and 65) the hypothalamic labelling appeared to be heavier
than with injections elsewhere and labelled cells could be found in the lateral, ventromedial, and dorsomedial hypothalamic nuclei.
(d) Basal ganglia. In all of the animals cells were occasionally found in the
caudate and globus pallidus. Only in the putamen was it possible to find evidence of a
dense labelling, and this was in the two animals with extensive injections (nos. 103 and
105) which spread beyond the amygdala. This suggests that the label in the putamen
was not derived from the amygdala. The claustrum was usually lightly labelled, independently of the injection site, though injections into the lateral basal (no. 355) or
accessory basal nuclei (no. 113) resulted in the greatest amount of label, especially in
the ventral claustrum lateral to the amygdala.
(e) Thalamus (nuclei after Olszewski41). Thalamic label was found almost exclusively in non-specific nuclei with the exception of the magnocellular part of the ventral
anterior (VAmc) nucleus which was labelled after the injections centred on the lateral,
and possibly the lateral basal nuclei. The majority of the remaining labelled cells were
found in the following midline and intralaminar thalamic nuclei: nucleus paraventricularis (Pa, Pac), nucleus centralis latocellutaris (Clc), nucleus centralis densocellularis
(Cdc), nucleus centralis superior (Cs), nucleus centralis inferior (Cif), nucleus centralis
361
intermedialis (Cim), nucleus rotundis (Ro), nucleus reuniens (Re), nucleus paracentralis (Pcn), nucleus subfascicularis (Sf.pc and Sf.mc) and nucleus centrum medianum
(Cn.Md). All these nuclei appeared to be labelled after amygdaloid injections and no
evidence of specific topographic injections was observed. The lateral (nos. 104 and
182) and lateral basal (no. 355) nuclei injections, for example, produced label in all of
these thalamic nuclei, the lateral basal nucleus producing the greatest number.
Injections into the accessory basal area (nos. 113 and 403), however, only resulted in
labelled cells in the nucleus paraventricularis (Pa). Very light label was present in
nucleus medianum (Cn.Md) and the habenula following injections centred in the
lateral nuclei (nos. 104 and 182). This is consistent with the similar but denser label
seen in these same nuclei in those animals with the largest injections (nos. 103 and
105). The medial pulvinar was lightly labelled after injections centred on the lateral
nuclei (nos. 104 and 182). None of the other thalamic nuclei, including the dorsomedial nucleus, were labelled.
The midbrain, caudal diencephalon and brain stem afferents
(a) The substantia nigra and peripeduncular nuclei. A few labelled cells were
observed in the substantia nigra after injections to the dorsal amygdala and substantia
innominata region (nos. 231 and 65). A few cells were also observable after lateral
nucleus injections but the problems of endogenous B1 label make interpretation difficult. The majority of animals revealed a narrow band of spindle-shaped labelled cells
running rostrally and diagonally just beneath the thalamus, between the peripeduncular nucleus and the nucleus subfascicularis parvocellularis. The labelled cells,
which were quite numerous, occurred after injections into the basolateral nuclei and
especially the lateral basal nucleus (no. 355). Labelled cells were occasionally found in
the tegmental area stretching ventromedially from the peripeduncular nucleus and
merging caudally with the nucleus reticularis tegmenti.
(b) Central gray. The midbrain was studied up to the caudal extent of the
periaqueductal central gray. The position of midbrain label was compared with the
stereotaxic atlas of Snider and Lee 50; thus the nomenclature is taken from their study.
All the animals examined showed a consistent but sparse scattering of labelled cells
within the midbrain. This occurred in an area of large cells, nucleus medialis annuli
aqueductus, ventromedial to the third ventricle in the central gray, and from a group
of smaller cells which course ventrally around the boundary of the trochlear nucleus
and interdigitate with the fibres of the fascicularis longitudinalis medialis and spread
laterally around the ventral margin of the fibre bundle. It was also possible to find
labelled cells bilaterally, running more caudally along the margin of the mesencephalic
trigeminal nucleus, but these appeared to derive from endogenous label 61. Midbrain
label was seen in all animals, but those with injections into the accessory basal nucleus
(nos. 113 and 403) produced label only in the more ventral central gray.
DISCUSSION
The demonstration of labelled cells does not necessarily prove a projection to the
362
amygdala. HRP may be picked up and transported by damaged axons ,59, and thus
great care is needed when interpreting results obtained by applying HRP to subcortical
nuclei. Fibres from the piriform cortex are known to traverse the amygdala of the rat 8,
although the routes of such connections in the primate are not known in detail.
However, Van Hoesen and Pandya 5z have shown that fibres from the anterior piriform
cortex pass medial to the basolateral nuclei. We do not think it likely that these fibres
were extensively damaged in this study, and take as direct evidence the very low
density of labelled cells found in the piriform cortex.
It is more difficult to determine the precise zones of active HRP uptake and so
dismiss the possibility of uptake by structures outside the amygdala. Evidence
concerning this point has been discussed in the 'Analysis' section. It is likely that in
animals 103 and 105 there was significant extra-amygdaloid involvement, and that this
is reflected in the more widespread pattern of labelling. Furthermore, the apparent
projections from sulcus principalis and the rhinal fissure in animal 65 point to some
uptake of HRP from an area outside the amygdala, probably the substantia innominata. However, in general the projections suggested by this study are consistent with
the findings of investigations using anterograde methodslS,lS,19,21, 4°. The anatomical
literature also provides information on the areas which project to structures adjacent
to the amygdata. Where we failed to find labelled cells in these areas we have supposed
that there was no significant uptake of HRP by these neighbouring structures.
We cannot make strong claims on the pattern of projections to specific amygdaloid nuclei. The injections of HRP were not sufficiently discrete and they might have
involved fibres passing to adjacent nuclei within the amygdala. This problem has been
discussed in the 'Analysis' section. We are reassured, however, by the similarity of the
results reported here for the temporal lobe, and those reported by Herzog and Van
Hoesen 15 using silver degeneration and autoradiography.
Two generalizations are suggested by this study. The first is that the amygdala is
closely connected with areas thought to be involved in the regulation of emotion and
motivation. The second is that the projections from association cortex are most dense
from the temporal lobe, and particularly so from the superior temporal sulcus (Fig. 6).
The caudal orbital frontal cortex, temporal pole, anterior insula and the anterior
cingulate and subcallosal gyri, all contain HRP-positive cells following injections into
the amygdala. These results confirm earlier neuronographic studies 44,45. This label was
most dense after injections involving the basolateral amygdala, in particular the lateral
or accessory basal nuclei areas. In all of these areas the cortex is dysgranular or
agranular a4. These cortical regions all appear to play some role in autonomic modulation. Thus Kaada 22 showed that in anaesthetized rhesus monkeys stimulation in any
of these agranular areas could result in inhibition of respiration, pyloric contraction,
changes in brood pressure and dilation of the pupils. Similar changes could not be
found after stimulation of other cortical areas. The effects of amygdala stimulation
seen in this and other studies were grossly similar to those of stimulating agranular
cortex, suggesting a functional relationship.
Other regions of consistent label were the substantia innominata and the hypothalamus. The hypothalamic label appeared relatively sparse in this study, although
363
evidence of a larger projection has been found in the rat s,a2 and squirrel monkey 19
using different techniques. The hypothalamus has traditionally been ascribed a central
role in controlling emotion and motivation, and recent recording studies3, 3s have
shown that the substantia innominata, like the lateral hypothalamus, has neurons
which specifically respond to the motivational properties of stimuli. The much denser
label in the substantia innominata may indicate that in the rhesus monkey this area
may be a more important final link in modulating the activity of the amygdala. Neither
the hypothalamus nor the substantia innominata appear to project solely to specific
amygdala nuclei, although label in the hypothalamus was more frequent after medial
or dorsal amygdala injections.
Evidence was found of a connection from the periaqueductal central gray area of
the midbrain to the amygdala. The results indicate a sparse but consistent projection
to most of the amygdaloid nuclei. The central gray is thought to receive information
related to pain24, 34. It is therefore of interest that the amygdala has been associated
with responses to pain1,13, 5s and this projection may be important in mediating these
effects. Furthermore, the highest concentrations of opiate receptors in the rhesus
monkey brain 80 are in the amygdala and periaqueductal central gray.
The thalamic afferents to the amygdala indicated by this study were confined to
the non-specific nuclei and the magnocellular part of nucleus ventralis anterior
(VAmc), which is often regarded as a non-specific nucleus. It is unlikely that this label
was caused by the uptake of HRP outside the amygdala, as every animal showed some
degree of thalamic labelling. These areas are thought to be rostral extensions of the
reticular formation and their activity is believed to be associated with arousal and
pain 1°,24,3s. Like the amygdala and periaqueductal gray the medial thalamus is rich in
opiate receptors 30.
We were unable to find any evidence of a projection from the dorsomedial
nucleus (DMN) to the amygdala as described by Nauta 4°. Our failure to find this
projection agrees with a previous report 37. It is possible that this pathway is insensitive
to the HRP technique 49, but when Nauta lesioned the D M N and demonstrated
degeneration in the amygdala he also damaged the non-specific midline nuclei lying
medial to the DMN. In our study these nuclei appear to project to the amygdala, and
so Nauta's finding could derive from damage to these midline structures, and not to
the DMN. The pattern of amygdaloid degeneration he reports agrees with the sites of
termination of midline thalamic afferents as demonstrated by HRP in the present
study. The existence of an apparent amygdaloid projection from an area stretching
from the peripeduncular nucleus rostrally and medially to the nucleus subfascicularis
agrees with a previous brief report 37. The importance of this connection is as yet
unknown.
There is a close anatomical association between the agranular cortical areas, in
particular the orbital frontal cortex, temporal pole and the amygdala. Experiments
studying the effects of lesioning these 3 areas suggest that they are all crucial in
maintaining appropriate social responses 27. Furthermore, some aspects of the KliiverBucy syndrome occur after removal of any of these structures 4,16,27,5s and the effect is
greater if more than one of these areas is damaged27, 48. The syndrome es,Ss consists of:
364
(l) abnormal tameness and approach behaviour; (2) 'visual agnosia'; (3) dietary
changes including meat eating and coprophagia; (4) orality; (5) hypermetamorphosis,
or the abnormally rapid switching of attention between stimuli: and (6) hypersexuality. It has been proposed that these areas may represent part of a neural system
essential for normal social behaviour 27. The anatomical results reported here support
the view that these structures may be part of a functional system. The orbital frontal
cortex and temporal pole both appear to project directly to the amygdala, especially to
the lateral and accessory basal nuclei. These connections appear to be reciprocal 39 as
are those between the temporal pole and the orbital frontal cortex21, 42. There is
evidence of an important indirect pathway from the amygdala to the orbital frontal
cortex via the magnocellular part of DMNaa, 40 and it has been supposed that this was
reciprocal 4°. Our results indicate that if there is an indirect thalamic route from the
orbital frontal cortex to the amygdala, it is via VAmc and the midline nuclei33, 39 and
not the DMN.
In view of the anatomical and functional interconnections of the orbitofrontal
cortex, temporal pole and amygdala, it is of interest whether they share similar
afferents. The rostral inferotemporal and rostral superior temporal gyri both project to
the amygdala, temporal pole ~1 and orbital frontal cortex 6. Whilst the amygdala and
orbitofrontal cortex share other similar projections such as midline thalamic
nuclei 2°,26, VAmc 5,47 and substantia innominata25, the afferents to the temporal pole
have not been studied in sufficient detail to enable a comparison to be made.
The second main finding of this study was that the temporal lobe projects more
densely to the amygdala than do other association areas. There have been several
previous studies of temporal association cortex projections to the amygdala 15,21,59.
With the use of HRP we have been able to confirm these connections and accurately
delineate their sites of origin. Thus both anterior inferotemporal and anterior superior
temporal gyri project to the amygdala, both apparently to the lateral nucleus. This site
of termination agrees with previous studies, though we have been unable to show
inferotemporal afferents to the more dorsal portions of the amygdala 15.
The extensive label in the superior temporal sulcus suggests a projection which
has not been previously described. It is of particular interest due to its size and extent.
Both superior and inferior banks and the fundus of the sulcus were heavily labelled
after injections into the lateral nuclear area (animals 104 and 182) (Fig. 6). There is no
evidence that particular portions of the sulcus contribute to this projection, which
extends to the level of the caudal limit of the sylvian fissure. There also appears to be a
lighter contralateral projection, of similar extent, restricted to the lateral nucleus
(animals 104, 182). This contralateral projection may comprise part of the anterior
commissural projection which terminates in the lateral nucleus of the amygdala51. This
sulcus supplies approximately one-fifth of all the label found in animals 104 and 182,
making it numerically one of the most important projections to the lateral nucleus.
Studies of the connections of primary sensory areas (somesthetic, visual and auditory)
have shown that the superior temporal sulcus is one of the first areas of convergence of
these respective association areas21, 48. Electrophysiological recording studies have
confirmed the existence of polysensory cells in the rostral-half of the superior temporal
365
sulcus 2, although more detailed anatomical work 4s has indicated that the different
association areas mainly project to different sites within the sulcus. That much of this
sulcus projects to one amygdala area suggests a further degree of convergence, which is
borne out by the finding of polysensory units within the amygdalaZL Machne and
Segundo 35, recording from cells in the amygdala of anaesthetized cats, remark that
'the convergence of different sensory modalities upon single units was outstanding'.
Most of the polysensory units they located were in the basolateral nuclei. Thus the
superior temporal sulcus could be the main source of polysensory information to the
amygdala.
The existence of direct projections to the amygdala from visual (inferotemporal)
and auditory (superior temporal) association areas suggests that the other cortical
association areas may project directly to this structure. However, afferents were not
conclusively demonstrated from somatosensory area II or parietal association cortex.
A small group of labelled cells was found in the depths of the intraparietal sulcus in
one animal (182) but not in others. Because of the levels at which the brains were
blocked the full posterior extent of parietal cortex was only studied in one animal (no.
104). The lateral frontal cortex was only occasionally labelled in those 5 animals with
intact frontal lobes.
Injections to more dorsal and medial nuclei suggest dense intraamygdaloid
connections. These findings parallel some of those of Krettek and Price 29 in the rat.
The role of these intra-amygdaloid projections is unknown but they are clearly of great
importance when considering functional subdivisions within this structure 23. These
connections were more numerous than those found from any other one area in nos.
113,403, 231 and 65, and since the spread of HRP around the injection site may have
obscured other intra-amygdaloid projections our results probably underestimate the
size and extent of these connections. The density of these projections shows that the
normal functioning of a particular nucleus may be partly dependent on the integrity of
another nucleus with which it is interconnected. This consideration should be borne in
mind when interpreting the effects of selective amygdaloid lesions.
These anatomical results suggest that two types of information converge in the
amygdala: external polysensory information, via temporal lobe association cortex;
and internal motivational and visceral information from various regions including the
substantia innominata, the hypothalamus and the dysgranular cortical areas. Our
findings are compatible with the proposal that the amygdala plays a role in integrating
information about the sensory aspects of stimuli and their motivational and emotional
significance17. It is true that Sanghera et al. a6 were unable to find cells in the amygdala
which modified their firing according to changes in the motivational significance of
objects with which the monkeys were presented. But the proposal is more directly
tested by analyzing the varied effects of amygdala lesions on behaviour: and for these
effects it still provides the most parsimonious explanation.
366
ACKNOWLEDGEMENTS
T h i s r e s e a r c h was s u p p o r t e d by M . R . C . G r a n t 971/1/397/B.
W e are g r a t e f u l to Dr. V. H. Perry f o r helpful c o m m e n t s on the m a n u s c r i p t , and
to I v o r H u g h e s a n d M a r y W a l k e r f o r the h i s t o l o g i c a l p r o c e s s i n g o f the brains.
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