Full text of DOI:10.1007/PL00008229

Anat Embryol (2000) 201:75–84
© Springer-Verlag 2000
O R I G I N A L A RT I C L E
Fiona Reardon · John Mitrofanis
Organisation of the amygdalo-thalamic pathways in rats
Accepted: 30 June 1999
Abstract This study examines the organisation of the
pathways from the amygdala to the thalamus. Amygda-
Introduction
loid nuclei (medial, central, basolateral and olfactory We have been interested in the general organisation of
groups) of Sprague-Dawley rats were injected with bio- subcortical afferents that reach the dorsal thalamus,
tinylated dextran using stereotaxic coordinates and their having described already those that arise from the ven-
brains were then aldehyde-fixed and processed using tral thalamus – thalamic reticular nucleus (Coleman
standard methods. We have three major findings. First, and Mitrofanis 1996; Kolmac and Mitrofanis 1997) and
the amygdala has a distinct set of projections to particu- the zona incerta (Power et al. 1999) - and from many
lar nuclei of the thalamus. The thalamic nuclei with the nuclei of the brainstem (Kolmac and Mitrofanis 1998;
heaviest amygdaloid terminations include the zona in- Kolmac et al. 1998). In this study, we describe the or-
certa, the mediodorsal and the midline nuclei. Second, ganisation of afferents from the amygdala, a major sub-
nuclei of different amygdaloid groups project to the thal- cortical centre of the forebrain thought to be responsi-
amus in slightly different patterns. For example, some ble for generating the appropriate emotional reaction in
groups of nuclei project to the thalamic reticular nucleus response to a given sensory stimulus (Turner and
(
e.g. medial, olfactory) whilst others do not (e.g. central, Herkenham 1991).
basolateral). Thus, there is a certain amount of heteroge-
The dorsal thalamus has been described as the “gate-
neity within the amygdaloid projections to the thalamus. way” to the neocortex, since most inputs that reach the
Third, when we compare our results on the amygdalo- neocortex from the sensory periphery (e.g., retina, co-
thalamic pathways to the many previous descriptions of chlea, skin) or from other brain parts (e.g., brainstem,
the thalamo-amygdaloid pathways, we note that they are cerebellum) do so after passing through the dorsal thala-
largely out of register. In other words, some of the tha- mus. The dorsal thalamus is made up of distinct nuclei
lamic nuclei that project to a given group of amygdaloid that can be grouped into either first-order, higher-order
nuclei do not necessarily receive a projection back from or intralaminar/midline nuclei. First-order nuclei receive
that same amygdaloid nucleus. Hence, there is no sub- much of their “primary drive” from usually one periph-
strate for a strong feed-back relationship between the eral or subcortical source (e.g., dorsal lateral geniculate
thalamus and the amygdala, as there has been shown for and ventral lateral nuclei) and project to one or two cor-
other centres of the brain (e.g. between the thalamus and tical areas; higher-order nuclei, for the most part, re-
neocortex).
ceive their primary drive from particular cortical areas
layer V cells) and then project back to these cortical
(
Key words Rat · Biotinylated dextran ·
Dorsal thalamus · Amygdala
(e.g., posterior thalamic and lateral posterior nuclei) and
the intralaminar/midline nuclei are generally driven by
many sources including the cerebellum, spinal cord,
basal ganglia and brainstem and project to more wide-
spread areas of cortex (e.g., paraventricular, rhomboid,
parafascicular and central-lateral nuclei; see Jones 1985;
Guillery 1995; Sherman and Guillery 1996; Steriade et
al. 1997).
The amygdala, as with the dorsal thalamus, can be di-
vided up into distinct functional groups of nuclei also. In
general, four groups are recognised – central, medial, ba-
solateral, olfactory – with each having largely distinct
F. Reardon · J. Mitrofanis (
Institute for Biomedical Research,
Department of Anatomy and Histology, University of Sydney,
)
✉
2
006 Australia
e-mail: zorba@anatomy.usyd.edu.au
Tel.: +61-2-93512838, Fax: +61-2-93516556

7
6
patterns of connections (de Olmos et al. 1985). For ex- dehyde. After removal of the brains, they were post-fixed in the
same fixative for 1 h, and immersed in PBS with the addition of
ample, the central nucleus has rich interconnections with
many of the distinct nuclei of the brainstem (Hopkins
2
0% sucrose until the block sank. The brains were then cut using a
freezing microtome into coronal sections at a thickness of 50 µm
and stored in PBS. In general, every second section was processed
1
1
975; Kretteck and Price 1978; Otterson 1981; Davis
992; Fallon and Ciofi 1992; Jia et al. 1992), the medial for dextran detection. Sections were washed in PBS with the addi-
tion of 0.5% Triton (Sigma, Mo., USA) for 1 h and then incubated
nucleus interconnects with the olfactory bulb, hypothala-
mus and preoptic area (Kretteck and Price 1978; Veening
in the avidin-biotin-peroxidase complex (1:120; Sigma, Mo.,
USA) for 4 h at room temperature. Next, sections were reacted in
a nickel-TRIS buffered saline (NTBS) - 3,3’-diaminobenzidine te-
1
978; Kevetter and Winans 1981; Luiten et al. 1983;
Wong et al. 1993), the olfactory nuclei have connections trahydrochloride (DAB; Sigma, Mo., USA) solution (Clemence
and Mitrofanis 1992). Sections were then mounted onto gelatini-
with olfactory bulb, cerebral cortex, hypothalamus (de
Olmos 1972; Scalia and Winans 1975; Kretteck and
Price 1977 1978), and the basolateral complex connects
heavily with the cortex (Kretteck and Price 1977;
Sripanidkulchai et al. 1984), hypothalamus (Petrovich et
sed slides, air-dried overnight, counterstained with neutral red, de-
hydrated in ascending alcohols, cleared in Histoclear, and cover-
slipped using DPX.
Analysis
al. 1996) and basal forebrain (Kretteck and Price 1977).
In addition to these connections, each of these amygda-
loid nuclei, particularly the medial, olfactory and baso-
lateral groups, have been shown to project to the dorsal sites and the anterogradely labelled terminals were plotted with
thalamus (Kretteck and Price 1977; 1978; Nitecka et al.
Coronal sections were drawn with reference to the atlases of Paxi-
nos and Watson (1986) and/or Swanson (1992) and the injection
the use of a camera lucida. Drawings and plots were then scanned
onto a computer graphics program and the schematic diagrams
1
979; Ottersen and Ben-Ari 1979; Turner and Herken-
shown in Figs. 3–6 were constructed.
ham 1991). The organisation of an amygdaloid projec-
tion back to the thalamus, however, has received little if
any attention previously.
Results
The major aim of this study was to explore the pat-
terns of projections from the amygdala to the thalamus in
rats. In general, the basic questions posed here are: (1)
which thalamic nuclei receive a heavy input from the
amygdala? (2) which amygdaloid nuclei form these pro-
jections to the thalamus? and (3) are these amygdalo-
thalamic projections in register with the previously de-
scribed thalamo-amygdaloid projections? Overall, the re-
sults generated should provide insights into whether the
amygdala is in a strong position to influence the activity
of different thalamo-cortical pathways through its con-
nections with the dorsal thalamus.
Injection site and tracer
In this study, biotinylated dextran was used as antero-
grade tracer for several reasons. It provides discrete in-
jection sites with little spread from the focal point (see
Fig. 1). Further, dextran has not been reported to be
transported trans-synaptically or to be taken up by intact
Abbreviations for figures ACo Anterior amygdaloid nucleus ·
AN anterior thalamic nucleus · AHIA Amygdaloid hippocampal
transitional area · BLA basolateral amygdaloid nucleus ·
BLP basolateral posterior amygdaloid nucleus · BMA basomedial
anterior amygdaloid nucleus · BMP basomedial posterior
amygdaloid nucleus · CeA central amygdaloid nucleus · CL central
lateral nucleus · CM central medial nucleus · cp cerebral peduncle ·
CPu caudate-putamen complex · cZI caudal sector zona incerta ·
DAB 3,3, diaminobenzidine tetrahydrochloride · dLGN dorsal
Materials and methods
Subjects
Sprague-Dawley rats of either sex were used (250–300 g; n=33). lateral geniculate nucleus · dMGN dorsal division medial
Prior to use, they were kept in a 12 h light/dark cycle and had ac- geniculate nucleus · dZI dorsal sector zona incerta · fr fasciculus
cess to food and drink ad libitum. All of the following experimen- retroflexus · G gustatory thalamic nucleus · GP globus pallidus ·
tal procedures were approved by the Animal Ethics Committee of Hb Habenula · IAM interoanteriormedial thalamic nucleus ·
the University of Sydney.
ic internal capsule · LD laterodorsal thalamic nucleus · LP lateral
posterior nucleus · MD mediodorsal thalamic nucleus ·
MeA medial amygdaloid nucleus · ml medial lemniscus ·
mt mammillothalamic tract · NTBS nickel tris base saline ·
ot optic tract · PBS phosphate-buffered saline · Pc paracentral
Tracer injections
Rats were anaesthetised after an intraperitoneal injection of ket- thalamic nucleus · pc posterior commissure · Pir Piriform area·
amine (100 mg/kg) and Rompun (10 mg/kg). Biotinylated dextran Pf parafascicular nucleus · PMCo posterior medial cortical
[
10 kDa; 10% in phosphate-buffered saline (PBS); Molecular amygdaloid nucleus · Po posterior thalamic nucleus ·
Probes, Ore., USA)] was injected, via iontophoresis (10–15 µA for Pt parataenial thalamic nucleus · Pv paraventricular thalamic
0 min; 6 s on, 6 s off), into the following nuclei using stereotaxic nucleus · R thalamic reticular nucleus · Re reuniens thalamic
2
coordinates (Paxinos and Watson 1986): central amygdaloid nu- nucleus · Rh rhomboid thalamic nucleus · rZI rostral sector zona
cleus (n=7), medial amygdaloid nucleus (n=8), anterior cortical incerta · scp superior cerebellar peduncle · sm stria medullaris ·
nucleus (n=5), amygdalo-hippocampal transition area (n=2), baso- Spf subparafascicular thalamic nucleus · STN subthalamic nucleus ·
lateral amygdaloid nucleus (n=7) and the basomedial amygdaloid VL ventrolateral thalamic nucleus · vLGN ventral lateral
nucleus (n=4). After surgery, the rats were allowed to recover for geniculate nucleus · VM ventromedial thalamic nucleus · vMGN
7
days and were then anaesthetised deeply with Nembutal (sodium ventral division medial geniculate nucleus · VPL ventral posterior
pentobarbitone: 60 mg/ml). The animals were perfused trans-car- lateral nucleus · VPM ventral posterior medial nucleus ·
dially with PBS (0.1 M; pH 7.4), followed by 4% buffered formal- vZI ventral sector zona incerta

7
7
Fig. 1 A, B Examples of bio-
tinylated dextran injection sites
into the amygdala of the rat.
In these cases (injections into
BMA), as in all the others con-
sidered in this study, the injec-
tion site was discrete and limit-
ed to the targeted nucleus. Ar-
rows indicate the focal point of
the injection site within the
BMA (two injections into the
same nucleus are shown for
comparison). Both A and B are
of coronal sections; dorsal to
top, and lateral to left. Sections
were counterstained with neu-
tral red. Bar 1 mm
and/or damaged axons of passage (Rajakumar et al. Organisation of the amygdalo-thalamic pathways
1
993; Coleman and Mitrofanis 1996; Kolmac and
Mitrofanis 1997). Finally, this tracer yields strong and The morphology of the labelled terminals in the thala-
consistent terminal-like labelling in the thalamus after mus after dextran injections into the different amygda-
amygdaloid injections (Fig. 2).
loid nuclei appeared very similar in all cases (Fig. 2).
For example, the labelled terminals seen in the zona in-
certa (Fig. 2A,B) were very similar in morphology and
organisation to those seen in the mediodorsal thalamic
nucleus (Fig. 2C,D). The labelled terminals were in the
General
The amygdaloid complex is made up of four major form of fine fibres with small swellings or boutons (ar-
groups of nuclei (see de Olmos et al. 1985). These are rows, Fig. 2). Although the morphology of labelled ter-
the central, medial, basolateral and olfactory nuclei. The minals was similar in the different thalamic nuclei, the
medial and central groups are each made up of a single distribution of these terminals across the thalamus was
nucleus, and these were injected with dextran. The baso- rather different.
lateral and olfactory groups, on the other hand, are each
made up of four and three nuclei respectively; in these
cases, two nuclei of each group were injected. We Central amygdaloid nucleus
thought that this series of injections would provide a
worthwhile portrait of the organisation of the amygdalo- Figure 3 shows a series of schematic diagrams depicting
thalamic pathways. Results from the different injections the pattern of anterograde labelling seen in the thalamus
into the same amygdaloid nuclei were very similar.
after a dextran injection into the central nucleus. After

7
8
Fig. 2 A–D Examples of anterogradely labelled terminals in the
thalamus after injections of biotinylated dextran into the rat amyg-
dala. A, B Show labelled terminals seen in the rostral sector of the
zona incerta (rZI) after an injection into the central nucleus of the
Medial amygdaloid nucleus
The pattern of anterograde labelling resulting from an in-
amygdala. C, D Show labelled terminals in the mediodorsal tha- jection of dextran into the medial nucleus is shown in
lamic nucleus (MD) after an injection into the amygdalo-hippo- Fig. 4. Other dextran injections into medial nucleus re-
campal transition area. Note that the morphology of the labelled
vealed similar patterns. Zones of rich anterograde label-
terminals in each nucleus after both injections was very similar.
ling were seen in the medial lip of the rostral reticular
Arrows point to small labelled boutons. Bar 50 µm
nucleus, the rostral sector of the zona incerta, the ventro-
medial nucleus, the central-medial/paracentral nucleus
this injection, as with others into the central nucleus, an- and subparafascicular nucleus of the intralaminar group
terogradely labelled terminals were distributed in a num- and in small isolated patches of the posterior thalamic
ber of thalamic nuclei. These terminals appeared in nucleus. A few labelled terminals were also seen in the
small, distinct regions in the medial part of the medio- nucleus reuniens of the midline group and in the dorsal
dorsal nucleus, rostral sector of the zona incerta and the and caudal sectors of the zona incerta.
paraventricular nucleus of the midline group. Fewer la-
belled fibres were seen in the rhomboid nucleus of the
midline group, the ventral sector of the zona incerta and Olfactory amygdala
in the ventral regions of the gustatory nucleus (Fig. 3).
The olfactory amygdala injected in this study were the
anterior cortical nucleus and the amygdalo-hippocampal
transition area. Labelling patterns in the thalamus after
injections into each of these nuclei were very similar

7
9
Fig. 3 Schematic diagrams of the distribution of anterogradely la- Fig. 4 Schematic diagrams of the distribution of anterogradely la-
belled terminals in the rat thalamus after an injection of biotinyla- belled terminals in the rat thalamus after an injection of biotinyla-
ted dextran into the central nucleus of the amygdala (injection site ted dextran into the medial nucleus of the amygdala (injection site
shown). Labelled axons in the thalamus with boutons were drawn; shown). Labelled axons in the thalamus with boutons were drawn;
labelled axons of passage (thicker and with no boutons) were not labelled axons of passage (thicker and with no boutons) were not
drawn. Sections were approximately 200 µm apart. Nuclear bor- drawn. Sections were approximately 200 µm apart. Nuclear bor-
ders were determined after Nissl counterstaining
ders were determined after Nissl counterstaining

8
0
Fig. 5 Schematic diagrams of the distribution of anterogradely la- tion sites shown). Labelled axons in the thalamus with boutons
belled terminals in the rat thalamus after injections of biotinylated were drawn; labelled axons of passage (thicker and with no bou-
dextran into the anterior cortical (A) and the amygdalo-hippocam- tons) were not drawn. Sections were approximately 200 µm apart.
pal transitional area (B) nuclei of the olfactory amygdala (injec- Nuclear borders were determined after Nissl counterstaining

8
1
Fig. 6 Schematic diagrams of the distribution of anterogradely la- the thalamus with boutons were drawn; labelled axons of passage
belled terminals in the rat thalamus after injections of biotinylated (thicker and with no boutons) were not drawn. Sections were ap-
dextran into the basolateral (A) and the basomedial (B) nuclei of proximately 200 µm apart. Nuclear borders were determined after
the basolateral complex (injection sites shown). Labelled axons in Nissl counterstaining

8
2
(
Fig. 5A,B). In general, many labelled terminals were pathways and therefore particular functional areas of
seen in the medial regions of the mediodorsal nucleus neocortex.
and in various nuclei of the midline group, including the
This relationship that the thalamus shares with the
paraventricular, parataenial, rhomboid and reuniens nu- amygdala is very similar to the one that it shares with the
clei. Labelled terminals were also seen in the medial lip basal forebrain and with the brainstem, at least in terms
of the rostral reticular nucleus, the parafascicular and of patterns of connections. Both the basal forebrain and
subparafascicular nuclei of the intralaminar group and in brainstem, for example, appear to target particular tha-
the ventral division of the medial geniculate nucleus. lamic nuclei with their projections. For instance, differ-
Other regions of the thalamus were usually devoid of la- ent centres of the basal forebrain (e.g. nucleus of the di-
belled terminals.
agonal band, substantia innominata, nucleus basalis)
have restricted terminations within the midline (e.g.
parataenial, rhomboid), intralaminar (e.g. central-lateral,
paracentral), zona incerta, reticular, gustatory and medio-
dorsal nuclei (see Kolmac and Mitrofanis 1999), whilst
Basolateral complex
In this study, we made injections into the basolateral and different brainstem nuclei target the zona incerta, reticu-
basomedial nuclei of the basolateral complex (Fig. 6). lar, lateral posterior, intralaminar (e.g. parafascicular,
After injections into each of these nuclei, many labelled central-lateral) and midline (e.g. reuniens, intermedialan-
terminals were found in the medial regions of the medio- terior) nuclei for innervation (see Kolmac and Mitrofanis
dorsal nucleus; a few labelled terminals were seen within 1998; Kolmac et al. 1998). For the most part, these tha-
various midline (e.g. paraventricular, rhomboid and in- lamic nuclei are the same as those targeted by the amyg-
teranteromedial) and intralaminar (e.g. parafascicular, dala. Thus, the reticular nucleus, midline, intralaminar,
subparafascicular) nuclei (Fig. 6). In addition, the baso- zona incerta and mediodorsal nuclei can be viewed as
lateral injections yielded many labelled terminals within thalamic nuclei transmitting functionally diverse subcor-
the rostral sector of the zona incerta (Fig. 6).
tical information to the neocortex. The first-order (ex-
cept for medial geniculate nucleus) and higher-order (ex-
cept for the mediodorsal and posterior thalamic nuclei)
nuclei are largely devoid of these subcortical projections.
Discussion
This study has three major findings:
Distinct amygdaloid groups have different patterns
of projections with the greater thalamus
1
2
3
. The amygdala sends a well-defined projection to dis-
tinct nuclei of the greater thalamus.
. There are some differences in the projections patterns
of the different amygdaloid nuclei to the thalamus.
. When comparing our results on the amygdalo-thalam-
ic pathway to the many previous descriptions of the
thalamo-amygdaloid pathways, we note that they are,
for the most part, not in register with one another.
Our results indicate that there are some distinct differ-
ences in the patterns of projections to the thalamus from
the different amygdaloid groups. For instance, no tha-
lamic nucleus receives a projection from all amygdaloid
groups, although some receive a projection from most
(
e.g. mediodorsal, midline, zona incerta), whilst other
Each of these findings will be discussed separately below. thalamic nuclei receive a projection from only one or
two (e.g. posterior thalamic, reticular). This finding
would suggest that even among the amygdaloid groups
Organisation of a well-defined amygdalo-thalamic
pathway
projecting to the thalamus, there appears to be some het-
erogeneity. Although the patterns of projection from nu-
clei of different amygdaloid groups are different, the pat-
The present study shows that, rather than “blanket” all of terns of projection from nuclei within the same groups
the thalamus with terminations, the amygdala is very are very similar; that is, the basolateral and basomedial
particular regarding its terminations within the thalamus nuclei of the basolateral group had similar projections as
(
see also McDonald 1985; Russchen et al. 1987; Kretteck do the anterior cortical and the amygdalo-hippocampal
and Price 1977). In essence, the amygdala has a discrete transition area of the olfactory group. This would sug-
and precise set of projections to distinct nuclei of the gest that nuclei within the same functional group of
thalamus, a feature that was not clear from previous amygdaloid nuclei may impart a similar influence on the
studies since none had focussed specifically on the activity of the thalamus.
amygdalo-thalamic pathway. We show that the thalamic
nuclei with the heaviest amygdaloid projections include
the mediodorsal nucleus, various midline nuclei (eg, Comparison between the amygdalo-thalamic and
paraventricular, parataenial) and the zona incerta (rostral thalamo-amygdaloid pathways: are they out of register?
sector). Thus, rather than have a very global effect on
thalamic, and hence cortical activity, the amygdala may Many previous studies have documented the organisa-
be in a position to influence particular thalamo-cortical tion of the thalamo-amygdaloid pathway and it would be

8
3
Table 1 Organisation of the thalamo-amygdaloid pathways in rats ceive a projection back from the zona incerta only (see
[
(
(
thalamo-amygdaloid results taken from Kretteck and Price
1978), Veening (1978) Otterson and Ben-Ari (1979), Nitecka et al
1979), Le Doux et al (1988), Turner and Herkenham (1991);
Kolmac and Mitrofanis 1997; Kolmac et al. 1998). Thus,
on the one hand, some centres have strong reciprocal con-
nections with the thalamus (e.g., neocortex), whilst other
centres have weak reciprocal connections (e.g., brain-
stem). The amygdala’s relationship with the thalamus ap-
pears to lie somewhere in between these two extremes,
although leaning more towards weak reciprocity.
amygdalo-thalamic (reciprocal) results taken from the present
study]
Amygdaloid nucleus
Central
Thalamic origins
Reciprocal?
Ventroposterior
Medial geniculate
Midline
–
–
√
–
Intralaminar
Conclusions
Medial
Medial geniculate
Mediodorsal
Midline
–
–
–
√
On the whole, the present results indicate that the amyg-
dala might be in a position to influence particular thala-
mo-cortical pathways, particularly those involved in
emotion, memory and viscero-sensation (see review by
Jones 1985), by its rather specific targeting of various
thalamic nuclei (e.g. mediodorsal, midline, zona incerta).
Intralaminar
Basolateral
Ventroposterior
Medial geniculate
Lateral posterior
Mediodorsal
Midline
–
–
–
–
√
√
Intralaminar
Acknowledgements We thank Sharon Spana for technical assis-
Olfactory
Medial geniculate
Midline
Intralaminar
√
√
√
tance. The grant sponsor was NHMRC of Australia, grant no.
9
90255.
References
useful to compare these projections with the amygdalo-
thalamic projections described in this study. Table 1
shows the thalamic projections to each amygdaloid
group reported by previous studies. These results, taken
Clemence AE, Mitrofanis J (1992) Cytoarchitectonic heterogene-
ities in the thalamic reticular nucleus of cats and ferrets. J
Comp Neurol 332: 167–180
together with ours, indicate that only a minority of the Coleman KA, Mitrofanis J (1996) Organisation of the visual retic-
ular thalamic nucleus of the rat. Eur J Neurosci 8: 388–404
thalamo-amygdaloid pathways to the different amygda-
loid nuclei are reciprocated by a projection back from
Davis M (1992) The role of the amygdala in fear and anxiety.
Annu Rev Neurosci 15: 353–375
these nuclei. Indeed, only the midline and intralaminar,
and to a lesser extent the medial geniculate, nuclei seem
to have strong reciprocal relationships with the different
nuclei of the amygdala. The other nuclei, namely the
ventroposterior, lateral posterior and mediodorsal nuclei
seem to not receive afferents back from the amygdala.
Fallon JH, Ciofi P (1992) Distribution of monoamines within the
amygdala. In: Aggleton JP (ed) The amygdala: neurobiologi-
cal aspects of emotion, memory and mental dysfunction. Wi-
ley-Liss, New York, pp 97–114
Guillery RW (1995) Anatomical evidence concerning the role of
the thalamus in cortico-cortical communication: a brief review.
J Anat 187: 583–592
Thus, except for the classical “non-specific” midline and Hopkins D (1975) Amygdalo-tegmental projections in the rat, cat
and rhesus monkey. Neurosci Lett 1: 263
intralaminar nuclei, there does not appear to be a strong
feed-back relationship between the thalamus and the
amygdala. The significance of this unusual and rather
particular relationship is not clear at present. It remains Jones EG (1985) The thalamus. Plenum Press, New York
to be determined which one of these pathways, thalamo-
amygdaloid or amygdalo-thalamic, is in fact the feed-
forward pathway, and which one the feed-back.
At this point, some comment on reciprocal thalamic
projections with other brain centres should be made. Per-
haps the best-described and most precise set of reciprocal
connections that the thalamus has is with the neocortex.
Jia HG, Rao ZR, Shi JW (1992) Projection from the ventrolateral
medullary neurones containing tyrosine hydroxylase to the
central amygdaloid nucleus in the rat. Brain Res 589: 167–170
Kevetter GA, Winans SS (1981) Connections of the cortico-medi-
al amygdala in the golden hamster. I. Efferents of the “Vome-
ronasal amygdala”. J Comp Neurol 197: 81–98
Kolmac CI, Mitrofanis J (1997) Organisation of the thalamic retic-
ular projection to the intralaminar and midline nuclei in rats. J
Comp Neurol 377: 165–178
Kolmac CI, Mitrofanis J (1998) Patterns of projection from the
brainstem to the thalamic reticular nucleus. J Comp Neurol
3
96: 531–543
For these connections, there is no thalamic nucleus that Kolmac CI, Mitrofanis J (1999) Preferential connections between
does not receive a projection back from the cortical ar-
ea(s) it projects to, although the cortico-thalamic projec-
tions do tend to be a little more widespread than the cor-
responding thalamo-cortical projections (see Steriade et
al. 1997). For the brainstem, a slightly different organisa- Kretteck JE, Price JL (1977) Projections from the amygdaloid
tion is apparent. Most brainstem nuclei have rich projec-
tions to several dorsal thalamic (particularly the intralam-
inar and midline groups) and ventral (reticular nucleus
and zona incerta) nuclei; these same brainstem nuclei re-
the basal forebrain and the thalamus. Proc Aust Neurosci Soc
0: 177
1
Kolmac CI, Power BD, Mitrofanis J (1998) Patterns of connec-
tions between the zona incerta and brainstem in rats. J Comp
Neurol 396: 544–555
complex to the cerebral cortex and thalamus in the rat and the
cat. J Comp Neurol 172: 687–722
Kretteck JE, Price JL (1978) Amygdaloid projections to subcorti-
cal structures within the basal forebrain and brainstem in the
rat and cat. J Comp Neurol 178: 225–254

8
4
Le Doux JE, Iwata J, Cicchetti P, Reis DJ (1988) Different projec- Power BD, Kolmac CI, Mitrofanis J (1999) Evidence for a large
tions of the central amygdaloid nucleus mediate autonomic
and behavioural correlates of conditioned fear. J Neurosci 8:
projection from the zona incerta to the dorsal thalamus. J
Comp Neurol 404: 554–565
Rajakumar N, Elisevich K, Flumerfelt BA (1993) Biotinylated
dextran: a versatile anterograde and retrograde neuronal tracer.
Brain Res 607: 47–53
Russchen FT, Amaral DG, Price JL (1987) The afferent input to
the magnocellular division of the mediodorsal thalamic nucle-
us in the monkey, Macaca fascicularis. J Comp Neurol 256:
175–210
2
517–2529
Luiten PG, Ono T, Nishigo H, Fukuda M (1983) Differential input
from the amygdaloid body to the ventromedial hypothalamic
nucleus in the rat. Neurosci Lett 35: 253–258
McDonald, AJ (1985) Immunohistochemical identification of
gamma-aminobutyric acid-containing neurones in the rat baso-
lateral amygdala. Neurosci Lett 53: 203–207
Nitecka L, Amereski L, Panek-Mukula J, Narkiewicz O (1979) Scalia F, Winans SS (1975) The differential projections of the ol-
Thalamo-amygdaloid connections studied by the method of
retrograde transport. Acta Neurobiol Exp 30: 585–601
factory bulb and accessory olfactory bulb in mammals. J
Comp Neurol 161: 31–56
Olmos JD de, Alheid GF, Beltramino CA (1985) The amygdala. Sherman SM, Guillery RW (1996) Functional organisation of thal-
In: Paxinos G (ed) The rat nervous system I. Forebrain and
midbrain. Academic Press, Sydney, pp 223–334
amo-cortical relays. J Neurophysiol 76: 1367–1395
Sripanidkulchai K, Sripanidkulchai B, Wyss JM (1984) The corti-
cal projection of the basolateral amygdaloid nucleus in the rat:
a retrograde fluorescent dye study. J Comp Neurol 229:
419–431
Steriade M, Jones EJ, McCormick DA (1997) The thalamus, vol 1.
Organisation and function. Elsevier, Oxford
Olmos JS de (1972) The amygdaloid projection field in the rat as
studied with the cupric silver method. In: Eleftheriou BE (ed)
Neurobiology of the amygdala. Plenum Press, New York, pp
1
45–204
Ottersen OP (1981) Afferent connections of the amygdaloid com-
plex in the rat with some observations in the cat. III Afferents Swanson LW (1992) Brain maps: structure of the rat brain. Else-
from the lower brainstem. J Comp Neurol 203: 335–356 vier, Amsterdam
Ottersen OP, Ben-Ari Y (1979) Afferent connections to the amyg- Turner BH, Herkenham M (1991) Thalamo-amygdaloid process-
daloid complex in the rat and cat. I. Projections from the thala-
mus. J Comp Neurol 187: 401–424
ing in the rat: a test of the amygdala’s role in sensory process-
ing. J Comp Neurol 313: 295–325
Paxinos G, Watson CJ (1986) The rat brain in stereotaxic coordi- Veening JG (1978) Subcortical afferents of the amygdaloid com-
nates, 2nd edn. Academic Press, Sydney plex in the rat: an HRP study. Neurosci Lett 8: 197–202
Petrovich GD, Risold PY, Swanson LW (1996) Organisation of Wong M, Chen Y, Moss RL (1993) Excitatory and inhibitory syn-
projections from the basomedial nucleus of the amygdala: a
PHA-L study in the rat. J Comp Neurol 374: 387–420
aptic processing in the accessory olfactory system of the fe-
male rat. Neuroscience 56: 355–365