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On the basis of chemoarchitecture and gene expression patterns in the amphibian amygdaloid complex, new subdivisions have been proposed and compared with their counterparts in amniotes. Thus, a portion of the ventral pallium of anurans has been tentatively named "lateral amygdala" (LA) and compared with the basolateral complex of mammals. To strengthen the putative homology, we have analyzed the pattern of afferent and efferent connections of the LA in the anurans Rana perezi and Xenopus laevis. Tract-tracing techniques with dextran amines were used under in vivo and in vitro conditions. The results showed important connections with the main olfactory bulb, via the lateral olfactory tract. In addition, abundant intratelencephalic connections, via the rostral branch of the stria terminalis, were revealed, involving mainly the basal ganglia, septal nuclei, bed nucleus of the stria terminalis, and especially other amygdaloid nuclei. Nontelencephalic connections were found from the dorsal thalamus and parabrachial area and, in particular, from the hypothalamus through the caudal branch of the stria terminalis. All these results strongly suggest that the LA in anurans is a multimodal area in the ventral pallium that shares many hodological features with the amygdaloid ventropallial derivatives of the basolateral complex of amniotes.
Fig. 1. Charting of retrograde and anterograde labeling following a BDA injection centered in the
lateral amygdala of Rana perezi. Large dots represent labeled neurons, whereas dashes and small dots
represent labeled fibers. The levels of the selected transverse sections aâo are indicated in the upper
right scheme of the brain. See list for abbreviations.
Fig. 2. Photomicrographs of Nissl-stained transverse sections through the brain of Rana perezi (a,b)
and Xenopus laevis (c) showing the lateral wall of the telencephalon at middle (a,c) and caudal (b) levels
to illustrate the topological position of the lateral amygdala. Scale bars 100 m.
Fig. 3. Photomicrographs of transverse sections through the brain
of the Rana perezi. a: Immunolabeling for nitric oxide synthase at the
level of the lateralamygdala. b,c: Representative BDA injection sites
into the lateralamygdala. d: Fibers and cells in the nucleus accumbens.
e: Fibers and cells in the bed nucleus of the stria terminalis and
the diagonal band. f: Labeled cells in the caudal pallium. g: Labeled
cells in the rostral portion of the lateralamygdala after BDA applications
in the caudal part. h,i: Labeled cells and fibers in the striatum
and the central amygdala. Scale bars 100 m.
Fig. 4. Photomicrographs of transverse sections through the brain
of Rana perezi (a,b,d–g) and Xenopus laevis (c) illustrating labeled
cells and fibers after BDA injection in the lateralamygdala.
a,b: Labeled cells and fibers at caudal telencephalic levels, showing
the labeled fibers in the rostral branch of the stria terminalis.
c,d: Detail of the labeled fiber bundle in the stria terminalis and cells
in the suprachiasmatic nucleus. e: Labeled neurons in the retrochiasmatic
nucleus and terminal field. f: Terminal field of the stria
terminalis in the ventromedial hypothalamus and retrogradely labeled
cells. g: Anterior thalamic nucleus. Scale bars 100 m in a,b,c,
(applies to c–e), f,g.
Fig. 5. Photomicrographs of transverse sections through the brain
of Rana perezi (a–e) and Xenopus laevis (f,g) illustrating labeled fibers
after BDA injection in the lateralamygdala. a: Labeled fibers in the
rostral branch of the stria terminalis at medial telencephalic levels.
b,c: Terminal fields of the stria terminalis in the retrochiasmatic area
and ventromedial hypothalamus. d,e: Pair of photomicrographs showing
double-labeled terminal field in the retrochiasmatic area after
BDA injections in the lateralamygdala (d) and immunohistochemistry
for nitric oxide synthase (e) immunohistochemistry. f,g: Terminal
fields of the stria terminalis at the suprachiasmatic and retrochiasmatic
area in the Xenopus brain. Scale bars 100 m.
Fig. 6. Photomicrographs of transverse sections through the brain
of Rana perezi. a: Retrogradely labeled cells in the lateral amygdala
after BDA injection centered in the central amygdala. b: Retrogradely
labeled cells in the lateral amygdala after BDA injection centered in
the ventromedial hypothalamus. c,d: Pair of photomicrographs showing
a fibers and a terminal field in the lateral amygdala after BDA
injection in the parabrachial area (c) and simultaneous labeling for
nitric oxide synthase (d) immunohistochemistry in the lateral amygdala.
Scale bars 50 m in a; 70 m in b; 100 in c and d.
Fig. 7. Photomicrographs showing labeled cells and fibers in
transverse sections in the brain in experiments confirming the connections
of the lateralamygdala. a: Lateral olfactory tract fibers after
FDA injection into the main olfactory bulb. b: Cells and fibers labeled
in the lateralamygdala and medialamygdala after BDA injection into
the ventralhypothalamus. c: Double-labeled section (the same as in a
and b) showing simultaneosly the terminal neuropil formed by axons
from the main olfactory bulb (green) and the labeled cells in the
lateralamygdala that project to the hypothalamus (red). d,e: Pair of
photomicrographs showing cells and fibers labeled in the lateralamygdala and medialamygdala after BDA injection into the ventralhypothalamus (d) and simultaneous labeling for nitric oxide synthase
(e) immunohistochemistry in order to distinguish both areas clearly.
f: Double-labeled section showing simultaneosly the terminal neuropil
formed by axons from the accessory olfactory bulb (green) and the
labeled cells in the medialamygdala and lateralamygdala that
project to the hypothalamus (red), confirming the vomeronasal input
to the medialamygdala. Scale bars 100 m.
Fig. 8. Summary diagram showing, in a dorsal view of the brain,
the afferent and efferent connections of the lateral amygdala found in
the present study.
Fig. 9. Diagram of two transverse sections through the telencephalon
(a) and diencephalon (b) illustrating the organization of the
efferent fibers from the lateral amygdala (red) and medial amygdala
(green) in the stria terminalis. Both telencephalic (1) and hypothalamic
(2) branches of the stria terminalis are indicated, and the
terminal fields in the hypothalamus are also depicted.
