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Stereological analysis of the rat and monkey amygdala - PubMed

  • ️Sat Jan 01 2011

Stereological analysis of the rat and monkey amygdala

Loïc J Chareyron et al. J Comp Neurol. 2011.

Abstract

The amygdala is part of a neural network that contributes to the regulation of emotional behaviors. Rodents, especially rats, are used extensively as model organisms to decipher the functions of specific amygdala nuclei, in particular in relation to fear and emotional learning. Analysis of the role of the nonhuman primate amygdala in these functions has lagged work in the rodent but provides evidence for conservation of basic functions across species. Here we provide quantitative information regarding the morphological characteristics of the main amygdala nuclei in rats and monkeys, including neuron and glial cell numbers, neuronal soma size, and individual nuclei volumes. The volumes of the lateral, basal, and accessory basal nuclei were, respectively, 32, 39, and 39 times larger in monkeys than in rats. In contrast, the central and medial nuclei were only 8 and 4 times larger in monkeys than in rats. The numbers of neurons in the lateral, basal, and accessory basal nuclei were 14, 11, and 16 times greater in monkeys than in rats, whereas the numbers of neurons in the central and medial nuclei were only 2.3 and 1.5 times greater in monkeys than in rats. Neuron density was between 2.4 and 3.7 times lower in monkeys than in rats, whereas glial density was only between 1.1 and 1.7 times lower in monkeys than in rats. We compare our data in rats and monkeys with those previously published in humans and discuss the theoretical and functional implications that derive from our quantitative structural findings.

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Figures

Figure 1
Figure 1

Low-magnification photomicrographs of representative coronal sections through the rat amygdala illustrating the locations of the main nuclei. L, lateral; B, basal; AB, accessory basal; CE, central; M, medial. Nonlabeled areas represent remaining nuclei of the amygdala; see list in Table 1. Scale bar = 500 μm in A (applies to all panels).

Figure 2
Figure 2

Low-magnification photomicrographs of representative coronal sections through the monkey amygdala illustrating the locations of the main nuclei. L, lateral; B, basal; PL, paralaminar; AB, accessory basal; CE, central; M, medial. Nonlabeled areas represent remaining nuclei of the amygdala; see list in Table 1. Scale bar = 1 mm in A (applies to all panels).

Figure 3
Figure 3

Classification and identification of different cell types in rats and monkeys. A: Typical neuron and glial cells viewed with a 100× objective in the rat amygdala basal nucleus as revealed in Nissl-stained sections cut at 40 μm. B: Typical neuron and glial cells viewed with a 100× objective in the monkey amygdala basal nucleus as revealed in Nissl-stained sections cut at 60 μm. Note that we were able to reliably distinguish between astrocytes and oligodendrocytes in monkeys, but not in rats, based on morphological criteria (see main text for details). Scale bar = 5 μm in A (applies to B).

Figure 4
Figure 4

Three-dimensional reconstruction of the main amygdala nuclei in rat (A–D), monkey (E–H), and human (I–L). Lateral nucleus is in red, basal nucleus is in orange, paralaminar nucleus is in dark orange (in monkeys only), accessory basal nucleus is in blue, central nucleus is in green, and medial nucleus is in pink (not represented in humans). Scales: rat, gray cube is 1 mm3; monkey, gray cube is 2 mm3; human, gray cube is 4 mm3. 3D reconstructions are available in movie format as Supporting Information 2 and 3 online.

Figure 5
Figure 5

A: Volumes of the main amygdala nuclei in rats, monkeys, and humans. The deep nuclei (lateral, basal, accessory basal) are relatively more developed in monkeys and humans than in rats. Note that the volume of the human medial nucleus was not estimated by Schumann and Amaral (2005). A dashed line in the bar representing the basal nucleus in monkeys indicates the volume of the paralaminar nucleus (upper part of the bar), and is included to enable the comparison with the human data (which included the paralaminar nucleus in the basal nucleus). B: Neuron numbers in the main amygdala nuclei of rats, monkeys, and humans. Note that neuron number in the human medial nucleus was not estimated by Schumann and Amaral (2005). A dashed line in bar representing the basal nucleus in monkeys indicates the number of neurons of the paralaminar nucleus (upper part of the bar), and is included to enable the comparison with the human data. C: Average neuronal soma size in the amygdala of the rat, monkey, and human. D: Average neuron density in the amygdala of the rat, monkey, and human. E: Percentage of total amygdala volume occupied by neuronal somas in the amygdala of the rat, monkey, and human. A lower percentage is associated with greater development of the neuropil. Error bars ± SD.

Figure 6
Figure 6

Distributions of neuronal soma size in the main amygdaloid nuclei of rats (A–E) and monkeys (A′–F′). A,A′: Lateral nucleus; B,B′: basal nucleus; C,C′: accessory basal nucleus; D,D′: central nucleus; E,E′: medial nucleus; F′: paralamniar nucleus (only in monkeys).

Figure 6
Figure 6

Distributions of neuronal soma size in the main amygdaloid nuclei of rats (A–E) and monkeys (A′–F′). A,A′: Lateral nucleus; B,B′: basal nucleus; C,C′: accessory basal nucleus; D,D′: central nucleus; E,E′: medial nucleus; F′: paralamniar nucleus (only in monkeys).

Figure 7
Figure 7

Relationship between neuronal density and neuronal soma size in the main nuclei of the rat, monkey, and human amygdala. Logarithmic regression of neuron density and neuron soma size in the amygdala (log10(neuron density) = 10.116 – 1.745 × log10(soma size); R2 = 0.85; F(1.59) = 342.44; P < 0.001). Rat, dark gray; monkey, gray; human, white. Lateral nucleus, circles; basal nucleus, upside-down triangles; accessory basal nucleus, squares; central nucleus, diamonds; medial nucleus, triangles; paralaminar (only in monkeys), stars.

Figure 8
Figure 8

Summary representation of the amygdala in rats (A), monkeys (B), and humans (C). Glial cells, circles; neurons, triangles: rats < monkeys < humans. Neuron density: rats > monkeys > humans. Glia density: rats = monkeys = humans. Glia/neuron ratio: rats < monkeys < humans. Connectivity with visceral and autonomic systems (mainly via the central nucleus): rats = monkeys = humans. Connectivity with cortical systems (between the neocortex and the lateral, basal, and accessory basal nuclei): rats < monkeys < humans. The proportions of the different parameters are not precisely scaled.

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