Synaptic organization of projections from the amygdala to visual cortical areas TE and V1 in the macaque monkey

Abstract

The primate amygdaloid complex projects to a number of visual cortices, including area V1, primary visual cortex, and area TE, a higher-order unimodal visual area involved in object recognition. We investigated the synaptic organization of these projections by injecting anterograde tracers into the amygdaloid complex of Macaca fascicularis monkeys and examining labeled boutons in areas TE and V1 using the electron microscope. The 256 boutons examined in area TE formed 263 synapses. Two hundred twenty-three (84%) of these were asymmetric synapses onto dendritic spines and 40 (15%) were asymmetric synapses onto dendritic shafts. Nine boutons (3.5%) formed double asymmetric synapses, generally on dendritic spines, and 2 (1%) of the boutons did not form a synapse. The 200 boutons examined in area V1 formed 211 synapses. One hundred eighty-nine (90%) were asymmetric synapses onto dendritic spines and 22 (10%) were asymmetric synapses onto dendritic shafts. Eleven boutons (5.5%) formed double synapses, usually with dendritic spines. We conclude from these observations that the amygdaloid complex provides an excitatory input to areas TE and V1 that primarily influences spiny, probably pyramidal, neurons in these cortices.

Figure 1

Line drawings representing a section in (A) area TE and (B) area V1. The approximate locations of regions chosen for electron microscopic analysis are identified by gray shading in both areas. While only one rostrocaudal plane is illustrated here, EM analysis was performed along the entire rostrocaudal extent of both areas. The insert demonstrates the lateral surface of the brain depicting the rostrocaudal locations of the represented area TE and V1 sections.

Figure 2

(A) A darkfield photomicrograph of a representative injection site. This PHA-L injection from case M1-03L was focused on the intermediate and magnocellular divisions of the basal nucleus and included the lateral and accessory basal nuclei as well. (B) A darkfield photomicrograph of a labeled fiber plexus in the superficial layers of area TE. Fibers are varicose and tend to run parallel to the pial surface. Layers I-III are indicated. (C) A high magnification brightfield photomicrograph of the fiber indicated by the arrow in (B). The arrows point to varicosities along the fiber. Scale bars: A = 250 μm, in B = 100 μm, and in C = 25 μm.

Figure 3

Electron micrographs of labeled amygdaloid terminals forming asymmetric axospinous synapses in area TE. PHA-L and BDA labeled boutons are identified by the dark, amorphous, electron-dense DAB reaction product. Unlabeled boutons (arrowheads) have a clear cytoplasm. Both amygdaloid boutons contain round synaptic vesicles and a single mitochondrion. The thickened postsynaptic densities (arrows) indicate that both synapses are asymmetric. Scale bar: 0.5 μm.

Figure 4

Graphs of the frequency distribution of bouton volumes in (A) area TE and (B) area V1.

Figure 5

Electron micrographs of 2 amygdaloid boutons each forming 2 asymmetric, axospinous synapses. The arrows point to the postsynaptic densities and “v” indicates small vacuoles that are an artifact of the DAB labeling process. Scale bar: 0.5 μm.

Figure 6

Electron micrographs of serial sections through a BDA labeled terminal in area TE. Sections are spaced 140 nm apart. This outon was classified as an asymmetric axospinous synapse based on the rounded synaptic vesicles (visible in all sections), the thickened postsynaptic density (arrows; apparent in panels C–F), and the spine apparatus (sa; panel E). Scale bar: 0.5 μm.

Figure 7

An electron micrograph of a PHA-L labeled bouton in area TE forming an asymmetric synapse with a dendritic shaft. The postsynaptic density between the amygdaloid bouton and the postsynaptic component is indicated by an arrow. This shaft also receives synapses from 2 axonal terminals of unknown origin (arrowheads). Scale bar: 0.5 μm.

Figure 8

(A–C) Three different asymmetric synapses between a labeled amygdaloid bouton and a spine in area V1. (D) An asymmetric axodendritic synapse in area V1. Scale bars = 0.5 μm.