Neurons of the basolateral amygdala: A Golgi study in the opossum (Didelphis virginiana)

Abstract

The cytoarchitecture of the opossum basolateral amygdala was studied using Golgi techniques. The neuronal morphology was similar in all nuclei of the basolateral complex, an three distinct cell classes were recognized. Class I neurons, which vary in size in different nuclei, have spiny dendrites and long, projection axons. Axon hillocks and initial axonal segments often have spinous protrusions, while more distal portions of the axon give off several beaded collaterals that arborize primarily in the vicinity of the cell. Class II neurons are smaller, spine-sparse cells that are found in all nuclei of the basolateral amygdala but are greatly outnumbered by class I neurons. Axons branch and give off beaded collaterals which form a moderate to dense arborization within the dendritic field of the cell. Class II neurons exhibit considerable morphologic variability including one subtype that resembles the chandelier cell of the cerebral cortex. Varicosities (1.0 - 1.5 micrometers swellings) found along the axonal collaterals of these amygdaloid chandelier cells do not have a uniform distribution but tend to be aggregated. Segments of the collaterals displaying such clustered varicosities sometimes form nest-like entanglements. Clusters of varicosities have been observed forming multiple contacts with initial segments of class I axons. Class III neurons are neurogliaform cells which have many short, varicose dendritic branches that contact dendrites of class I neurons. Only the initial portions of their axons were impregnated. This study indicates that many of the cell types seen in the generalized, metatherian opossum are similar to those described in more specialized, placental mammals. This is the first description of amygdaloid chandelier cells and their contacts with the spiny initial segments of class I projection neurons.

Pyramidal cells of the rat basolateral amygdala: Synaptology and innervation by parvalbumin‐immunoreactive interneurons

“…Betette and McDonald (1997) described an AIS of a pyramidal cell in the rat BLa that was 30 μm long and was postsynaptic to 17 PV+ axon terminals, and no PV-negative terminals. The CaMK+ AIS of the pyramidal cell seen in the present study was postsynaptic to 16 axon terminals, all forming symmetrical synapses, including 10 intensely-stained PV+ terminals.ABL chandelier cells were first described in Golgi studies of the opossum amygdala (McDonald and Culberson, 1981), and later in the rat (McDonald, 1982). Since their axons are often myelinated, some of the myelinated PV+ axons seen in the present study may belong to chandelier cells.…”

“…Similar results were obtained in the neocortex and hippocampus, where there are actually two separate subpopulations of perisomatic PV+ interneurons: (1) basket cells that have a robust innervation of pyramidal cell somata, and (2) chandelier cells forming "axonal cartridges" that only innervate the axon initial segments of pyramidal cells (Freund and Buzsaki, 1996;Kawaguchi and Kubota, 1998; Maccaferri et al, 2000). Since Golgi studies in the ABL (McDonald and Culberson, 1981;McDonald, 1982) have described chandelier cells whose axons appear to only form axonal cartridges, it appears that the pericellular baskets surrounding ABL pyramidal cell somata may be formed by a separate population of PV+ basket cells.…”

“…The latter cartridges typically exhibit 10-15 axon terminals. In Golgi-stained preparations the axon terminals in cartridges have been seen to make intimate synaptic-like contacts with the AISs of ABL pyramidal cells (McDonald and Culberson, 1981;McDonald, 1982).One Golgi-stained chandelier cell in the rat lateral nucleus, whose axon appeared to be almost entirely confined to the (150-μm-thick) section of origin, formed a total of 126 axonal cartridges within a field that was about 300 um in diameter (see Fig. 14 of McDonald, 1982).…”

“…Similar results were obtained in the neocortex and hippocampus, where there are actually two separate subpopulations of perisomatic PV+ interneurons: (1) basket cells that have a robust innervation of pyramidal cell somata, and (2) chandelier cells forming "axonal cartridges" that only innervate the axon initial segments of pyramidal cells (Freund and Buzsaki, 1996;Kawaguchi and Kubota, 1998; Maccaferri et al, 2000). Since Golgi studies in the ABL (McDonald and Culberson, 1981;McDonald, 1982) have described chandelier cells whose axons appear to only form axonal cartridges, it appears that the pericellular baskets surrounding ABL pyramidal cell somata may be formed by a separate population of PV+ basket cells.PV+ chandelier cells in the ABL-There have been very few observations of the innervation of pyramidal cell axon initial segments (AISs) in the ABL at the electron microscopic level. Sorvari and co-workers found numerous "axonal cartridges" formed by PV+ axons enclosing elongated, non-immunostained structures in the human ABL at the light microscopic level (Sorvari et al, 1996).…”

Somatostatin-like immunoreactivity in the amygdala of the pig.

“…Although the data concerning the neuronal organization [3][4][5] and circuitry [6,7] of the particular regions in CA are abundant, little is known about how the amygdala participates in these emotional functions at the neuronal and synaptic levels. To answer this question is to identify first the chemical coding pattern of the major cell types.…”