A correlative electron microscopic study of basket cells and large gabaergic neurons in the monkey sensory-motor cortex

Abstract

Large basket cells were identified in Golgi and horseradish peroxidase labeled material from the sensory-motor cortex of adult monkeys. Their morphology was correlated at the light and electron microscopic level with large comparable cells stained immunocytochemically for glutamate decarboxylase. In Golgi-impregnated material these cells have a very large cell body and dendrites that extend through several layers of the cortex with a predominant vertical orientation. The axon is only stained for a few micrometers. The same cells studied electron microscopically in serial sections after gold-toning show very distinctive ultrastructural characteristics: the cell bodies contain a large number of organelles, the nuclei are rounded with homogeneously dispersed chromatin and synapsing onto the somata are many axon terminals, both symmetrical and asymmetrical but the symmetrical type forms 70–80% of the total; dendrites also receive a large number of both symmetrical and asymmetrical synaptic contacts. All the axons of basket cells become myelinated and the Golgi labeling of the initial segments is interrupted at the commencement of the first myelin internode. The axon initial segments receive several symmetrical synaptic contacts in the proximal one-third of their length. The axonal arborization of a basket cell retrogradely labeled in the somatosensory cortex after intracortical injection of horseradish peroxidase was analyzed in detail. The mainly horizontal axonal collaterals of this cell are myelinated for most of their trajectory and have a preferred orientation in the anteroposterior dimension. These axonal collaterals, although very long (more than 1.8 mm), at intervals give rise to a small number of short unmyelinated terminal branches that bear a series of boutons terminaux forming a multi-terminal ending. The multi-terminal endings surround somata and proximal dendrites of pyramidal and non-pyramidal cells. Dense pericellular terminations (baskets or nests) like those drawn by Ramón y Cajal 5 and Marin-Padilla 31 are not formed by the axon of a single basket cell. Thus, basket formations are presumably formed by converging axons from several basket cells. Immunocytochemical material was stained for glutamate decarboxylase, the enzyme involved in the synthesis of γ-aminobutyrate (GABA). This shows that large glutamate decarboxylase-positive neurons of the same size as those positively identified as basket cells in the Golgi and horseradish peroxidase material have virtually the same morphological characteristics, at both the light and electron microscope levels, as the basket cells. Serial electron microscopic reconstructions of large glutamate decarboxylase-positive cells show the same proportions and number of synapses onto the cell bodies, dendrites and axon initial segments as for positively identified basket cells. Many of the symmetrical synaptic contacts on the cell bodies and dendrites of large glutamate decarboxylase positive cells are formed by glutamate decarboxylase positive multiterminal endings similar to those seen on pyramidal cells in both horseradish peroxidase and glutamate decarboxylase immunoreactive material. Serial electron microscopic reconstruction of these multi-terminal endings show that many of them make additional contacts on adjacent pyramidal cells. Basket cells in monkey sensory-motor cortex are, thus, revealed as GABAergic interneurons that appear to inhibit mutually one another in addition to inhibiting pyramidal neurons.