Plasmalemmal appositions between cholinergic and non-cholinergic neurons in rat caudate-putamen nuclei

We have observed that in rat caudate-putamen nuclei, neurons immunolabeled for choline acetyltransferase were sometimes in direct apposition to unlabeled perikarya and dendrites [Pickel V. M. and Chan J. (1990) J. Neurosci. Res. 25, 263-280]. Similar juxtapositions between plasmalemmas of nerve cells each receiving input from one common terminal have been associated with activation of certain central neurons [Theodosis D. T. and Poulain D. A. (1989) Brain Res. 484, 361-366]. Thus, we sought to determine the relative abundance and ultrastructure of the appositions and the frequencies of shared synapses between choline acetyltransferase-labeled and unlabeled neurons in the rat striatum. A monoclonal antibody raised against choline acetyltransferase was localized in semi-adjacent ultrathin sections through 24 neurons in the dorsolateral caudate-putamen nuclei. Five of these choline acetyltransferase-labeled perikarya showed direct somatic appositions with unlabeled neurons. The remaining 19 of the choline acetyltransferase-labeled perikarya did not show somatic appositions with unlabeled perikarya; however, when traced through multiple (20-100) semi-adjacent sections their dendrites always showed extensive plasmalemmal juxtapositions with one or more unlabeled perikarya. The apposed perikarya had round nuclei and other characteristics of medium, spiny neurons. The majority of the apposed cholinergic and non-cholinergic neurons were postsynaptic to at least one common unlabeled terminal. These terminals usually formed symmetric junctions. At sites of appositions, the plasmalemmas of choline acetyltransferase-immunoreactive soma or dendrites and unlabeled neurons were closely spaced without intervening astrocytic processes. The appositions lacked the ultrastructural features typical of gap-junctions, but did occasionally show parallel arrays of thin (1-2 nm) electron-dense bands. In both labeled and unlabeled perikarya, the nuclei were separated from the appositional zones by narrow (0.7-3.3 microns) rims of cytoplasm. This cytoplasmic rim contained subsurface cisternae and other less specialized smooth and rough endoplasmic reticulum, and vesicular structures. The findings suggest that in the caudate-putamen nuclei (1) the tonically active cholinergic neurons [Wilson C. J. et al. (1990) J. Neurosci. 10, 508-519] may modulate or be modulated by non-cholinergic spiny neurons through non-synaptic somatic or dendritic appositions, and (2) that both neurons may be simultaneously inhibited by shared afferent input. Activation of this system could facilitate coordinated movements through synchronization of cholinergic interneurons and spiny projection neurons containing GABA or other transmitters.