Network Architecture of Gap Junction-Coupled Neuronal Linkage in the Striatum

Previous studies have revealed the existence of gap junctions between GABAergic interneurons of a particular type in the striatum. Because of the technical difficulties, however, there is no information about their positions within the striatal circuitry. We have developed a method to detect neuronal gap junctions reliably at the light microscopic level and thereby explored the network architecture of the gap junctional linkage. Gap junction-coupled networks among parvalbumin-containing GABAergic interneurons extended nonuniformly in the feline striatum. They were located predominantly in the methionine-enkephalin-poor matrix. Moreover, the density of gap junctional coupling showed a marked regional difference along the anterior-posterior axis of the striatum. The densest interconnectivity was found in the posterior part of both caudate nucleus and putamen that corresponds to the sensory-recipient area of the feline striatum. Electron microscopic observations provided clear evidence of internalization of neuronal gap junction, indicating the dynamic nature of gap junctional linkage between neurons in vivo. The nonuniform organization of gap junction networks suggests differential modes of information processing in heterogeneous subregions of the striatum.