Serotonergic transmission and gap junctional coupling in proventricular muscle cells in the American cockroach, Periplaneta americana

Abstract

The visceral muscle tissues of insects consist of striated muscle cells. The mechanisms responsible for delivering signals to the contractile muscles in the insect digestive tract remain unclear. We found that serotonergic nerves innervate the hemocoel surfaces of foregut and midgut muscles in the American cockroach. Electron microscopy of the neuromuscular junctions in the proventriculus (gizzard) revealed typical synaptic structures, the accumulation of large core/cored vesicles (neuropeptides) and small clear vesicle (neurotransmitter) at presynapses, and synaptic clefts. However, only a limited number of muscle cells, which were located in the outer part of the muscle layer, came into contact with synapses, which contained classical neurotransmitters, such as glutamate. A gap junction channel-permeable fluorescent dye, Lucifer yellow, was microinjected into single muscle cells, and it subsequently spread to several neighboring muscle cells. The dye movement occurred in the radial (hemocoel-lumen) direction rather than tangential directions. A gap junction blocker, octanol, reversibly inhibited the dye coupling. Messenger RNA for innexin 2, a gap junction-related protein, was detected in the proventriculus. These results suggest that motile signals in the insect digestive tract only reach the outermost part of the visceral muscles and are propagated to the inner muscle cells via gap junctions. Therefore, invertebrate gap junction-related proteins have potential as new targets for pest control.