Graded neuromuscular transmission in the heart of the isopod crustacean Ligia exotica

Abstract

We present several lines of evidence for the occurrence of graded synaptic transmission in addition to impulse-mediated transmission at the neuromuscular junction between cardiac ganglion (CG) neurones and the myocardium in the isopod crustacean Ligia exotica. In the heart of adult Ligia exotica, the CG acts as a primary pacemaker for the heartbeat by generating periodic bursts of impulses and entrains the myogenicity of the myocardium via impulse-mediated excitatory junctional potentials. When impulse generation was blocked by tetrodotoxin (TTX; 50 nmol l(−)(1)), the CG neurones and the myocardium periodically exhibited synchronized slow depolarizing potentials. The association between the slow depolarizing potentials in the neurone and the myocardium was eliminated by application of Joro spider toxin (JSTX), a specific glutamate antagonist. When the CG neurone was made quiescent by a higher dose of TTX (1.0 micromol l(−)(1)), sinusoidal current injected into the CG neurone induced similar sinusoidal membrane potential responses in the myocardium. The sinusoidal muscle responses were eliminated by application of either JSTX or low-Ca(2+) saline. Under voltage-clamp conditions, the myocardium exhibited periodic inward current responses to sinusoidal current stimuli applied to the CG neurone. The reversal potential for the current response of the myocardium was similar to that of the impulse-mediated excitatory junctional current (EJC). Extracellular macropatch recordings of EJCs made at the neuromuscular junctional site revealed the spontaneous appearance of miniature EJCs asynchronous with the CG spikes in addition to large spike-evoked EJCs. The miniature EJCs were present in saline containing TTX, and their frequency was strongly affected by the slow membrane potential change in the CG neurone. These results suggest that the CG neurones drive the myocardium by graded neuromuscular transmission in addition to impulse-mediated transmission in the heart of Ligia exotica.