Tension sensitivity of the heart pacemaker neurons in the isopod crustaceanLigia pallasii

Abstract

SUMMARYIn the crustacean neurogenic heart, the cardiac ganglion (CG) acts as a peripherally located central pattern generator (CPG) by producing rhythmic motor output that initiates the heartbeat. In the isopod Ligia, the CG consists of six electrically coupled neurons that all function both as endogenous oscillators and as glutamatergic motoneurons innervating heart muscle. In the present study, we present several lines of evidence to suggest that the CG neurons are sensitive to passive stretch and active tension of the heart muscle. Stretching the heart wall caused a sustained decrease in the burst frequency of the CG neuron. Releasing from the stretch caused a rebound increase in burst frequency above the control rate. A brief stretch (200-300 ms duration) caused either phase advance or phase delay of the following CG bursts, depending on the timing at which the stretch was applied. Repeated brief stretches could entrain the CG bursts to either higher or lower frequencies than the free-run burst frequency. Intracellular recording from one of the CG neurons revealed that it exhibited hyperpolarization during the stretch. The stretch-induced hyperpolarization was followed by a burst discharge upon release from the stretch. With increased stretch amplitude, the amplitude of hyperpolarizing response increased and the timing of the following burst was advanced. When the myogenic activity of the heart muscle was pharmacologically isolated from the ganglionic drive by applying a glutamatergic antagonist, Joro spider toxin (JSTX), the spontaneous muscle contraction caused a hyperpolarizing deflection in the CG neuron. Under specific conditions made by JSTX and tetrodotoxin, the CG burst became entrained to the myogenic rhythm. These results suggest that the Ligia CG neurons have tension sensitivity in addition to their pacemaker and motoneuronal functions. Such multifunctional neurons may form a single neuron reflex arc inside the heart.