Revisiting the reticulum: feedforward and feedback contributions to motor program parameters in the crab cardiac ganglion microcircuit

Abstract

The neurogenic heartbeat of crustaceans is controlled by the cardiac ganglion (CG), a central pattern generator (CPG) microcircuit composed of nine neurons. In most decapods, five “large” motor neurons (MNs) project from the CG to the myocardium, where their excitatory synaptic signals generate the rhythmic heartbeat. The processes of four “small” premotor neurons (PMNs) are confined to the CG, where they provide excitatory drive to the MNs via impulse-mediated chemical signals and electrotonic coupling. This study explored feedforward and feedback interactions between the PMNs and the MNs in the CG of the blue crab ( Callinectes sapidus). Three methods were used to compare the activity of the MNs and the PMNs in the integrated CG to their autonomous firing patterns: 1) ligatures were tightened on the ganglion trunk that connects the PMNs and MNs; 2) TTX was applied focally to suppress selectively PMN or MN activity; and 3) sucrose pools were devised to block reversibly PMN or MN impulse conduction. With all treatments, the PMNs and MNs continued to produce autonomous rhythmic bursting following disengagement. Removal of PMN influence resulted in a significantly reduced MN duty cycle that was mainly attributable to a lower autonomous burst frequency. Conversely, after removal of MN feedback, the PMN duty cycle was increased, primarily due to a prolonged burst duration. Application of sucrose to block impulse conduction without eliminating PMN oscillations disclosed significant contributions of spike-mediated PMN-to-MN signals to the initiation and prolongation of the MN burst. Together, these observations support a view of the Callinectes CG composed of two classes of spontaneously bursting neurons with distinct endogenous rhythms. Compartmentalized feedforward and feedback signaling endow this microcircuit with syncytial properties such that the intrinsic attributes of the PMNs and MNs both contribute to shaping all parameters of the motor patterns transmitted to the myocardium.