The electric organ discharge of pulse gymnotiforms: the transformation of a simple impulse into a complex spatio-temporal electromotor pattern

Abstract

An understanding of how the nervous system processes an impulse-like input to yield a stereotyped, species-specific electromotor output is relevant for electric fish physiology, but also for understanding the general mechanisms of coordination of effector patterns. In pulse gymnotids, the electromotor system is repetitively activated by impulse-like signals generated by a pacemaker nucleus in the medulla. This nucleus activates a set of relay cells whose axons descend along the spinal cord and project to electromotor neurones which, in turn, project to electrocytes. Relay neurones, electromotor neurones and electrocytes may be considered as layers of a network arranged with a lattice hierarchy. This network is able to coordinate a spatio-temporal pattern of postsynaptic and action currents generated by the electrocyte membranes. Electrocytes may be innervated at their rostral face, at their caudal face or at both faces, depending on the site of the organ and the species. Thus, the species-specific electric organ discharge patterns depend on the electric organ innervation pattern and on the coordinated activation of the electrocyte faces. The activity of equally oriented faces is synchronised by a synergistic combination of delay lines. The activation of oppositely oriented faces is coordinated in a precise sequence resulting from the orderly recruitment of subsets of electromotor neurones according to the ‘size principle’ and to their position along the spinal cord. The body of the animal filters the electric organ output electrically, and the whole fish is transformed into a distributed electric source.