Lateral-line activity during undulatory body motions suggests a feedback link in closed-loop control of sea lamprey swimming

Abstract

The lateral-line system is common to most aquatic organisms. It plays an important role in behaviours involving detection of other animals and obstacles. In gnathostome fishes, these behaviours appear to be dependent on an efferent inhibitory system that filters out stimuli caused by the animal’s own movement. Sea lampreys ( Petromyzon marinus L., 1758), the most basal extant vertebrate, possess a functional lateral-line system. Yet they completely lack the inhibitory efferent system. Thus, they may use the lateral line to sense their own swimming movements, helping to stabilize swimming. To test this hypothesis, we first investigated the kinematics of free-swimming lampreys. In an intact tethered preparation, we then generated undualatory body motions of comparable amplitude and frequency to swimming, while monitoring the evoked responses of the posterior lateral-line nerve. Last, we tested the effect of eliminating lateral-line inputs by cobalt treatment. In the tethered preparation, we recorded distinctive and consistent activity in the lateral-line nerve that was strongly dependent on characteristics of the motion. We found that distinct characteristics of the rhythmic movements are encoded in the temporal characteristics of the response. Swimming kinematics of cobalt-treated animals differed from controls, suggesting a complex, yet necessary role of the lateral-line system in closed-loop control of swimming.