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.

Efferent Modulation of Spontaneous Lateral Line Activity During and after Zebrafish Motor Commands

“…We still know relatively little about efferent modulation in freely-swimming fishes, where hydrodynamic stimuli from swimming can further impact afferent activity, but we now have a greater appreciation for the complex relationship between sensory and motor systems. In freely moving fish, afferent spike frequencies increase both during swimming and during feeding strikes (Palmer et al 2005; Palmer et al 2003; Ayali et al 2009; Mensinger et al 2019). This is consistent with our observation that efferent activity only partially suppresses spontaneous spike rates.…”

“…Fishes sense perturbations in the fluid environment through the lateral line, a sensory organ on the body surface that translates fluid motion relative to the body into neural signals essential for navigation (Olszewski, et al 2012, Suli et al 2012, Oteiza et al 2017), predator avoidance, prey capture (McHenry et al 2009; Stewart et al 2013), and schooling (Mekdara et al 2018). However, since water motions are also self-generated by behaviors such as swimming (Palmer et al 2003; Ayali et al 2009; Mensinger et al 2019), respiration (Montgomery et al 1996; Montgomery and Bodznick 1994; Palmer et al 2003), and feeding (Palmer et al 2005), fishes should possess a mechanism to discriminate such self-generated signals from environmental signals.…”

Hydrodynamic sensing does not facilitate active drag reduction in the golden shiner (Notemigonus crysoleucas)

“…This entrained swimming, called the Kàrmàn gait, is altered when the lateral line system is pharmacologically ablated (Liao, 2006). The same treatment causes lamprey (Petromyzon marinus) swimming in still water to use a slightly greater undulatory wavelength (Ayali et al, 2009). These studies demonstrate that swimming may be altered by disabling the lateral line, but it remains unclear what performance advantages come from using flow sensing to mediate steady swimming.…”

The fish body functions as an airfoil: surface pressures generate thrust during carangiform locomotion

“…Anguilliform swimmers (A) produce negative pressure thrust along the whole body using an undulatory pump mechanism, in which high amplitude body movements suck fluid along the body. Anguilliform kinematics adapted from (57). In contrast, carangiform swimmers (B) produce thrust on the anterior body through airfoil-like mechanics.…”