The role of mechanical resonance in the neural control of swimming in fishes

Abstract

The bodies of many fishes are flexible, elastic structures; if you bend them, they spring back. Therefore, they should have a resonant frequency: a bending frequency at which the output amplitude is maximized for a particular input. Previous groups have hypothesized that swimming at this resonant frequency could maximize efficiency, and that a neural circuit called the central pattern generator might be able to entrain to a mechanical resonance. However, fishes swim in water, which may potentially damp out many resonant effects. Additionally, their bodies are elongated, which means that bending can occur in complicated ways along the length of the body. We review previous studies of the mechanical properties of fish bodies, and then present new data that demonstrate complex bending properties of elongated fish bodies. Resonant peaks in amplitude exist, but there may be many of them depending on the body wavelength. Additionally, they may not correspond to the maximum swimming speed. Next, we describe experiments using a closed-loop preparation of the lamprey, in which a preparation of the spinal cord is linked to a real-time simulation of the muscle and body properties, allowing us to examine resonance entrainment as we vary the simulated resonant frequency. We find that resonance entrainment does occur, but is rare. Gain had a significant, though weak, effect, and a nonlinear muscle model produced resonance entrainment more often than a linear filter. We speculate that resonance may not be a critical effect for efficient swimming in elongate, anguilliform swimmers, though it may be more important for stiffer carangiform and thunniform fishes.

Batoid locomotion: effects of speed on pectoral fin deformation in the little skate, Leucoraja erinacea

“…Fourth, active stiffening of tissues as speed changes is a key area of interest in aquatic locomotion. For fishes, activation of red musculature along the body causes changes in stiffness and the fluid-structure interaction that may be related to changing locomotor efficiency (Flammang, 2010;Long et al, 2011;Root et al, 2007;Tytell et al, 2010Tytell et al, , 2014, but data suggesting active changes in wing surface stiffness are not available for any batoid. By analyzing wing kinematics over a doubling of swimming speed in the little skate, we aim to determine whether kinematic data show evidence of active wing stiffening by intrinsic musculature.…”

Closed-Loop Control of Active Sensing Movements Regulates Sensory Slip

“…Closed-loop experimental approaches [6,50] are crucial for disentangling complex interactions between sensing and control [51][52][53]…”

Automatic control: the vertebral column of dogfish sharks behaves as a continuously variable transmission with smoothly shifting functions

“…No one to our knowledge has attempted an experiment of this complexity in a living fish, probably because it would require, simultaneously and in a flow tank, surgical implantation of vast arrays of EMG electrodes, pressure transducers, strain gauges and sonomicrometry crystals; digital particle image velocimetry; and oxygen consumption measurements. New closedloop physiological preparations in fish may offer an important intermediate approach between ideally complete and isolatedstructure experiments (Tytell et al, 2014).…”