Interactions between internal forces, body stiffness, and fluid environment in a neuromechanical model of lamprey swimming

Eric Tytell, Chia-Yu Hsu, Thelma L. Williams, Avis H. Cohen, Lisa Fauci

Proceedings of the National Academy of Sciences · 2010 · 303 citations · 35 references

Concepts

TL;DR

Animal movements arise from the complex interplay of muscular forces, body inertial, elastic, and damping properties, and environmental reaction forces, producing emergent motion. The study develops a computational lamprey model to investigate how body stiffness, muscle activation, and fluid environment influence swimming. The model couples Navier–Stokes fluid dynamics with an actuated elastic body using an immersed boundary framework, enabling full fluid–structure interaction at a realistic Reynolds number. Results show that the same muscle activation can yield different kinematics based on body stiffness, with distinct optimal stiffness values for peak acceleration versus steady speed, and that higher tail‑beat frequencies generate negative muscle work that may enhance energy efficiency, suggesting that fish can tune stiffness to optimize performance.

Abstract

Animal movements result from a complex balance of many different forces. Muscles produce force to move the body; the body has inertial, elastic, and damping properties that may aid or oppose the muscle force; and the environment produces reaction forces back on the body. The actual motion is an emergent property of these interactions. To examine the roles of body stiffness, muscle activation, and fluid environment for swimming animals, a computational model of a lamprey was developed. The model uses an immersed boundary framework that fully couples the Navier–Stokes equations of fluid dynamics with an actuated, elastic body model. This is the first model at a Reynolds number appropriate for a swimming fish that captures the complete fluid-structure interaction, in which the body deforms according to both internal muscular forces and external fluid forces. Results indicate that identical muscle activation patterns can produce different kinematics depending on body stiffness, and the optimal value of stiffness for maximum acceleration is different from that for maximum steady swimming speed. Additionally, negative muscle work, observed in many fishes, emerges at higher tail beat frequencies without sensory input and may contribute to energy efficiency. Swimming fishes that can tune their body stiffness by appropriately timed muscle contractions may therefore be able to optimize the passive dynamics of their bodies to maximize peak acceleration or swimming speed.

References

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