The role of curvature feedback in the energetics and dynamics of lamprey swimming: A closed-loop model

PLoS Comput Biol. 2018 Aug 17;14(8):e1006324. doi: 10.1371/journal.pcbi.1006324. eCollection 2018 Aug.

Abstract

Like other animals, lampreys have a central pattern generator (CPG) circuit that activates muscles for locomotion and also adjusts the activity to respond to sensory inputs from the environment. Such a feedback system is crucial for responding appropriately to unexpected perturbations, but it is also active during normal unperturbed steady swimming and influences the baseline swimming pattern. In this study, we investigate different functional forms of body curvature-based sensory feedback and evaluate their effects on steady swimming energetics and kinematics, since little is known experimentally about the functional form of curvature feedback. The distributed CPG is modeled as chains of coupled oscillators. Pairs of phase oscillators represent the left and right sides of segments along the lamprey body. These activate muscles that flex the body and move the lamprey through a fluid environment, which is simulated using a full Navier-Stokes model. The emergent curvature of the body then serves as an input to the CPG oscillators, closing the loop. We consider two forms of feedback, each consistent with experimental results on lamprey proprioceptive sensory receptors. The first, referred to as directional feedback, excites or inhibits the oscillators on the same side, depending on the sign of a chosen gain parameter, and has the opposite effect on oscillators on the opposite side. We find that directional feedback does not affect beat frequency, but does change the duration of muscle activity. The second feedback model, referred to as magnitude feedback, provides a symmetric excitatory or inhibitory effect to oscillators on both sides. This model tends to increase beat frequency and reduces the energetic cost to the lamprey when the gain is high and positive. With both types of feedback, the body curvature has a similar magnitude. Thus, these results indicate that the same magnitude of curvature-based feedback on the CPG with different functional forms can cause distinct differences in swimming performance.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Biomechanical Phenomena / physiology
  • Central Pattern Generators / physiology*
  • Computer Simulation
  • Feedback
  • Lampreys / physiology*
  • Locomotion / physiology
  • Models, Biological
  • Muscles
  • Nerve Net / physiology
  • Spinal Cord / physiology
  • Swimming / physiology*

Grants and funding

This work was funded by the National Science Foundation https://www.nsf.gov under grant numbers DBI-RCI 1062052 (LFJ) and DMS-1312987 (EDT) and The Army Research Office http://www.arl.army.mil under grant number W911NF-13-1-0289 (LJF). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.