The role of curvature feedback in the energetics and dynamics of lamprey swimming: A closed-loop model.
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 als...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2018-08-01
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| Series: | PLoS Computational Biology |
| Online Access: | http://europepmc.org/articles/PMC6114910?pdf=render |
| _version_ | 1811269808966074368 |
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| author | Christina L Hamlet Kathleen A Hoffman Eric D Tytell Lisa J Fauci |
| author_facet | Christina L Hamlet Kathleen A Hoffman Eric D Tytell Lisa J Fauci |
| author_sort | Christina L Hamlet |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-04-12T21:49:48Z |
| format | Article |
| id | doaj.art-697b58aff16f4eac9c50ee74c58ff2ab |
| institution | Directory Open Access Journal |
| issn | 1553-734X 1553-7358 |
| language | English |
| last_indexed | 2024-04-12T21:49:48Z |
| publishDate | 2018-08-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Computational Biology |
| spelling | doaj.art-697b58aff16f4eac9c50ee74c58ff2ab2022-12-22T03:15:32ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582018-08-01148e100632410.1371/journal.pcbi.1006324The role of curvature feedback in the energetics and dynamics of lamprey swimming: A closed-loop model.Christina L HamletKathleen A HoffmanEric D TytellLisa J FauciLike 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.http://europepmc.org/articles/PMC6114910?pdf=render |
| spellingShingle | Christina L Hamlet Kathleen A Hoffman Eric D Tytell Lisa J Fauci The role of curvature feedback in the energetics and dynamics of lamprey swimming: A closed-loop model. PLoS Computational Biology |
| title | The role of curvature feedback in the energetics and dynamics of lamprey swimming: A closed-loop model. |
| title_full | The role of curvature feedback in the energetics and dynamics of lamprey swimming: A closed-loop model. |
| title_fullStr | The role of curvature feedback in the energetics and dynamics of lamprey swimming: A closed-loop model. |
| title_full_unstemmed | The role of curvature feedback in the energetics and dynamics of lamprey swimming: A closed-loop model. |
| title_short | The role of curvature feedback in the energetics and dynamics of lamprey swimming: A closed-loop model. |
| title_sort | role of curvature feedback in the energetics and dynamics of lamprey swimming a closed loop model |
| url | http://europepmc.org/articles/PMC6114910?pdf=render |
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