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Increasing Viscosity Helps Explain Locomotor Control in Swimming Polypterus senegalus

ABSTRACT: Synopsis Locomotion relies on the successful integration of sensory information to adjust brain commands and basic motor rhythms created by central pattern generators. It is not clearly understood how altering the sensory environment impacts control of locomotion. In an aquatic environment, mechanical sensory feedback to the animal can be readily altered by adjusting water viscosity. Computer modeling of fish swimming systems shows that, without sensory feedback, high viscosity systems dampen kinematic output despite similar motor control input. We recorded muscle activity and kinematics of six Polypterus senegalus in four different viscosities of water from 1 cP (normal water) to 40 cP. In high viscosity, P. senegalus exhibit increased body curvature, body wave speed, and body and pectoral fin frequency during swimming. These changes are the result of increased muscle activation intensity and maintain voluntary swimming speed. Unlike the sensory-deprived model, intact sensory feedback allows fish to adjust swimming motor control and kinematic output in high viscous water but maintain typical swimming coordination.

SUBMITTER: Lutek K

PROVIDER: S-EPMC8414443 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Amphibious fishes moving from water to land experience continuous changes in environmental forces. How these subtle changes impact behavioural transitions cannot be resolved by comparisons of aquatic and terrestrial locomotion. For example, aquatic and terrestrial locomotion appear distinct in the actinopterygian fish Polypterus senegalus; however, it is unclear how gradual water level changes influence the transition between these locomotor behaviours. We tested the hypothesis in P. senegalus that swimming and walking are part of an incremental continuum of behaviour and muscle activity across the environmental transition from water to land rather than two discrete behaviours, as proposed by previous literature. We exposed P. senegalus to discrete environments from fully aquatic to fully terrestrial while recording body and pectoral fin kinematics and muscle activity. Anterior axial red muscle effort increases as water depth decreases; however, a typical swimming-like anterior-to-posterior wave of axial red muscle activity is always present, even during terrestrial locomotion, indicating gradual motor control changes. Thus, walking appears to be based on swimming-like axial muscle activity whereas kinematic differences between swimming and walking appear to be due to mechanical constraints. A discrete change in left-right pectoral fin coordination from in-phase to out-of-phase at 0.7 body depths relies on adductor muscle activity with a similar duty factor and adductor muscle effort that increases gradually as water depth decreases. Thus, despite distinct changes in kinematic timing, neuromuscular patterning is similar across the water depth continuum. As the observed, gradual increases in axial muscle effort reflect muscle activity changes between aquatic and terrestrial environments observed in other elongate fishes, a modified, swimming-like axial muscle activity pattern for terrestrial locomotion may be common among elongate amphibious fishes.

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Increasing Viscosity Helps Explain Locomotor Control in Swimming Polypterus senegalus

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