Increasing Viscosity Helps Explain Locomotor Control in Swimming Polypterus senegalus

Abstract

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 show 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 wavespeed 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.

Behaviour and muscle activity across the aquatic–terrestrial transition in Polypterus senegalus

“…A swimming-like axial motor pattern appears to be sufficient to produce walking in P. senegalus , which suggests the utility (and possible evolutionary advantage) of a single pattern that can be used in several environments. Polypterus senegalus also use modified swimming axial muscle activity in high viscosity ( Lutek and Standen, 2021 ). However, in such high-resistance aquatic environments, they increase posterior body muscle effort (rather than anterior body muscle effort as water depth decreases), suggesting different modifications of the base swimming pattern in response to novel aquatic and terrestrial environments.…”

“…Pectoral fin frequency was calculated based on the pectoral fin stroke as defined above. Pectoral fin angle was defined as the angle between the nose, back of skull and tip of fin lobe (as in Foster et al, 2018 , and Lutek and Standen, 2021 ). Both fin RoM and nose elevation showed no differences in magnitude between the left and right side; thus, a mean value for each trial calculated from both left- and right-side data was used in the final analysis.…”

“…Two-pronged fine wire hook electrodes were fashioned from 0.051 mm bi-filament wire (California Fine Wire Company, Grover Beach, CA, USA) and implanted percutaneously using 27-gauge needles (Sigma-Aldrich, St Louis, MO, USA). Electrodes were implanted in the middle of the pectoral fin adductor, in five locations spaced evenly along the left-side red body muscle between the pectoral fin lobe and anal fin (19.8±0.73% BL, 33.1±0.51% BL, 42.8±0.69% BL, 57.4±0.39% BL and 67.4±0.74% BL), and opposite positions 2 and 4 on the right side of the body (as in Lutek and Standen, 2021 ). Following the placement of all electrodes, the wires were sutured to the dorsal spines to reduce strain on the electrodes.…”

Sensorimotor control of swimming Polypterus senegalus is preserved during sensory deprivation conditions across altered environments

“…When the viscosity of the fluid is increased in the model without altering muscle activation, a decrease in tail amplitude and wave speed resulting in a reduced swimming speed is observed ( Tytell et al, 2010 ). The opposite kinematic response is seen in behavioural testing of living animals; swimming fish react to high-viscosity environments by increasing their lateral displacement as well as their tail and fin beat frequency to either maintain or increase swimming speed ( Horner and Jayne, 2008 ; Lutek and Standen, 2021 ). This suggests that sensory feedback is used to actively adjust swimming form in viscous water, but it is as yet unclear which senses are involved in this response.…”

New Data on Nephron Microanatomy and Ultrastructure of Senegal Bichir (Polypterus senegalus)

“…Polypterids are characterized by the presence of asymmetric dilobed lungs, which are similar in essential features to the lungs of vertebrates, as well as an adapted system for regulating the excretion of metabolites to the conditions of temporary stay in the ground-air environment [ 6 , 7 ]. The use of the body and pectoral fins of Polypterus senegalus for movement along terrestrial substrates and the formation of tetrapod-like gait during seasonal migrations from drying temporary spawning lakes to feeding rivers has been proven [ 8 , 9 ].…”