From Single Neurons to Behavior in the Jellyfish<i>Aurelia aurita</i>

Pallasdies, Fabian; Goedeke, Sven; Braun, Wilhelm; Memmesheimer, Raoul-Martin

doi:10.1101/698548

Cited by 6 publications

(9 citation statements)

References 64 publications

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“…Even with the relatively simple nature of this distributed control mechanism, jellyfish manage to perform complicated maneuvers (21,27). Ultimately, the turn was initiated by a temporal mismatch in the contraction of opposite sides of the bell by controlling propagation of muscle contraction around bell.…”

Section: Discussionmentioning

confidence: 99%

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Neuromechanical wave resonance in jellyfish swimming

Hoover

Gemmell

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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For organisms to have robust locomotion, their neuromuscular organization must adapt to constantly changing environments. In jellyfish, swimming robustness emerges when marginal pacemakers fire action potentials throughout the bell’s motor nerve net, which signals the musculature to contract. The speed of the muscle activation wave is dictated by the passage times of the action potentials. However, passive elastic material properties also influence the emergent kinematics, with time scales independent of neuromuscular organization. In this multimodal study, we examine the interplay between these two time scales during turning. A three-dimensional computational fluid–structure interaction model of a jellyfish was developed to determine the resulting emergent kinematics, using bidirectional muscular activation waves to actuate the bell rim. Activation wave speeds near the material wave speed yielded successful turns, with a 76-fold difference in turning rate between the best and worst performers. Hyperextension of the margin occurred only at activation wave speeds near the material wave speed, suggesting resonance. This hyperextension resulted in a 34-fold asymmetry in the circulation of the vortex ring between the inside and outside of the turn. Experimental recording of the activation speed confirmed that jellyfish actuate within this range, and flow visualization using particle image velocimetry validated the corresponding fluid dynamics of the numerical model. This suggests that neuromechanical wave resonance plays an important role in the robustness of an organism’s locomotory system and presents an undiscovered constraint on the evolution of flexible organisms. Understanding these dynamics is essential for developing actuators in soft body robotics and bioengineered pumps.

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Section: Discussionmentioning

confidence: 99%

“…The resulting wave of muscular activation travels along the bell margin, yielding an asymmetrical contraction. Recent studies have incorporated network neural models to demonstrate the passage of action potentials in the MNN (27).…”

mentioning

confidence: 99%

Neuromechanical wave resonance in jellyfish swimming

Hoover

Gemmell

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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“…Models of hydrostatic skeletons are rare and have focused on muscular hydrostats, including leech (Wadepuhl and Beyn, 1989; Skierczynski et al, 1996) and octopus tentacles (Yekutieli et al, 2005) . Related work has explored the neural control of swimming in jellyfish (Pallasdies et al, 2019) ; in this case the animal is an open membrane and the model treats the hydrodynamic interaction with the surrounding fluid. We constructed our model using the COMSOL Multiphysics ® 5.3 package.…”

Section: Methodsmentioning

confidence: 99%

“…While there have been exciting developments of predictive models that incorporate musculoskeletal dy-namics in humans and an array of vertebrate and invertebrate animals (Daniel, 1995; Rajagopal et al, 2016; Delp and Loan, 2000; Ting and Chiel, 2017) , many are hampered by the inability to observe the system in its entirety, with simultaneous spatial and temporal patterns of neural activity, muscular activation and whole animal behavior. Small model systems pose the opportunity to develop relatively complete models of the transformations from neural activity to behavior, taking into account the biomechanics of the body (Kim et al, 2019; Pallasdies et al, 2019; Kim and Shlizer-man, 2020) . As an active medium, however, muscle tissue has its own dynamics that can contribute significantly to this transformation.…”

Section: Introductionmentioning

confidence: 99%

From neuron to muscle to movement: a complete biomechanical model ofHydracontractile behaviors

Wang

Swore

Sharma

et al. 2020

Preprint

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How does neural activity drive muscles to produce behavior? The recent development of genetic lines in Hydra that allow complete calcium imaging of both neuronal and muscle activity, as well as systematic machine learning quantification of behaviors, makes this small Cnidarian an ideal model system to understand and model the complete transformation from neural firing to body movements. As a first step to achieve this, we have built a biomechanical model of Hydra, incorporating its neuronal activity, muscle activity and body column biomechanics, incorporating its fluid-filled hydrostatic skeleton. Our model is based on experimental measurements of neuronal and muscle activity, and assumes gap junctional coupling among muscle cells and calcium-dependent force generation y muscles. With these assumptions, we can robustly reproduce a basic set of Hydra's behaviors. We can further explain puzzling experimental observations, including the dual kinetics observed in muscle activation and the different engagement of ecto- and endodermal muscle in different behaviors. This work delineates the spatiotemporal control space of Hydra movement and can serve as a template for future efforts to systematically decipher the transformations in the neural basis of behavior.

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“…Moreover, individual Sarsia are known to each use a unique set of contraction frequencies while swimming [62]. Katija et al 2015 [8] found that Sarsia tubulosa tend to swim about 2 bodylengths per contraction, with a range between [1,3.5] [56,57,[64][65][66][67][68][69][70][71][72] and have compared swimming performance over a large mechanospace, including bell stiffness and flexibility, muscular contraction strength and amplitude, and contraction frequencies. While many in situ and laboratory studies have been performed that quantify bell kinematics, velocity, acceleration, feeding (predation), and/or vortex wake structure [8,46,54,55,58,63,[73][74][75][76][77][78][79][80][81][82], computational studies are becoming increasingly more of an attractive alternative and/or complement for scientists, as they is easier (e.g., more cost and time efficient) to do widespread parameter studies.…”

Section: Introductionmentioning

confidence: 99%

Naut Your Everyday Jellyfish Model: Exploring How Tentacles and Oral Arms Impact Locomotion

Miles

Battista

2019

Fluids

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Jellyfish -majestic, energy efficient, and one of the oldest species that inhabits the oceans. It is perhaps the second item, their efficiency, that has captivated scientists to investigate their locomotive behavior for decades. Yet, no one has specifically explored the role that their tentacles and oral arms may have on their potential swimming performance, arguably the very features that give jellyfish their beauty while instilling fear into their prey (and beach-goers). We perform comparative in silico experiments to study how tentacle/oral arm number, length, placement, and density affect forward swimming speeds, cost of transport, and fluid mixing. An open source implementation of the immersed boundary method was used (IB2d) to solve the fully coupled fluid-structure interaction problem of an idealized flexible jellyfish bell with poroelastic tentacles/oral arms in a viscous, incompressible fluid. Overall tentacles/oral arms inhibit forward swimming speeds, by appearing to suppress vortex formation. Non-linear relationships between length and fluid scale (Reynolds Number) as well as tentacle/oral arm number, density, and placement are observed, illustrating that small changes in morphology could result in significant decreases in swimming speeds, in some cases by downwards of 400% between cases with to without tentacles/oral arms.

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From Single Neurons to Behavior in the JellyfishAurelia aurita

Cited by 6 publications

References 64 publications

Neuromechanical wave resonance in jellyfish swimming

Neuromechanical wave resonance in jellyfish swimming

From neuron to muscle to movement: a complete biomechanical model ofHydracontractile behaviors

Naut Your Everyday Jellyfish Model: Exploring How Tentacles and Oral Arms Impact Locomotion

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