A complete biomechanical model of Hydra contractile behaviors, from neural drive to muscle to movement

Abstract

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. To achieve this, we have built a neuromechanical model of Hydra ’s fluid-filled hydrostatic skeleton, showing how drive by neuronal activity activates distinct patterns of muscle activity and body column biomechanics. 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 by 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 timescale kinetics observed in muscle activation and the engagement of ectodermal and endodermal muscles 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.

Microbes as part of ancestral neuronal circuits: Bacterial produced signals affect neurons controlling eating behavior inHydra

“…Cnidarians emerge as informative models for neuroscience, as they have surprisingly complex neuronal circuits and enable the study of neuronal activity in complete organisms lacking a centralized nervous system 20,26,54,55 . Neuronal control of behavior in cnidarians is dispersed and control takes place in neuronal subpopulations.…”

Nonlinear elasticity and short-range mechanical coupling govern the rate and symmetry of mouth opening in Hydra

“…While transgenic Hydra lines exist for imaging myonemes in vivo [9], the large-scale tissue deformation of mouth opening prevents the resolution of individual myonemes (electronic supplementary material, figure S2). However, because Hydra's epitheliomuscular cells require intracellular calcium (Ca 2+ ) for contraction, we can visualize the spatio-temporal pattern of calcium in the epithelial tissue using genetically encoded Ca 2+ indicators (GCaMP6s) and thus obtain the spatio-temporal pattern of active contractile forces [10][11][12]. This allowed us to determine whether the initial active forces are localized within a specific region of the head.…”

“…Mouth opening was induced via exposure to quinine or reduced glutathione [1,14], which bind to receptors in sensory neurons [15,16]. The neurons are thought to activate epithelial cell contraction using neuropeptides [12,17,18]. Upon stimulation, variations in Ca 2+ signalling across the head were observed (electronic supplementary material, figure S3).…”

A new look at the architecture and dynamics of theHydranerve net

“…The results showed that both ectodermal and endodermal epithelial cells responded simultaneously to activity of the CB circuit. Since there are no nerve cell connections between the ectoderm and the endoderm (see above), they postulated (Wang et al, 2023) that the ectodermal epitheliomuscle cells activate endodermal epitheliomuscle cells directly via gap junction connections across the mesoglea (Hand and Gobel, 1972). This conclusion is consistent with our findings.…”