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

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. 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.

Multiple neuronal networks coordinate Hydra mechanosensory behavior

“…To further test our hypothesis, we created a transgenic Hydra strain that expresses the calcium indicator GCaMP7b (under the EF1ɑ promoter, see Materials and methods) in the endodermal epitheliomuscular cells. During body contractions, both endodermal and ectodermal epitheliomuscular cells are co-activated ( Wang et al, 2020 ). With this transgenic line we measured contraction pulses and contraction bursts by averaging calcium activity in all epitheliomuscular cells ( Figure 2—figure supplements 3 and 5 ).…”

Integrative Neuroscience ofParamecium, a “Swimming Neuron”

“…Computational neuroethology is a subfield of computational neuroscience focusing on the modeling of autonomous behavior ( Beer, 1990 ), which has been investigated in particular artificial organisms ( Beer and Gallagher, 1992 ) and robots ( Webb, 2001 ). More recently, integrated models of C. elegans ( Izquierdo and Beer, 2016 ; Cohen and Denham, 2019 ), Hydra ( Dupre and Yuste, 2017 ; Wang et al, 2020 ), and jellyfish Aurelia aurita ( Pallasdies et al, 2019 ) have been developed. Those model organisms have certain obvious advantages over Paramecium , namely the fact that they have a nervous system, with interacting neurons.…”

“…Nevertheless, even in this more favorable situation, developing functional and empirically valid neuromechanical models of C. elegans remains very challenging. Two other recently introduced model organisms for this type of integrative work are Hydra , which has a few thousand neurons and the advantage of being transparent ( Dupre and Yuste, 2017 ; Wang et al, 2020 ), and jellyfish Aurelia aurita ( Pallasdies et al, 2019 ). Here, I will present a model organism that is significantly simpler as it consists of a single “neuron.”…”

Functional modules within a distributed neural network control feeding in a model medusa

“…An additional opportunity for comparative neuroscience would be between Clytia and Hydra, which is also emerging as a systems neuroscience model (Dupre and Yuste, 2017;Szymanski and Yuste, 2019;Badhiwala et al, 2020;Wang et al, 2020;Bosch et al, 2017).…”