A functional network model for body column neural connectivity in Hydra

Abstract

Hydra is a non-senescent animal with a relatively small number of cell types and overall low structural complexity, but a surprisingly rich behavioral repertoire. The main drivers of Hydra s behavior are neurons that are arranged in two nerve nets comprising several distinct neuronal populations. Among these populations is the ectodermal nerve net N3 which is located throughout the animal. It has been shown that N3 is necessary and sufficient for the complex behavior of somersaulting and is also involved in Hydra feeding behavior. Despite being a behavioral jack-of-all-trades, there is insufficient knowledge on the coupling structure of neurons in N3, its connectome, and its role in activity propagation and function. We construct a model connectome for the part of N3 located on the body column. Using experimental data on the placement of neuronal somata and the spatial dimensions of the body column, we show that a generative network model combining non-random placement of neuronal somata and the preferred orientation of primary neurites yields good agreement with experimentally observed distributions of connection distances, connection angles, and the number of primary neurites per neuron. Having validated the N3 connectome model in this fashion, we place a simple excitable dynamical model on each node of the body column network and show that it generates directed, short-lived, fast propagating patterns of activity. In addition, by slightly changing the parameters of the dynamical model, the same structural network can also generate persistent activity. Finally, we use a neuromorphic circuit based on the Morris-Lecar model to show that the same structural connectome can, in addition to through-conductance with biologically plausible time scales, also host a dynamical pattern related to the complex behavioral pattern of somersaulting. We speculate that such different dynamical regimes act as dynamical substrates for the different functional roles of N3, allowing Hydra to exhibit behavioral complexity with a relatively simple nervous system that does not possess modules or hubs.