Assembly of a functional neuronal circuit in embryos of an ancestral metazoan is influenced by temperature and the microbiome.

Abstract

Understanding how neural populations emerge to give rise to behavior is a major goal in neuroscience. Here, we explore the self-assembly of neural circuits in <i>Hydra</i>, an organism with a simple nervous system but no centralized information processing, to enhance the understanding of nervous system evolution. We define self-assembly as spontaneous organization of neurons into functional circuits without requiring a prespecified structural template. In this context, the N4 neuronal circuit, which we have previously found to be particularly important in the feeding of the animal, develops in embryos through activity-driven self-assembly, a process in which intrinsic calcium activity drives connectivity and synchronization among spatially distributed neurons over time. Gap junctions and vesicle-mediated communication between neuronal and non-neuronal cells drive rapid assembly, with the embryo's prospective oral region exhibiting the highest neuronal density. An artificial electrical circuit-based model as a biophysically inspired simulation demonstrates dynamic increases in synchronization over time, along with predictions for selective dynamic adaptions of connections. Environmental factors, like temperature and an absent microbiome, modify neural architecture, suggesting the existence of a certain adaptability during neural development. We propose that these fundamental features originated in the last common bilaterian ancestor, supporting the hypothesis that the basic architecture of the nervous system is universal. Since in the natural habitat of <i>Hydra</i> both temperature fluctuations and changes in the microbiome can occur, our work not only illuminates a fundamental developmental process but also may guide environmental and evolutionary studies by explaining how organisms adapt to environmental variations.