Alternative neural systems: What is a neuron? (Ctenophores, sponges and placozoans)

How to make a neuron, a synapse, and a neural circuit? Is there only one 'design' for a neural architecture with a universally shared genomic blueprint across species? The brief answer is No. Four early divergent lineages from the nerveless common ancestor of all animals independently evolved distinct neuroid-type integrative systems. One of these is a subset of neural nets in comb jellies with unique synapses; the second lineage is the well-known Cnidaria + Bilateria; the two others are non-synaptic neuroid systems in sponges and placozoans. By integrating scRNA-seq and microscopy data, we revise the definition of neurons as synaptically-coupled polarized and highly heterogenous secretory cells at the top of behavioral hierarchies with learning capabilities. This physiological (not phylogenetic) definition separates 'true' neurons from non-synaptically and gap junction-coupled integrative systems executing more stereotyped behaviors. Growing evidence supports the hypothesis of multiple origins of neurons and synapses. Thus, many non-bilaterian and bilaterian neuronal classes, circuits or systems are considered functional rather than genetic categories, composed of non-homologous cell types. In summary, little-explored examples of convergent neuronal evolution in representatives of early branching metazoans provide conceptually novel microanatomical and physiological architectures of behavioral controls in animals with prospects of neuro-engineering and synthetic biology.

Automated summary

By studying the evolution of neural structures in early branching animals, we have discovered multiple origins of neural architecture and revised the definition of neurons. These findings offer new perspectives for neuro-engineering and synthetic biology.