Neurons that connect without synapses

Evolutionarily, which animal came first? Sponges or comb jellies? Concerning the evolution of animal nervous systems, it had been quite well accepted that all neurons connect to each other with synapses, and that the nervous system arose only once in evolutionary history and was never lost. But this “consensus” opinion has now been challenged [see attached article & editorial]. A lay description of this study was posted in GEITP on 24 Apr 2023; attached is the scientific article.

Authors provide new information on the structure of the nervous system of ctenophores — marine invertebrates commonly known as comb jellies. All living animals belong to one of five groups: Porifera (sponges) and Placozoa (small, disc-shaped animals distributed in warm ocean water) lack neurons; Ctenophora (comb jellies) and Cnidaria (corals, medusa jellyfish, siphonophores, and others) have “nerve nets” — (nervous systems with neurons arranged into diffuse networks); and Bilateria (which contains most animal species, including humans and other vertebrates, arthropods, and many other invertebrates; they have left-right, head-tail and dorsal ventral orientations) includes some animals with a nerve net, but most have a central nervous system.

The consensus explanation for this nervous system diversity is that these organisms represent ancestral steps in the increase of nervous system complexity (i.e., sponges diverged first from other animals, before the origin of the nervous system, and nervous system complexity increased in a ratchet-like manner in other animals). Then, surprisingly, the first sequences of Porifera and Placozoa genomes were found to contain genes that were previously thought to be specific to nervous system function. A closer look in placozoans found that they have gland cells that secrete neurosecretory components.

More recently, single-cell expression analyses revealed that some sponge cells communicate through structures that resemble synapses; this made it clear that neuron morphology and neuron signaling molecules have different distributions across animals. Consequently, traditional hypotheses about the earliest relationships in the animal phylogeny have been challenged. Some phylogenomic analyses support Porifera as the sister group to all other animals; but there is growing evidence that Ctenophora is the sister group to all other animals — indicating that some nervous system features arose independently in ctenophores or that some nervous system components were lost in sponges. This evidence further challenges the historically accepted consensus of stepwise increments in nervous system complexity through the course of animal evolution.

The current study [attached] goes right to the heart of these questions. Authors report that the ctenophore nerve net is unlike the nervous systems of other animals. Authors used serial block face scanning electron microscopy to make 3-dimensional ultrastructural reconstructions of a ctenophore subepithelial nerve net; they observed that this nerve net is not formed by neurons connecting to each other with synapses. Instead, the processes of the neurons are directly fused to each other, forming a syncytial continuum. There are synapses elsewhere, including where the nerve net connects to effector cells, but the subepithelial nerve net itself is not formed with synaptic connections. It was never a question, then, of whether all animal nervous systems conform to the neuronal doctrine or the reticulate theory — but rather of describing which animals conform to which theory.   😊


Science, 21 Apr 2023; 380: 293-297 & editorial pp 241-242

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