A fundamental breakthrough in neurobiology has been the formulation of the neuron doctrine by Santiago Ramón y Cajal, which stated that the nervous system is composed of discrete cells. Electron microscopy later confirmed the doctrine and allowed the identification of synaptic connections. In this work, we used volume electron microscopy and three-dimensional reconstructions to characterize the nerve net of a ctenophore, a marine invertebrate that belongs to one of the earliest-branching animal lineages. We found that neurons in the subepithelial nerve net have a continuous plasma membrane that forms a syncytium. Our findings suggest fundamental differences of nerve net architectures between ctenophores and cnidarians or bilaterians and offer an alternative perspective on neural network organization and neurotransmission.
SummaryA fundamental breakthrough in neurobiology has been the formulation of the neuron doctrine by Santiago Ramón y Cajal, which states that the nervous system is composed of discrete individual cells. Electron microscopy later confirmed the doctrine and allowed the identification of synaptic connections. Here we use volume electron microscopy and 3D reconstructions to characterize the nerve net of a cydippid-phase ctenophore, belonging to one of the earliest-branching animal lineages. We found that neurons of its subepithelial nerve net do not follow Cajal’s neuron doctrine but instead show a continuous plasma membrane forming a syncytium. This is more similar to the reticulate theory of the nervous system put forward by Camillo Golgi. Additionally, we were able to identify new sensory cell types and describe simple neuro-sensory circuits for cydippid-phase ctenophores. Together with the ctenophore-specific synaptic architecture and the presence of an extensive repertoire of lineage-specific neuropeptides our morphological data provide substantial evidence for the independent evolution of the nervous system of ctenophores and the remaining animals.
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