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From nerve net to nerve ring, nerve cord and brain — evolution of the nervous system

Abstract

The puzzle of how complex nervous systems emerged remains unsolved. Comparative studies of neurodevelopment in cnidarians and bilaterians suggest that this process began with distinct integration centres that evolved on opposite ends of an initial nerve net. The 'apical nervous system' controlled general body physiology, and the 'blastoporal nervous system' coordinated feeding movements and locomotion. We propose that expansion, integration and fusion of these centres gave rise to the bilaterian nerve cord and brain.

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Figure 1: Animal phylogeny.
Figure 2: Comparison of neurodevelopment in the frog, annelid and sea anemone.
Figure 3: A hypothetical scenario of nervous system evolution.
Figure 4: Development of gastrula-like body forms with an ectodermal nerve net in cnidarians and ctenophores.
Figure 5: The ANS in cnidarians and bilaterians.
Figure 6: Molecular regions in the BNS.
Figure 7: WNT and HH signalling in cnidarians and vertebrates.

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Acknowledgements

The authors thank K. Achim, E. Benito-Gutierrez, P. Bertucci, T. Brunet, T. Chartier, A. Lauri, H. Martinez Vergara, D. Puga, S. Rohr and P. Vopalensky for their comments and suggestions on earlier versions of the manuscript, and the entire Arendt laboratory for continuous exciting discussions.

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Glossary

Anthozoans

A group of cnidarians with bilateral symmetry including the sea anemones, corals and sea pens. Anthozoans have a biphasic life cycle involving swimming planula larvae and adult polyps with tentacles; they do not have a medusa stage.

Apical nervous system

(ANS). An integrative nervous centre developing from the apical plate and composed of sensory-neurosecretory cells and of sensory neurons and interneurons projecting into the apical neuropil.

Apical neuropil

A neuropil located at the apical pole of cnidarian larvae and bilaterian primary larvae, underneath the 'apical organ'. The apical neuropil is formed by neurons that belong to the 'apical nervous system' and receives paracrine input from the apical organ.

Bilaterians

A group of animals with bilateral symmetry, including the vertebrates, cephalochordates, sea urchins, insects, annelids and molluscs. Characteristic features relevant for nervous system evolution include a through-gut with mouth and anus, commissural interneurons, a chimeric brain and paired sensory organs.

Blastoporal nervous system

(BNS). An integrative nervous centre developing from ectoderm surrounding the blastopore.

Cerianthids

A group of tube-dwelling cnidarian polyps that branched off early in the cnidarian tree and are thus especially informative about early cnidarian conditions

Cnidarians

A group of animals characterized by their name-giving stinging cells (cnidocytes) and simple gut with a single opening; the cnidarians include jellyfishes, corals and sea anemones. Adults in this group are polyps and/or medusae.

Ctenophore

One of a group of jelly-like animals with bilateral symmetry that spend their entire life swimming in the water, propelled by cilia in a comb-like arrangement; they have a nerve net and a primitive gut. The phylogenetic position of this group is not settled.

Homology

Traits present in distinct groups that are thought to be inherited from a similar trait in their last common ancestor. Homologous traits often share specific internal structures, similar positions within the body and continuity of phylogenetic distribution.

Medusozoans

A group of cnidarians that form medusae as part of their adult life cycle. Medusozoans include the stinging jellyfish, box jellyfish and the developmental model systems Clytia hemisphaerica and Hydra Spp.

Nerve cords

The most-prominent longitudinal part of the central nervous system in bilaterian animals, extending along the animal's anterior–posterior axis. In vertebrates, the nerve cords correspond to the hindbrain and spinal cord.

Nerve rings

In Cnidaria, concentrations of neurons and axons around the pharynx or interconnecting the rhopalia.

Neuralia

A group of animals that includes the Cnidaria, Ctenophora and Bilateria but excludes more basal metazoans, such as the sponges (the Porifera). The defining feature of this group is the presence of neurons.

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Arendt, D., Tosches, M. & Marlow, H. From nerve net to nerve ring, nerve cord and brain — evolution of the nervous system. Nat Rev Neurosci 17, 61–72 (2016). https://doi.org/10.1038/nrn.2015.15

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