Cargando…

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 dist...

Descripción completa

Detalles Bibliográficos
Autores principales: Moroz, Leonid L., Romanova, Daria Y.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9816575/
https://www.ncbi.nlm.nih.gov/pubmed/36619868
http://dx.doi.org/10.3389/fcell.2022.1071961
_version_ 1784864566308503552
author Moroz, Leonid L.
Romanova, Daria Y.
author_facet Moroz, Leonid L.
Romanova, Daria Y.
author_sort Moroz, Leonid L.
collection PubMed
description 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.
format Online
Article
Text
id pubmed-9816575
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-98165752023-01-07 Alternative neural systems: What is a neuron? (Ctenophores, sponges and placozoans) Moroz, Leonid L. Romanova, Daria Y. Front Cell Dev Biol Cell and Developmental Biology 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. Frontiers Media S.A. 2022-12-23 /pmc/articles/PMC9816575/ /pubmed/36619868 http://dx.doi.org/10.3389/fcell.2022.1071961 Text en Copyright © 2022 Moroz and Romanova. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cell and Developmental Biology
Moroz, Leonid L.
Romanova, Daria Y.
Alternative neural systems: What is a neuron? (Ctenophores, sponges and placozoans)
title Alternative neural systems: What is a neuron? (Ctenophores, sponges and placozoans)
title_full Alternative neural systems: What is a neuron? (Ctenophores, sponges and placozoans)
title_fullStr Alternative neural systems: What is a neuron? (Ctenophores, sponges and placozoans)
title_full_unstemmed Alternative neural systems: What is a neuron? (Ctenophores, sponges and placozoans)
title_short Alternative neural systems: What is a neuron? (Ctenophores, sponges and placozoans)
title_sort alternative neural systems: what is a neuron? (ctenophores, sponges and placozoans)
topic Cell and Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9816575/
https://www.ncbi.nlm.nih.gov/pubmed/36619868
http://dx.doi.org/10.3389/fcell.2022.1071961
work_keys_str_mv AT morozleonidl alternativeneuralsystemswhatisaneuronctenophoresspongesandplacozoans
AT romanovadariay alternativeneuralsystemswhatisaneuronctenophoresspongesandplacozoans