Neural versus alternative integrative systems: molecular insights into origins of neurotransmitters
Open accessAbstract
Transmitter signalling is the universal chemical language of any nervous system, but little is known about its early evolution. Here, we summarize data about the distribution and functions of neurotransmitter systems in basal metazoans as well as outline hypotheses of their origins. We explore the scenario that neurons arose from genetically different populations of secretory cells capable of volume chemical transmission and integration of behaviours without canonical synapses. The closest representation of this primordial organization is currently found in Placozoa, disk-like animals with the simplest known cell composition but complex behaviours. We propose that injury-related signalling was the evolutionary predecessor for integrative functions of early transmitters such as nitric oxide, ATP, protons, glutamate and small peptides. By contrast, acetylcholine, dopamine, noradrenaline, octopamine, serotonin and histamine were recruited as canonical neurotransmitters relatively later in animal evolution, only in bilaterians. Ligand-gated ion channels often preceded the establishment of novel neurotransmitter systems. Moreover, lineage-specific diversification of neurotransmitter receptors occurred in parallel within Cnidaria and several bilaterian lineages, including acoels. In summary, ancestral diversification of secretory signal molecules provides unique chemical microenvironments for behaviour-driven innovations that pave the way to complex brain functions and elementary cognition. This article is part of the theme issue ‘Basal cognition: multicellularity, neurons and the cognitive lens'.
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“This, on many accounts, was the impetus for the evolution of modern neurons ([10]; although simpler forms predate the Cambrian [11]), which coordinated muscles across larger bodies [12].”
- Authors
- Moroz, L. L., Romanova, D. Y., & Kohn, A. B.
- Affiliations
- University of Florida (US)
- Russian Academy of Sciences (RU)
- Corresponding author
- Moroz, Leonid L.
- Venue
- Philosophical Transactions of the Royal Society B
- Publisher
- The Royal Society
- Published
- 2021-02-08
- Volume
- 376
- Issue
- 1821
- Pages
- 20190762-20190762
- ISSN
- 0962-8436 (ISSN-L)
- 1471-2970
- PMC
- PMC7935107
- OpenAlex
- W3127282149
- Cited by
- 130
- References
- 271
- Citations by year
- 2026: 13 · 2025: 26 · 2024: 26 · 2023: 32 · 2022: 11 · 2021: 22
- FWCI
- 2.76
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- Locations
- Philosophical Transactions of the Royal Society B Biological Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation (1146575, 1557923, 1548121 and 1645219)
- National Institute of Health (R01NS114491)
- Topics
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Keywords
- Placozoa, secretory cells, basal metazoans, nitric oxide, ATP, protons, glutamate, small peptides, acetylcholine, dopamine, norepinephrine, octopamine, serotonin, histamine, ligand-gated ion channels, neurotransmitter receptors, Cnidaria, acoels, basal cognition
- MeSH terms
- Animals, Cell Communication, Signal Transduction, Neurotransmitter Agents, Evolution, Molecular, Placozoa
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