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Cited by 20Marine Invertebrate Physiology and EcologyIon channel regulation and functionPlant and Biological Electrophysiology Studies

Electrogenesis in the lower Metazoa and implications for neuronal integration

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Meech, Robert W.·2015·Journal of Experimental Biology
DOI 10.1242/jeb.111955PMC PMC4334145
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Abstract

Electrogenic communication appears to have evolved independently in a variety of animal and plant lineages. Considered here are metazoan cells as disparate as the loose three-dimensional parenchyma of glass sponges, the two-dimensional epithelial sheets of hydrozoan jellyfish and the egg cell membranes of the ctenophore Beroe ovata, all of which are capable of generating electrical impulses. Neuronal electrogenesis may have evolved independently in ctenophores and cnidarians but the dearth of electrophysiological data relating to ctenophore nerves means that our attention is focused on the Cnidaria, whose nervous systems have been the subject of extensive study. The aim here is to show how their active and passive neuronal properties interact to give integrated behaviour. Neuronal electrogenesis, goes beyond simply relaying 'states of excitement' and utilizes the equivalent of a set of basic electrical 'apps' to integrate incoming sensory information with internally generated pacemaker activity. A small number of membrane-based processes make up these analogue applications. Passive components include the decremental spread of current determined by cellular anatomy; active components include ion channels specified by their selectivity and voltage dependence. A recurring theme is the role of inactivating potassium channels in regulating performance. Although different aspects of cnidarian behaviour are controlled by separate neuronal systems, integrated responses and coordinated movements depend on interactions between them. Integrative interactions discussed here include those between feeding and swimming, between tentacle contraction and swimming and between slow and fast swimming in the hydrozoan jellyfish Aglantha digitale.

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  • The anatomical simplicity of the cnidarian nervous system masks neurophysiological specializations including bidirectional chemical synapses, peptide-gated channels, rapid nematocyst discharge, and axons with two kinds of impulse propagation.

    “The anatomical simplicity of the cnidarian nervous system masks some remarkable neurophysiological specializations [35] including, for example, bidirectional chemical synapses (Figure 2) [36,37], signaling by a diversity of peptide-gated channels [38–40], the rapid discharge of nematocysts (Figure 2) [41] and axons with two kinds of impulse propagation [35,42–45].”

    From Back to the Basics: Cnidarians Start to Fire (2017) · cites this paper as [35]

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Authors
Meech, R. W.
Affiliations
University of Bristol (GB)
Corresponding author
Meech, Robert W.
ORCID
Meech, Robert W.
Venue
Journal of Experimental Biology
Publisher
The Company of Biologists
Published
2015-02-15
Volume
218
Issue
4
Pages
537-550
ISSN
  • 0022-0949 (ISSN-L)
  • 1477-9145
DOI
10.1242/jeb.111955
PMC
PMC4334145
OpenAlex
W2110547545
Cited by
20
References
8
Citations by year
2026: 1 · 2025: 1 · 2024: 5 · 2023: 1 · 2022: 1 · 2021: 3 · 2020: 1 · 2019: 2 · 2017: 1 · 2016: 3 · 2015: 1
FWCI
0.21
Type
journal article
Language
en
Open access
Locations
  • Journal of Experimental Biology (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • Bristol Research (University of Bristol) (publishedVersion)
  • Explore Bristol Research (submittedVersion)
Funders
  • National Science Foundation
  • Wellcome Trust
Topics
  • Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant and Biological Electrophysiology Studies
Keywords
neural integration, cnidarian nervous system, Hexactinellida, hydrozoan jellyfish, pacemaker activity, ion channels, nervous system evolution
MeSH terms
Animals, Cell Membrane, Cnidaria, Ion Channels, Nervous System Physiological Phenomena, Porifera, Swimming, Ctenophora, Electrophysiological Phenomena

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