Neuroid Conduction and the Evolution of Conducting Tissues
Abstract
Neuroid conduction, as here defined, refers to the propagation of electrical events in the membranes of non-nervous, nonmuscular cells. Examples from protistants, plants, and animals are described. In the dinoflagellate Noctiluca, propagated membrane depolarizations accompany the spread of the luminescent response, and local electrical changes are associated with tentacle movement. The ability of Noctiluca to conduct is attributable to its peculiar geometry, in which much of the cytoplasm is confined to a thin peripheral layer surrounding the flotation vacuole, a condition that permits local current flow to develop. Fresh-water algae of the family Characeae show propagated action potentials in which chloride efflux is the major event responsible for electrogenesis. Chloride spikes are presumed to be an adaptation to fresh water, following Grundfest (1966c). Among the higher plants, Dionaea and Mimosa provide examples of neuroid conduction. The former also possess trigger cells which function in an analagous way to certain animal receptors. In Mimosa there is evidence that the cells responsible for conduction of electrical events are located in the vascular bundles and that propagation requires simultaneous activation of a number of cells lying parallel in the bundles, as in mammalian smooth muscle. In both cases transmission from cell to cell is thought to be electrical via low-resistance pathways. In hydromedusae and siphonophores neuroid conduction occurs in the exumbrellar ectoderm and subumbrellar endoderm, the two layers being linked as a transmission pathway for excitation going to ectodermal smooth muscle systems. The "crumpling" behavior of medusae is transmitted by this system, but nervous components may be involved in the generation of the full response. Reverse locomotion in physonectid siphonophores (e.g., Nanomia) involves activation of neuroid pathways. In the siphonophore Hippopodius, neuroid conduction in the exumbrella is coupled to luminescent and blanching reactions. Neuroid conduction in all these forms provides a rapid and efficient method of information transfer. It is typically associated with the spread of protective and locomotory responses and is general rather than local in effect. The more complex and local responses are believed to be organized by the nervous system. In ctenophores, recent work suggests that propagation of the ciliary beat between cells of the comb plates is neuroid, and that inhibition of ciliary activity is nervous. Certain cells in the ciliated grooves seem to represent neurons in process of evolution from non-nervous, ciliated cells. In the pluteus larva of an echinoderm, coordination of ciliary reversal is associated with electrical signals apparently of non-nervous origin. In another larval form, that of the toad Xenopus, neuroid conduction has been demonstrated in the skin at a stage before the nerve supply reaches the skin, giving the tadpole a precocious capacity for response. As for the evolution of conduction, conducting tissues probably arose independently in many lines of evolution. Frequently the conducting tissue would have evolved from an epithelium in which the cells were connected by pathways serving for metabolic communication, the existence of these junctions predisposing the tissue for electrical transmission of propagated depolarizations. The effective conducting units in such tissues would have been groups of electrically coupled cells, rather than individual cells as such. In animals, nerve and muscle tissues are considered to have arisen from primitive myoepithelial sheets in which transmission occurred through low-resistance intercellular pathways. With the need for increased specificity in the conduction and response system, the original tight coupling between the cells would be replaced by specialized synapses. While electronic synapses have the potential to perform many integrative functions of the nervous system, chemical synapses have in general prevailed.
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Historically, attempts to understand nervous system function and early neural evolution have strongly emphasized input-output models.
“Historically, there has been a strong emphasis on IO models in attempts to understand nervous system function and early neural evolution.”
From An option space for early neural evolution (2015) · cites this paper as [4]
The presence of a well-developed nerve net correlates with the presence of basiepithelial muscle fibres directly innervated by nerve net neurons in cnidarians and ctenophores.
“The presence of a well-developed nerve net correlates with the presence of basiepithelial muscle fibres directly innervated by nerve net neurons, in cnidarians and in ctenophores [61,67,128,132,133,135,136,138–142].”
From Gastric pouches and the mucociliary sole: setting the stage for nervous system evolution (2015) · cites this paper as [67]
The first neurons arose by division of labour from mechanosensory-contractile ectochoanocytes.
“The prevalence of mechanosensory neurons with actin collar and cilium, multipolar ganglion cells and myoepithelial cells in extant nerve nets supports the idea that the first neurons arose by division of labour from mechanosensory-contractile ectochoanocytes, as hypothesized in the diversification scheme in figure 4f.”
From Gastric pouches and the mucociliary sole: setting the stage for nervous system evolution (2015) · cites this paper as [67]
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LOCOMOTION AND PROPAGATED SKIN IMPULSES IN SALPS (TUNICATA: THALIACEA)
Mackie, G. O., & Bone, Q. (1977) · Biological Bulletin · doi:10.2307/1540700 · Cited by 43 · see citing works
Self-citationChapman, D. M. F. (1974) · Elsevier eBooks · doi:10.1016/b978-0-12-512150-7.50006-2 · Cited by 72 · see citing works
Non-Nervous Conduction in Invertebrates and Embryos
Spencer, A. N. (1974) · American Zoologist · doi:10.1093/icb/14.3.917 · Cited by 42 · see citing works
Ros-Rocher, N., & Brunet, T. (2023) · Animal Cognition · doi:10.1007/s10071-023-01776-z · Cited by 41 · see citing works
“A deeper characterization of molecular and cellular sensors, processors and effectors in choanoflagellates might help inform and test “division-of-labor” scenarios for the origin of animal neuronal circuits (Mackie 1970; Arendt 2008).”
BackgroundConditions for minimal intelligence across eukaryota: a cognitive science perspective
Calvo, P., & Baluška, F. (2015) · Frontiers in Psychology · doi:10.3389/fpsyg.2015.01329 · Cited by 40 · see citing works
“As a matter of fact, so-called neuroid conduction (“the propagation of electrical events in of non-nervous, nonmuscular cells,” see Mackie, 1970, p. 319) takes place in protists and plants.”
BackgroundVidal, B., Gülez, B., Cao, W. X., Leyva‐Díaz, E., Reilly, M. B., Tekieli, T., & Hobert, O. (2022) · eLife · doi:10.7554/elife.76003 · Cited by 37 · see citing works
“Primitive nervous systems are generally thought to have emerged in the context of monolayers of epithelial cells, with individual cells in such layers specializing into primitive sensory motor- type neurons (Arendt, 2008; Mackie, 1970; Varoqueaux and Fasshauer, 2017).”
BackgroundA MYCOPLASMA-LIKE ARCHAEBACTERIUM POSSIBLY RELATED TO THE NUCLEUS AND CYTOPLASM OF EUKARYOTIC CELLS
Searcy, D. G., Stein, D. B., & Searcy, K. B. (1981) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1981.tb46527.x · Cited by 41 · see citing works
Alternative neural systems: What is a neuron? (Ctenophores, sponges and placozoans)
Moroz, L. L., & Romanova, D. Y. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.1071961 · Cited by 39 · see citing works
“…and Grunert, 1988; Anderson and Spencer, 1989); (b) different neuroid-type conductive, (chemo) sensory and secretory cells in non-bilaterian animals (Mackie, 1970; Anderson, 1980; Anderson and Schwab, 1982; Mackie, 1990; Tamm, 2014a; Nakanishi et al., 2015; Smith et al., 2015; Moroz et al.,…”
BackgroundCrystalline Ferredoxin from a Blue‐Green Alga, Nostoc sp.
MITSUI, A., & Arnon, D. I. (1971) · Physiologia Plantarum · doi:10.1111/j.1399-3054.1971.tb01102.x · Cited by 38 · see citing works
Modern genomic tools reveal the structural and cellular diversity of cnidarian nervous systems
Rentzsch, F., Juliano, C. E., & Galliot, B. (2019) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.12.004 · Cited by 36 · see citing works
BIOLUMINESCENCE AND OTHER RESPONSES SPREAD BY EPITHELIAL CONDUCTION IN THE SIPHONOPHOREHIPPOPODIUS
Bassot, J., Bilbaut, A., Mackie, G. O., Passano, L. M., & de Ceccatty, M. P. (1978) · Biological Bulletin · doi:10.2307/1540785 · Cited by 37 · see citing works
Self-citationAnalysis of blue-green and red algal ribosomal-RNAs by gel electrophoresis
Howland, G. P., & Ramus, J. S. (1971) · Archives of Microbiology · doi:10.1007/bf00408526 · Cited by 37 · see citing works
Temperature dependence of the action potential in Nitella flexilis
Blatt, F. J. (1974) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/0005-2736(74)90165-5 · Cited by 36 · see citing works
The fine structure of neuroglia in the central nervous system of nereid polychaetes
Baskin, D. G. (1971) · Cell and Tissue Research · doi:10.1007/bf00431288 · Cited by 35 · see citing works
“Except as a provisional basis for electrotonic intercellular communication (neuroid conduction; Mackie, 1970), the significance of gap junctions in glial cells is not understood.”
BackgroundJosephson, R. K. (1974) · Elsevier eBooks · doi:10.1016/b978-0-12-512150-7.50011-6 · Cited by 35 · see citing works
Microanatomy of the bell rim of<i>Aurelia aurita</i>(Cnidaria: Scyphozoa)
Chapman, D. M. (1999) · Canadian Journal of Zoology · doi:10.1139/z98-193 · Cited by 33 · see citing works
Novel bridge of axon‐like processes of epithelial cells in the aboral sense organ of ctenophores
Tamm, S. L., & Tamm, S. (2002) · Journal of Morphology · doi:10.1002/jmor.10019 · Cited by 37 · see citing works
“Epithelial conduction, although present in cnidarians (Mackie, 1970; Spencer, 1974; Anderson, 1980), has never been demonstrated in ctenophores.”
BackgroundOrganization of Conducting Systems in “Simple” Invertebrates: Porifera, Cnidaria and Ctenophora
Satterlie, R. A., & Spencer, A. N. (1987) · Springer eBooks · doi:10.1007/978-1-4613-1955-9_9 · Cited by 33 · see citing works
Behavioral Modifications in Coelenterates
Rushforth, N. B. (1973) · Springer eBooks · doi:10.1007/978-1-4684-3006-6_3 · Cited by 31 · see citing works
- Authors
- Mackie, G. O.
- Corresponding author
- Mackie, G. O.
- Venue
- The Quarterly Review of Biology
- Publisher
- University of Chicago Press
- Published
- 1970-12
- Volume
- 45
- Issue
- 4
- Pages
- 319-332
- ISSN
- 0033-5770 (ISSN-L)
- 1539-7718
- OpenAlex
- W2091160861
- Cited by
- 230
- References
- 0
- Citations by year
- 2026: 3 · 2025: 6 · 2024: 4 · 2023: 7 · 2022: 3 · 2021: 14 · 2020: 3 · 2019: 8 · 2018: 4 · 2017: 11 · 2016: 6 · 2015: 13 · 2014: 6 · 2013: 1
- FWCI
- 32.85
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Quarterly Review of Biology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant and Biological Electrophysiology Studies
- 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
- Keywords
- electrogenesis, Noctiluca, Characeae, Dionaea, Mimosa, siphonophores, hydromedusae, ctenophores, chloride efflux
- MeSH terms
- Action Potentials, Chlorophyta, Animals, Cnidaria
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