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Neuroid Conduction and the Evolution of Conducting Tissues

1970/12/01 by G. O. Mackie · 5 citations
Earth and Planetary Sciences · Agricultural and Biological Sciences · Neuroscience · #Marine Invertebrate Physiology and Ecology #Plant and Biological Electrophysiology Studies #Photoreceptor and optogenetics research

paper · doi:10.1086/406645

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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