Electrogenesis in the lower Metazoa and implications for neuronal integration

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. KEY WORDS: Cnidaria, Ctenophores, Electrogenesis, Ion channel, Ionic currents, Sponges Introduction: electrogenesis in early MetazoaIt is evident that many of the ion channel variants involved in signal propagation in multicellular life forms have their origins in bacteria and other single-celled species. In fact, propagating impulses arise in a number of different evolutionary lineages. In each case, natural selection co-opted much the same set of ion channels but inserted them into a different cell matrix. Besides networks of neuronal-like cells, these matrices include the loose three-dimensional parenchyma of glass sponges such as Rhabdocalyptus (Leys and Mackie, 1997;Leys et al., 1999) and the two-dimensional epithelial sheets found in the Hydrozoa (Mackie, 1965;Mackie, 1976;Mackie and Passano, 1968). The following is a brief description of four classes of non-neuronal electrogenesis followed by a more detailed REVIEWSchool of Physiology and Pharmacology, University of Bristol, Bristol BS8 1TD, UK.*Author for correspondence (r.meech@bristol.ac.uk) account of integrative aspects of neuronal electrogenesis as exhibited by the Cnidaria. For an account that includes aspects of electrogenesis in the Protozoa, see Meech and Mackie (Meech and Mackie, 2007), for a more general account,...

Back to the Basics: Cnidarians Start to Fire

“…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]. In the following section, we will briefly touch on these mechanisms and other distinct neural characteristics to illustrate the functional sophistication of these “primitive” nervous systems and highlight fertile avenues for neurobiological research.…”

Neuroepithelial progenitors generate and propagate non-neuronal action potentials across the spinal cord

“…Indeed, epithelial and syncytial conduction systems are commonly observed in non-bilaterian animals exhibiting either a "primitive" nervous system, like jellyfish and comb jellies, or in those lacking a nervous system like the glass sponges [38][39][40][41] . It has been proposed that the modern neuron-based nervous systems of bilaterians using axonal/chemical synaptic transmission evolved from such epithelial conduction systems coupled electrically by gapjunctions 42 .…”

Physiology and Evolution of Voltage-Gated Calcium Channels in Early Diverging Animal Phyla: Cnidaria, Placozoa, Porifera and Ctenophora

“…Unfortunately, only a few examples of electrophysiologically-recorded synaptic potentials are available for ctenophores (Moss and Tamm, 1987; Meech, 2015), and no experimental evidence is available describing the involvement of the single Ca v 2-like channel or other Ca 2+ channels in vesicle exocytosis. In bilaterian synapses, Ca 2+ influx through Ca v 2 channels is required to activate Ca 2+ -sensitive exocytotic machinery, and this is achieved by close apposition of the channels with docked vesicles.…”