The multiple swimming bells, or nectophores, of the colonial hydrozoan Nanomia septata are capable of coordinated avoidance swims in both forward and reverse directions. Individual nectophores also contribute to slower forms of swimming during foraging. Communication between a nectophore and the rest of the colony is at cone-shaped structures in the nectosome stem. The stem provides an attachment point for the nectophores and houses the simple nervous system responsible for their coordination. As revealed by immunocytochemistry, the nectosome stem has three main components: two giant axons, a distributed nerve network and a set of FMRFamide-immunoreactive nerve tracts. Whereas the nerve network is distributed throughout the stem, the nerve tracts link specific contralateral nectophores. Action potentials in the giant axons spread excitation rapidly along the stem, but their connection with individual nectophores is by way of the nerve network. Anatomical evidence suggests a location for the two pathways connecting the nerve network and the nectophore: one excites an epithelial impulse and leads to reverse swimming, and the other provides excitation for forward swimming by feeding into a ganglion-like cluster of nerve cells. The two-way exchange of neural information between the stem and the nectophore is by way of this terminal ganglion and a single nerve leading to a nerve ring at the nectophore margin. This work presents physiological evidence for mechanisms, such as facilitation and summation, operating within a multifunctional, bidirectional nerve network, responsible for coordinating epithelial and neural signals in an early-branching nervous system containing both condensed and distributed units.

George Mackie was a comparative physiologist who explored how behaviour can arise from interactions between nerves and excitable epithelia. Reading about colonial marine life as a student at Oxford, he wondered how a colony of individual ‘jellyfish’ could coordinate to perform ‘loop-the-loop’ swimming. This led to studies on a wide range of invertebrates such as ctenophores, glass sponges, hydromedusae and tunicates, all animals where behaviour can be approached at a cellular level and from an evolutionary point of view. Mackie’s training as a neuroanatomist was the key to his many discoveries, of which perhaps best known is the role of non-neural signalling pathways in generating behaviour. This, together with electrical signalling in sponges and dual threshold signalling in the jellyfish Aglantha digitale , are among the many fields that Mackie either initiated or promoted. His ingenuity, patience, persistence, curiosity and independence of thought made him a brilliant innovator. He spent most of his career at the University of Victoria, British Columbia, but retained a lifelong affection for UK and Continental European culture. He and his wife, Gillian, were creative potters and warm and generous hosts. Their five children survive them, all highly innovative in their different fields.

Unlike in the Cnidaria, where muscle cells are coupled together into an epithelium, ctenophore muscles are single, elongated, intramesogleal structures resembling vertebrate smooth muscle. Under voltage-clamp, these fibers can be separated into different classes with different sets of membrane ion channels. The ion channel makeup is related to the muscle's anatomical position and specific function. For example, Beroe ovata radial fibers, which are responsible for maintaining the rigidity of the body wall, generate sequences of brief action potentials whereas longitudinal fibers, which are concerned with mouth opening and body flexions, often produce single longer duration action potentials.Beroe muscle contractions depend on the influx of Ca2+. During an action potential the inward current is carried by Ca2+, and the increase in intracellular Ca2+ concentration generated can be monitored in FLUO-3-loaded cells. Confocal microscopy in line scan mode shows that the Ca2+ spreads from the outer membrane into the core of the fiber and is cleared from there relatively slowly. The rise in intracellular Ca2+ is linked to an increase in a Ca2+-activated K+ conductance (KCa), which can also be elicited by iontophoretic Ca2+ injection. Near the cell membrane, Ca2+ clearance monitored using FLUO3, matches the decline in the KCa conductance. For light loads, Ca2+ is cleared rapidly, but this fast system is insufficient when Ca2+ influx is maintained. Action potential frequency may be regulated by the slowly developing KCa conductance.

ABSTRACT Although neural tissues in cnidarian hydroids have a nerve net structure, some cnidarian medusae contain well-defined nerve tracts. As an example, the hydrozoan medusa Aglantha digitale has neural feeding circuits that show an alignment and condensation, which is absent in its relatives Aequorea victoria and Clytia hemisphaerica. In some cases, neural condensations take the form of fast propagating giant axons concerned with escape or evasion. Such giant axons appear to have developed from the fusion of many, much finer units. Ribosomal DNA analysis has identified the lineage leading to giant axon-based escape swimming in Aglantha and other members of the Aglaura clade of trachymedusan jellyfish. The Aglaura, along with sister subclades that include species such as Colobonema sericeum, have the distinctive ability to perform dual swimming, i.e. to swim at either high or low speeds. However, the form of dual swimming exhibited by Colobonema differs both biomechanically and physiologically from that in Aglantha and is not giant axon based. Comparisons between the genomes of such closely related species might provide a means to determine the molecular basis of giant axon formation and other neural condensations. The molecular mechanism responsible may involve ‘fusogens’, small molecules possibly derived from viruses, which draw membranes together prior to fusion. Identifying these fusogen-based mechanisms using genome analysis may be hindered by the many changes in anatomy and physiology that followed giant axon evolution, but the genomic signal-to-noise ratio may be improved by examining the convergent evolution of giant axons in other hydrozoa, such as the subclass Siphonophora.

Although members of the Rhopalonematidae family (Cnidaria, Hydrozoa, Trachymedusae) are known to exhibit unusually powerful jet swimming in addition to their more normal slow swimming behaviour, for the most part, reports are rare and anecdotal. Many species are found globally at depths of 600-2000 m, and so observation and collection depend on using remotely operated submersible vehicles. With a combination of in situ video footage and laboratory measurements, we have quantified kinematic aspects of this dual swimming motion and its electrophysiology. The species included are from two Rhopalonematidae clades; they are Colobonema sericeum, Pantachogon haeckeli, Crossota millsae and two species of Benthocodon. Comparison is made with Aglantha digitale, a species from a third Rhopalonematidae clade brought to the surface by natural water movement. We find that although all Rhopalonematidae appear to have two swimming modes, there are marked differences in their neural anatomy, kinematics and physiology. Giant motor axons, known to conduct impulses during fast swimming in A. digitale, are absent from C. sericeum and P. haeckeli. Slow swimming is also different; in C. sericeum and its relatives it is driven by contractions restricted to the base of the bell, whereas in A. digitale it is driven by contractions in the mid-bell region. These behavioural differences are related to the position of the different clades on a ribosomal DNA-based phylogenetic tree. This finding allows us to pinpoint the phylogenetic branch point leading to the appearance of giant motor axons and escape swimming. They place the remarkable dual swimming behaviour of members of the Rhopalonematidae family into an evolutionary context.

Although the bell-shaped nectophores of the siphonophore Nanomia bijuga are clearly specialized for locomotion, their complex neuroanatomy described here testifies to multiple subsidiary functions. These include secretion, by the extensively innervated 'flask cells' located around the bell margin, and protection, by the numerous nematocytes that line the nectophore's exposed ridges. The main nerve complex consists of a nerve ring at the base of the bell, an adjacent column-shaped matrix plus two associated nerve projections. At the top of the nectophore the upper nerve tract appears to have a sensory role; on the lower surface a second nerve tract provides a motor input connecting the nectophore with the rest of the colony via a cluster of nerve cells at the stem. N. bijuga is capable of both forward and backward jet-propelled swimming. During backwards swimming the water jet is redirected by the contraction of the Claus' muscle system, part of the muscular velum that fringes the bell aperture. Contractions can be elicited by electrical stimulation of the nectophore surface, even when both upper and lower nerve tracts have been destroyed. Epithelial impulses elicited there, generate slow potentials and action potentials in the velum musculature. Slow potentials arise at different sites around the bell margin and give rise to action potentials in contracting Claus' muscle fibres. A synaptic rather than an electrotonic model more readily accounts for the time course of the slow potentials. During backward swimming, isometrically contracting muscle fibres in the endoderm provide the Claus' fibres with an immobile base.

Although the Cnidaria have evolved a wide range of body forms matched with an equally varied neural anatomy, individual species exhibit common patterns of behavior. For example, in all species a key challenge for the nervous system is to transfer food from the peripherally mounted tentacles to the centrally located stomach. Foraging movements, necessary to maintain the food supply, must be accomplished in such a way as to avoid interference with the primary objective of getting prey into the mouth. Furthermore, the hunt for prey must be balanced by a measured response to “threat.” Different species respond to threat in markedly different ways, but in each case foraging is inhibited, just as it is during transmission of food. One hundred years ago, G. H. Parker questioned whether a centralized or a locally organized nervous system could best account for sea anemone behavior. Anatomical and electrophysiological studies now suggest that in most Cnidaria there is a degree of hierarchical control, with local reflexes coordinated by more condensed systems of neurons. This organization is highly developed in the nerve rings of hydrozoan medusae and takes the form of ganglion-like rhopalia in the Cubozoa. Even in hydrozoan polyps such as Hydra there are at least four separate neuronal systems. It is likely that the underlying mechanisms (containing both homologous and analogous elements) will be best revealed by a comparative approach that directly relates behavior with its molecular basis. Useful examples include comparisons between sea anemones with and without through-conducting systems; between hydra with and without oral rings; between medusae with and without coordinated escape swimming. Recent advances in transgenomic labeling have shown the way forward.

Chapter 5 The Evolution of Neurons Robert W. Meech, Robert W. MeechSearch for more papers by this author Robert W. Meech, Robert W. MeechSearch for more papers by this author Book Editor(s):Stephen V. Shepherd, Stephen V. ShepherdSearch for more papers by this author First published: 23 December 2016 https://doi.org/10.1002/9781118316757.ch5 AboutPDFPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShareShare a linkShare onFacebookTwitterLinked InRedditWechat Summary This chapter considers the evolution of both aspects of neuronal function: signal transmission and integration of information. It begins with an account of the Porifera and the question of whether the sponges contain the elements of a proto-nervous system. Ctenophores are voracious predators whose locomotion depends on the beating of (usually) eight bands of cilia, an arrangement that makes them highly maneuverable. The chapter focuses on examples from the Hydrozoa with only a short summary to show some differences in the Scypho- and Cubozoa. Neural coordination in the Hydrozoa is so reliant on electrical junctions that their absence in the Scyphozoa and Cubozoa is something of a surprise. Examination of the Cnidaria suggests that nervous systems evolved in a modular fashion with components being responsible for specific functions such as swimming, feeding, and defense. The chapter reviews how these modular neuronal systems came to perform in an integrated fashion. The Wiley Handbook of Evolutionary Neuroscience RelatedInformation

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.

The low numbers of hydrogen ions in physiological solutions encouraged the assumption that H(+) currents flowing through conductive pathways would be so small as to be unmeasurable even if theoretically possible. Evidence for an H(+)-based action potential in the luminescent dinoflagellate Noctiluca and for an H(+)-conducting channel created by the secretions of the bacterium Bacillus brevis, did little to alter this perception. The clear demonstration of H(+) conduction in molluscan neurons might have provided the breakthrough but the new pathway was without an easily demonstrable function, and escaped general attention. Indeed the extreme measures that must be taken to successfully isolate H(+) currents meant that it was some years before proton channels were identified in mammalian cells. However, with the general availability of patch-clamp techniques and evidence for an important role in mammalian neutrophils, the stage was set for a series of structure/function studies with the potential to make the proton channel the best understood channel of all. In addition, widespread genomic searches have established that proton channels play important roles in processes ranging from fertilization of the human ovum to the progression of breast cancer. © 2012 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim.

Contact of food with the manubrial lips in the genus Polyorchis A. Agassiz, 1862 evokes trains of electrical impulses (E potentials) that propagate to the margin. E potentials are also produced by food stimuli at the margin and tentacle bases. E potentials are shown to be associated with inhibitory postsynaptic potentials (ipsps) in the swimming motor neurons and contribute to the arrest of swimming during feeding. The conduction pathway for E potentials is a nerve plexus located in the endodermal walls of the stomach and radial and ring canals. We have explored the conducting properties of the system; the conduction velocity varies with stimulus frequency but is about 15 cm/s when stimuli are more than 50 s apart. Neurites belonging to the E system run around the margin adjacent to the inner nerve ring, where the swimming pacemaker neurons are located. We suggest that they may make inhibitory synapses on to the swimming motor neurons, but this has yet to be demonstrated anatomically. The reversal potential for ipsps, recorded intracellularly with potassium acetate micropipettes, was estimated to be about –69 mV. Swimming inhibition mediated by this endodermal pathway is distinct from that observed during protective “crumpling” behaviour and that associated with contractions of the radial muscles seen during feeding, though it may accompany the latter.

N eoturris breviconis (Anthomedusae) has a nerve plexus in the walls of its endodermal canals. The plexus is distinct from the ectodermal nerve plexuses supplying the radial and circular muscles in the ectoderm and no connections have been observed between them. Stimulation of the endodermal plexus evokes electrical events recorded extracellularly as "E" potentials. These propagate through all areas where the plexus has been shown by immunohistology to exist and nowhere else. When Neoturris is ingesting food, trains of "E" potentials propagate down the radial canals to the margin and cause inhibition of swimming. This response is distinct from the inhibition of swimming associated with contractions of the radial muscles but both may play a part in feeding and involve chemoreceptors. Preliminary observations suggest that the "E" system occurs in other medusae including Aglantha digitale (Trachymedusae) where the conduction pathway was previously thought to be an excitable epithelium.

Sponges 'sneeze' without the benefit of nerves or muscles. While genomic analysis has uncovered a surprisingly complex set of molecular components in these ancient metazoans, physiological studies have revealed equally sophisticated cellular coordination.

All forms of life exhibit excitability; it is one of the characteristics by which living creatures can be recognized. In this chapter, we examine the different manifestations of excitability exhibited by the Metazoa and show how elements present in the Bacteria come together in the Protozoa, Porifera, Cnidaria, and Ctenophora (see Fig. 1) to form the patterns of excitability known as “behavior.” We consider the role of excitation in fertilized eggs and conducting epithelia, as well as the origins of signaling in nerves and muscles. We describe different forms of all-or-nothing signaling, as well as ways of generating graded responsiveness. This study attempts to provide a practical approach to understanding the limitations of excitable systems. We believe that defining these limits is more useful than glorifying their seemingly endless sophistication. THE NATURE OF EXCITABILITY Excitability Defined Excitability is easy to recognize; less easy to define. We recognize excitability when we see it, by the way an organism responds to an external stimulus. For there to be a response, stimulus and organism must interact and the organism must “receive” the stimulus. Inevitably, the stimulus site, or receptor, and the response site, or effector, will be at different locations even in single cells. Thus, excitability depends on the transmission of signals from receptor to effector. The signals may be chemical and spread by passive diffusion, electrical and spread by the transfer of ionic charge, or mechanical and spread by a physical disturbance. We focus in this section on the links between chemical...

Human red cell anion exchanger AE1 (band 3) is an electroneutral Cl–HCO3− exchanger with 12–14 transmembrane spans (TMs). Previous work using Xenopus oocytes has shown that two co‐expressed fragments of AE1 lacking TMs 6 and 7 are capable of forming a stilbene disulphonate‐sensitive 36Cl‐influx pathway, reminiscent of intact AE1. In the present study, we create a single construct, AE1Δ(6: 7), representing the intact protein lacking TMs 6 and 7. We expressed this construct in Xenopus oocytes and evaluated it employing a combination of two‐electrode voltage clamp and pH‐sensitive microelectrodes. We found that, whereas AE1Δ(6: 7) has some electroneutral Cl–base exchange activity, the protein also forms a novel anion‐conductive pathway that is blocked by DIDS. The mutation Lys539Ala at the covalent DIDS‐reaction site of AE1 reduced the DIDS sensitivity, demonstrating that (1) the conductive pathway is intrinsic to AE1Δ(6: 7) and (2) the conductive pathway has some commonality with the electroneutral anion‐exchange pathway. The conductance has an anion‐permeability sequence: NO3−≈ I− > NO2− > Br− > Cl− > SO42−≈ HCO3−≈ gluconate−≈ aspartate−≈ cyclamate−. It may also have a limited permeability to Na+ and the zwitterion taurine. Although this conductive pathway is not a usual feature of intact mammalian AE1, it shares many properties with the anion‐conductive pathways intrinsic to two other Cl–HCO3− exchangers, trout AE1 and mammalian SLC26A7.

When “fishing” for prey the jellyfish Aglantha digitale undergoes a series of “slow swims” driven by pacemaker neurones at the base of its bell-shaped body wall. To avoid predators Aglantha generates an altogether stronger form of “escape” swimming. During an escape swim, the striated muscle sheet that lines the inside of the body wall gives a strong contraction and water is forced from the bell opening. Neuromuscular synapses are distributed widely within this myoepithelium. An overshooting Na+-dependent action potential in each motor axon sets off a large depolarising post-synaptic potential (psp) with a 1 ms synaptic delay. A spike-like component on its rising phase initiates contraction. During slow swimming, low amplitude impulses in the motor axons set off a more slowly rising psp and spike in the myoepithelium. Although the properties and functions of different excitable epithelia have been studied extensively, the basis of their epithelial impulses is not well understood. Using the loose patch clamp technique to study the muscle spike in Aglantha, we find that the voltage-gated inward (Na+ and Ca2+) and outward (K+) currents that form its ionic basis are inactivated within 10 ms. We suggest that differences in the strength of muscle contraction during swimming arise from differences in the rate of rise of the psp. The more slowly rising psp during slow swimming partially inactivates the voltage-gated currents, producing a reduced Ca2+ influx and a weaker contraction. This flexible response to synaptic input accommodates the two forms of swimming in Aglantha but may be absent in other medusae, which depend on myoid-propagated spikes in their striated muscle sheets rather than the presence of distributed synapses.

All multicellular organisms need a means of communicating between cells and between regions of the body. The evolution of a nervous system, by the Cnidaria, provided a fast means of communication and enabled the colonization of rapidly changing environments. Sponges, the descendants of the first multicellular animals, lack nerves but nevertheless have a number of different systems that allow coordinated behaviour, albeit rather slow coordinated behaviour. It is from elements within these systems that the origins of the nervous and endocrine systems, the grand organizing principles of higher animals, seem likely to have appeared. Electrical activity has not been found in cellular sponges, yet local contractions are elicited in response to a variety of stimuli and, in some cases, contractions propagate across the body to control the hydrodynamics of the feeding current. The mechanism of propagation is thought to involve hormones or a combination of other signaling molecules and direct mechanical action of one cell on the next, leading to increased intracellular calcium. In other instances cellular sponges respond to stress, such as heat shock, by elevating intracellular calcium by way of second messengers such as cyclic ADP-ribose. Electrical communication, well known in plants and protists, was first demonstrated in a sponge in 1997. Hexactinellids (glass sponges), which arrest their feeding current within 20 s of mechanical or electrical stimulation, do so via an electrical impulse that propagates through syncytial tissues. These unusual syncytial tissues are cytoplasmically coupled from outside to inside and top to bottom so that there are no membrane boundaries to impede the electrical currents. Pharmacological tests suggest that Ca 2+ , rather than Na + , drives the action potential. The conduction velocity is slow (0.27 cm·s –1 ) and is highly temperature sensitive (Q 10 ~3). At present, glass sponges are the only poriferans known to have propagated electrical signals. In addition, reports of directional swimming in sponge larvae, of the rapid and coordinated changes in the tensile strength of the extracellular matrix in Chondrosia Nardo, 1847, and of the rapid closure of ostia of some cellular sponges in response to mechanical stimuli further illustrate the variety of coordinating mechanisms that evolved in the Porifera in the absence of a nervous system.

In the jellyfish Aglantha digitale two forms of swimming arise from two separate propagating axonal impulses: a fast, overshooting action potential that depends on TTX-resistant Na+ channels, and a low-amplitude spike that depends on T-type Ca2+ channels. While the Na+ action potential is propagated simply and without distortion, the shape of the Ca2+ spike depends on the past history of the axon; it is processed as well as propagated. Patch- and voltage-clamp experiments show how three classes of K+ channels contribute to this apparently unique system. A dual Na+/Ca2+ impulse mechanism may increase the bandwidth of an axonal line of communication but it also places restrictions on the form of the synaptic input needed for spike initiation.

High-conductance Ca2+-activated K+ (BKCa) channels from isolated adult guinea-pig outer hair cells were studied in inside-out membrane patches. They had a 300 pS unitary conductance and were inhibited by tetraethyl ammonium (1 mM), iberiotoxin (33 nM) and charybdotoxin (50 nM). In symmetrical 144 mM KCl their K+ permeability (PK) was 5.4×10−13 cm3/s; this was reduced to around 4.5×10−13 cm3/s with 160 mM Na+ in place of K+ on either internal or external membrane surface. BKCa channels from trypsin-isolated hair cells had a high open probability, that depended on both membrane voltage (16 mV/e-fold change) and the concentration of calcium ions at their intracellular surface ([Ca2+]i). The Hill coefficient was 3–4. About 50% of BKCa channels from mechanically isolated outer hair cells had similar characteristics; the remainder had the same high conductance but a low open probability. Trypsin (<0.5 mg/ml) applied to the intracellular face of these ‘inactive’ channels markedly increased their open probability. It is possible that exposure to trypsin during cell isolation removes an inactivating β subunit. This would account for the absence of ‘inactive’ BKCa channels in trypsin-isolated cells.