Mini Review Nervous System (914 to 915) Answers

April 15, 2022 Posting Komentar

1. Introduction

Reflecting on the benefits that came along with the evolution of the nervous organisation, a straightforward answer is that it boosted noesis—non the least in ourselves. The more complex a nervous system, the higher its cognitive capacities. When information technology comes to the very origins of the nervous system, still, this link is less clear. Information technology may seem surprising at first, just major questions about nervous system origins remain unsolved, starting with the most basic: what exactly was information technology that from and so onwards deserved to exist called a nervous system? What was the major innovation? What became possible that was non possible before?

Crucially, the answer to these questions is non that the nervous system enabled animal cognition for the offset fourth dimension. As is clear nearly recently with this special consequence of Transactions, most of the basic elements of cognition were already nowadays and functional before the nervous organisation evolved. The ability to selectively perceive specific stimuli, the discrimination between favourable and unfavourable, the cess of the overall valence of a situation, the retention of memory, and the integration of information for decision-making—all of this was in place in one form or another in unicellular organisms and early metazoans that did not (yet) possess a nervous system. In consequence, what did the nervous system enable? A start answer can be easily framed: nervous system evolution is almost information substitution and integration betwixt cells. Information technology is about shifting cognition from the unicellular to the multicellular level; information technology is nigh the evolution of circuits. But what was the nature of the first circuit, the elementary circuit, and what did it accomplish? What new functionality was added to the animals' toolbox that fabricated them thrive in the Precambrian past? Working on diverse bilaterian and non-bilaterian metazoan animals without or with simple nervous systems (figure ane), comparative neurobiologists have addressed these questions for the past 150 years and provided manifold answers. I volition survey their contributions and the vivid debate on nervous system origins and, edifice and expanding on this, endeavour some preliminary conclusions.

Figure 1. — Figure one. A simplified phylogenetic tree of the animals. Depicted species represent groups of special relevance for comparative neurobiology that are mentioned in the text. The presence of a centralized nervous organisation in cnidarians and of a brain in ctenophores is discussed in Satterlie [1] and Jager *et al*. [2]. The branching of the tree follows Kapli & Telford [3].

The divergent historical viewpoints are best understood if i considers that they were looking at nervous systems at different levels—at the cellular level at showtime, and then at the level of unabridged tissues or fifty-fifty the whole body. The cellular perspective—i.e. the origin of the first neuron—was developed as early equally the late nineteenth century past Kleinenberg [iv] and the Hertwigs [five], and afterwards refined past Parker [vi]. These authors derived the first neurons from isolated cells that started to relay to each other and thus formed elementary circuits, mediating vertical information flow from receptor to effector cells. Such circuits would enable improved integration and processing of environmental signals and thus raise and diversify basic forms of cognition in early animals. The tissue perspective—the origin of the nervous system as a whole—was developed in the middle of the twentieth century by Pantin [vii] and Passano [eight], and further elaborated by Mackie [9] and Pavan de Cecatty [10]. Rather than on isolated vertical circuits, these authors focused on the evolutionary emergence of elementary nerve nets that interconnected receptor cells and/or effector cells horizontally beyond entire tissues; and addressed the advantages this brought to the performance of the animal body as a whole. Such early nerve nets would have facilitated coordination and integration of primordial behaviours.

Beyond that, the hypotheses on nervous system origins differ in the nature of the effectors that were envisaged downstream of the elementary circuits or nerve nets. While most of the twentieth-century authors favoured contractile effector cells or tissues, more recent contributions as well considered bands or sheets of ciliated cells equally primordial effectors, for the ship of food or locomotion [11]. Others envisaged effector cells carrying out immune functions in response to environmental microbes [12]. Finally, a strong camp emphasized the secretory nature of early neurons that may take acted at a distance on effector cells via the release of neuropeptides [13–15].

For each view, the underlying assumptions on the relatedness of neurons to other cell types will be discussed and evaluated from a modern viewpoint—taking into account cantankerous-phyla comparisons of neural cell types and tissues [sixteen–29], as well as of their constituent molecular machinery such as synaptic proteins, ion channels and transmitter systems [30–35].

From this survey, some consensus emerges. Equally advocated by the twentieth-century comparative neurobiologists, the new functionality that came with the nervous system may indeed accept been nigh credible at the tissue level—with a nerve net equally a whole-body integrative system. Nascent nerve nets may take coordinated body movements—involving contractions of tissue sheets for rapid shape changes, or ciliary chirapsia across tissues for feeding and locomotion. Either selection finds support in recent single-prison cell transcriptomics-based, whole-torso jail cell type and tissue comparisons; and both inventions would have been especially relevant in animals of increasing body size. This suggests that the non-neural-to-neural transition may have occurred more than once, in different tissues and, mayhap, distinct evolutionary lineages.

2. Elementary circuits: simple sensory-effector reflex arcs

The early cell-centric views on nervous organization evolution focused on the emergence of the first neuron as the key element of a local vertical circuit, which relays data between sensory receptor and effector cells. From this perspective, major questions can be put equally follows: what was the sensory receptor and what the effector cell that formed part of the starting time elementary excursion? Epithelial, and different sensory and contractile cell types have been put forward in this context since the nineteenth century, and new candidates have been added in more recent times—such as ciliated cells, secretory cells or even immune cells.

(a) Kleinenberg's neuromuscular theory

Nikolaus Kleinenberg was the first to come upward with ideas on how neurons and primordial circuits emerged in evolution [4]. Studying the epithelial muscle cells in the cnidarian fresh water polyp Hydra, he observed that these cells possessed contractile myofibers that were continued to the residual of the cell via slender processes (figure iia)—every bit if the cell was subdivided into ii separate functional compartments: a contractile fibre and the cell body proper (which Kleinenberg considered sensory given its prominent cilium). In his neuromuscular theory, Kleinenberg thus assumed that the neuron and the muscle cell of the get-go elementary circuit originated from an evolutionary precursor prison cell that was both excitable and contractile, resembling Hydra'southward epithelial musculus cells. This ancient multifunctional cell would have physically segregated the excitable from the contractile function, and then that both formed separate entities. He thus put forward an early (and with today's noesis impossible) version of a partition of labour scenario of cell blazon development [18,37]. Kleinenberg'due south early version of the neuromuscular theory was refuted by his contemporaries [5]. The brothers Richard and Oscar Hertwig considered Hydra's myoepithelial cells to exist simple contractile cells with an epithelial anchor, which coexisted with separate sensory and ganglion cells in the same epithelium. They thus believed that these cell types evolved independently, each one on their own and from epithelial cells, and not from multifunctional precursors.

Figure 2. Historic views of uncomplicated sensory-effector circuits. (a) Kleinenberg's ascertainment of epithelial musculus cells in *Hydra*. The first circuit would have evolved via the physical separation of the contractile myofiber from the jail cell body. Original drawings from Kleinenberg [iv]. (b) Parker's three stages of elementary circuit evolution. Original drawings from Parker [half dozen]. (c) Three steps towards the development of a elementary ciliomotor excursion co-ordinate to Jékely [11]. (d) A multipolar secretory jail cell filled with dumbo cadre vesicles and multiple extensions as observed in nervous system-less sponges. Redrawn later Lentz [36]. (Online version in colour.)

(b) Parker's contained effectors

In his influential monograph on the 'unproblematic nervous organisation', George Howard Parker followed the viewpoint of the Hertwig brothers [six]. Parker postulated three steps towards the development of the first neuron (effigy 2b). At first, some kind of independent effector cells were scattered across aboriginal epithelia, possibly resembling Kleinenberg's myoepithelial cells or nematocysts in cnidarians. These effector cells were supposed to react to stimuli autonomously. Secondly, separate receptor cells were assumed to have evolved from the undifferentiated epithelium adjacent to the effector cells. 'The most primitive nerve jail cell from the standpoint of animal phylogeny is the sense-cell, or receptive cell, such as occurs in the sensory epithelium of the coelenterates' [iii, p. 210]. As a tertiary step, existent neurons evolved between receptor and effector to eventually requite rise to the reflex triad of 'receptor, adjustor and effector'. Similar ideas were voiced by Cajal [38] who proposed an platonic invertebrate in which contained neurons are scattered across epithelia and are—each 1 of them—both sensory and motor. Thus, the founders of modern neurobiology proposed that the most elementary course of the nervous organisation was a characteristic mononeuronal reflex arc composed of a sensory neuron, a neuron and an effector cell [x]. In line with these ideas, two- or three-celled mechanosensory-contractile vertical neuronal circuits are widespread in today'south cnidarians [39] and ctenophores [40].

(c) Elementary ciliomotor circuits

A modern variant of Parker's theory put forward by Gáspár Jékely differs in the nature of the effector cells, interpreted every bit epithelial cells with motile cilia [xi]. This view links the evolutionary emergence of neurons to the emergence of a primordial ciliomotor circuit for the improved coordination of ciliary swimming. Following this view, the development of neurons started from a sensory cell that slowly acquired basal processes, which contacted neighbouring cells bearing motile cilia (effigy twoc). Indeed, ciliary bands with motile cilia coordinated by sensory-ciliary mini-circuits are a widespread ways of locomotion in primary larvae, innervated past an apical organ and associated receptor cells that mediate mechano-, chemo, baro- or photosensory input [41–44]. Of note, such ciliomotor larval nervous systems are only reported for bilaterians.

Similarly, sensory-ciliomotor circuits drive ciliary swimming in the enigmatic ctenophores (figure 1). In these animals, an apical sense organ innervates and controls the rhythmic chirapsia of the comb plates, which are composed of motile cilia [45,46]. Chiefly, however, the sensory-ciliomotor circuits of bilaterians and ctenophores are often regarded independent evolutionary acquisitions ([46]; see however [47]).

(d) The first neuron—a secretory cell?

Parker and followers emphasized the sensory nature of the commencement neuron, and regarded information technology the sister jail cell type of sensory epithelial cells. Implicit to this view, these sensory cells would have started secondarily to emit signals to the neighbouring effector cells via secretion. Other authors turned this view around and instead causeless that the secretory nature of the neuronal precursors was first and the sensory nature secondary. They thus considered the sister cell type of the first evolving neuron a secretory jail cell [48–l]. Consequentially, neurons would accept first appeared as neurosecretory cells. For example, studying the subcellular localization of catecholamines, serotonin, neuropeptides and other putative transmitters in sponges, Thomas L. Lentz observed bi- and multipolar secretory cells (effigy iid) that he likened to primitive neurons [36]. In nervous system evolution, similar excitable and conductive 'prenervous cells' with secretory capabilities would take influenced nearby effectors; they would have adult elongated processes, become sensitive to stimuli and thus given ascension to the outset circuits [50]. Studying neurosecretion in Hydra, Lentz pointed out the essential value of neurosecretion non just for the chemical synapses but also for the activity of nervous tissue as a trophic system, that is, decision-making growth and development by means of synthesis and release of specific substances [10,50].

(eastward) An ancestral neuroimmune organisation

Related to the notion of early neurons serving secretory functions is the more contempo idea that neurons may have evolved every bit immune cells [12]. Given that multicellular animals emerged in a earth of microbes, and that all extant animals are colonized by a large number of symbiotic microbes; and considering that host-associated microbiota has been shown to be in a permanent dialogue with the host enteric and central nervous systems [51], neurons might have emerged as a cell type exerting functions unremarkably attributed to immune systems: they may have monitored the environment and sensed and discriminated microbes. Indirectly, via secretory release, and directly, via innervation, neurons may accept adjusted the animal's vital processes (i.e. evolution, physiology, tissue homeostasis and behaviour) to the presence and state of the microbiota. In addition, neurons might take exerted an immunomodulatory result by tuning the immune response of epithelial cells [12]. Later in development, the intercellular communication channels established by such neuroimmune cells could and then accept caused secondary functions in the class of sensory-motor circuits.

(f) Local circuits first or nerve net first?

In summary, the above prison cell-centric views envisage the showtime neuron as the key part of an uncomplicated sensory-effector circuit. They kickoff from more or less isolated precursors, equally is the case for Kleinenberg's myoepithelial cells, Parker's effectors, Lentz' neurosecretory cells and for the putative neuroimmune cells. Each of these can be seen every bit stand up-solitary sensory-effector reflex arcs that raise local integration past means of their newly caused neurite-like processes. Only in a second footstep would these elementary circuits get horizontally interconnected.

What would take been the selective advantage of such local circuits? This question has been extensively discussed and is far from footling [7,ix,eleven,52]. 1 elegant concept envisages an increase in 'sensory-to-motor transformation', defined as the ratio of involved sensory cells to effector cells that they can influence [11]. Another reward would prevarication in the improved conductive capacity of the newly evolving neurites, which may have enabled faster data processing and integration. Such changes would entail incremental increases in cognitive ability for the animal.

Alternatively, isolated vertical elementary circuits may have never existed. Instead, early neurons may have been horizontally interconnected from the very kickoff, across tissues, in the class of a nerve net. In these nets, vertical and horizontal information transfer may have co-occurred, with dispersed receptor cells feeding into the nerve cyberspace and distributed effector tissue innervated by the nerve net. Specialized local circuits would then have arisen via restricted secondary diversification. This exciting culling requires u.s.a. to change perspective: from the cell to the tissue level. This style, the selective advantage of the nascent nervous system becomes more than obvious.

3. Elementary nervus nets (i): the contractile network hypothesis

In search of the start evolutionary manifestation of the nervous system, some authors in the mid twentieth century no longer envisaged local, vertical circuits. Instead, they postulated the primacy of the unproblematic nerve net: i.eastward. neurons forming large horizontal networks spanning entire tissues from the very kickoff. Nervus nets every bit propounded by these views are observed for example in extant ctenophores and cnidarians (figure 3). A primordial nature of the nervus net would require that some kind of tissue- or trunk-wide system predated the nervous organisation, which then evolved into the nerve net. If so, what was the nature of this arrangement and what was its function? Or, in other words: what kind of cellular network was the evolutionary precursor of the nerve net, and can we identify related non-neural networks ('sis networks') in extant animals?

Figure 3. Characteristic nervus nets in ctenophores and cnidarians. (a) The polygonal epithelial nervus net of *Pleurobrachia pileus* redrawn after Jager *et al*. [45]. (b) The epithelial nerve internet of the *Hydra* polyp from Arendt [53]. (c) Cellular view of the *Hydra* nervus internet. Nervus nets are known to contain stereotypic elements with singled-out transmitters [54]. Redrawn subsequently Lentz [50].

(a) Muscle fields and global shape changes

An early tissue-axial view was developed by Carl Frederick Abel Pantin [7], who was the start to postulate an elementary nerve internet (and considered local neural circuits secondary specializations thereof). Pantin suggested that the nervus net evolved aslope an epithelial contractile tissue sheet, conducting excitation with its longer processes faster than the contractile sheet cells themselves. This led to simultaneous wrinkle of the unabridged tissue every bit opposed to the slower wave-similar contractions. The coordinated contraction of contractile tissue units (referred to as musculus fields; [ten]) enabled global shape changes and behaviour that was not possible before. This was especially relevant for animals with increasing body size, which needed to respond to environmental stimuli with a total (rather than local) integration of effectors—which cannot exist achieved by isolated reflex arcs [vii].

Pantin built his theory on observations of contractile systems in cnidarians, referring for example to the sphincter closure apparatus in Calliactis. He reasoned that, in many cases, the activity of the nervus net would result from spontaneous, endogenous activity, as is besides frequently observed in other cnidarians (see for example [55]). The response to an ecology stimulus would then consist of a prolonged change in the pattern of spontaneous action (rather than the initiation of activity itself). Such behaviour would be generated internally and modified by external cues—with the spontaneous pattern having priority over that of the reflex blueprint: 'The reflex arc is non a primitive unit of measurement' [iv, p. 176].

Inspired by Pantin'due south theory, the cnidarian biologist L. M. Passano developed a tissue-centric sectionalisation of labour scenario with nervus nets and muscle sheets diversifying from a single network of highly interconnected, gristly cells with contractile and conductive properties [8]. He proposed that some of these cells acquired the capacity to endogenously generate electrical activity, comparable to pacemaker cells, while others started to respond to these protoneurons. The onetime and then specialized more and more on the generation, integration and conduction of electrical signals and finally became the neurons of the first nerve net, whereas the letter specialized on wrinkle and became bona fide muscle cells innervated past the nerve cyberspace. Passano's thought is named hither the 'contractile network hypothesis', which can exist regarded a modern tissue variant of the initial neuromuscular theory. It is visualized in an interpretative cartoon in figure iv.

Figure 4. — Effigy 4. The contractile network hypothesis. (a) Evolutionary precursor state with epithelial mechanosensory and mesenchymal cells with long interconnected contractile and conductive processes forming a tissue-wide network. (b) The outset nervous organization comprising mechanosensory neurons innervating a tissue-spanning simple nerve internet composed of multipolar interneurons. The nerve internet neurons innervate a network of contractile myocytes. Red boxes on the cells represent conductive ion channels. Red lines indicate actomyosin filaments for contraction. (Online version in colour.)

Another cnidarian biologist, George O. Mackie, strengthened the case for this hypothesis by describing various forms of contractile and/or conductive tissue sheets in cnidarians [9]. For example, the bong-shaped body of the hydromedusae is equanimous of myoepithelial cells, which constrict to produce the locomotory jet of water. The excitation for this response is conducted in the contractile sheet itself. In addition, the contractile sheet is innervated past the ganglion cells of a proper nerve net, which act as pacemakers initiating the rhythmical pond beat out and apace transmitting the excitation into all four quadrants of the medusae [9]. In general, multifunctional contractile and conductive tissue sheets announced typically involved in elementary behaviours such equally rapid whole-tissue wrinkle, whereas functionally divide nerve net and muscles are involved in more than complex movements that require sophisticated integration. Thus, neuroid-myoid tissues (resembling the presumed multifunctional precursor tissue), besides as bona fide nerve nets and musculus sheets (representing the possible outcome of an evolutionary partitioning of labour process) coexist in cnidarians. This makes the contractile network hypothesis a plausible scenario that may occur whenever complex behaviour evolves in animals of increasing body size.

The contractile network hypothesis besides underlies the and so-called peel brain thesis recently put frontward by Fred Keijzer and colleagues [56,57]. In line with Pantin and Passano, they postulate that early nervous system evolution gave ascension to a nervus-net-innervated muscle effector tissue, the primary source of animal move. This tissue was capable of inducing and coordinating cocky-organized contractile activity across an all-encompassing muscle surface underneath the skin [56,58].

(b) A neuromuscular orthogon in Dickinsonia?

In support of the contractile network hypothesis, the presence of a well-developed nerve net in cnidarians and in ctenophores reliably correlates with the presence of myofibers directly innervated by the nerve net neurons [37,52,59]. In these animals, muscular systems are composed of longitudinal muscles (in the direction of the master torso axis) and of ring muscles [60,61]. This indicates that, once myofibers segregated from neurons, they were arranged at right angles and contracted antagonistically, in an system termed a neuromuscular orthogon (effigy fivea,b) [37]. In line with this, forward locomotion of the Ediacaran fossil Dickinsonia has recently been discussed based on body and trace fossils, and may have involved antagonistic wrinkle of myofibers oriented parallel and perpendicular to the longitudinal axis [62]. Indicative of this, the upper surface of these fossils frequently contains wrinkle marks parallel to the longitudinal centrality (effigy 5c). These observations constitute a plausible anatomical setting in which the nervous and muscular system may have co-evolved.

Figure 5. Locomotor patterns in bequeathed metazoans. (a,b) The evolution of nerve-net innervated longitudinal musculature from polarized conductive-contractile cells via division of labour. From Arendt *et al.* [37]. (c) Interpretative drawing of a *Dickinsonia*-similar creature feeding on organic mats covering the Ediacaran seafloor ('onetime elephant pare'), following Evans *et al.* [62] and Ivantsov [63]. Fossil evidence indicates that the animals remained stationary for a period of time, removed the organic mat beneath them via external digestion or ciliary activity, and so moved from that area leaving a low ('footprint'). Chains of footprints are interpreted every bit forward movement. Wrinkles on the surface bespeak the presence of longitudinal muscles parallel or perpendicular to the gastric pouches (violet and reddish double arrows), enabling shape change. Locomotor movements may take been cilia- and musculature-driven and controlled by nerve nets.

(c) Contractile-conductive tissue in sponges

How about early on-branching Metazoa that exercise not (all the same) take a nervous system, such as sponges—exercise we find interconnected myofiber-like cells as postulated by the contractile network hypothesis? The sponge biologist Max Pavans de Cecatty affirmed this, investigating various sponges [10]. He showed that the sponge ectomesenchyme represents neuroid-myoid tissue with mixed contractile and conductive properties. Its surface comprises apartment expansions of so-called pinacocytes, the cell bodies of which are located deeper in the connective tissue, where contractile cells form a mesenchymal network—connected to each other and to the pinacocytes (effigy 6). All cells have secretory granules, supposedly for prison cell–cell communication. Based on these observations, Pavans de Cecatty regarded the sponge contractile mesenchyme a 'protonervous or neuroid system'. 'Reticulated and discrete, it has pacemaker and secretory activities, is direct excitable, and is conductive from jail cell to jail cell' [seven, p. 386].

Figure 6. Ectomesenchyme in sponges. Interconnected contractile and conductive cells with secretory granules form a mesenchymal network underneath the pinacocyte outer epithelium. Red lines signal actomyosin fibres. Redrawn and modified subsequently Pavans de Ceccatty [10].

iv. Unproblematic nerve nets (ii): the neurosecretory network hypothesis

The contractile network hypothesis builds on the premise that beginning coordinated fauna trunk move was driven by tissue contraction. Even so, this is non the full picture. In an alternative view, larger fields of motile cilia might have propelled early on animals forwards [63]—and myofibers may take mediated steering rather than propulsion. Indeed, the Ediacaran Dickinsonia are postulated to accept possessed a ventral mucociliary sole for particle send, ciliary gliding or even pond movements [37,63,64]. Dickinsonia and related species such as Yorgia apparently moved forward by short episodes of swimming as evidenced by a series of feeding traces on algal mats without whatever show of the body moving on the substrate (figure 5d,e). Only like tissue contraction, ciliary beating patterns that may take enabled such swimming movements would have required increasing degrees of coordination with increasing body size.

A concurrent scenario for nerve net evolution at the tissue level thus gains momentum: namely that ciliated tissue with coordinated chirapsia was centre phase in nervus net evolution. A homogeneous array of neuroid-ciliated cells may have been in place in early on metazoans—before a division of labour event separated neuronal precursors and motile ciliated sister jail cell types. How can we envisage a possible evolutionary emergence of a nerve internet from within ciliated tissue?

(a) The neurosecretory network hypothesis

This hypothesis builds on the primacy of secretory cells equally advocated by Lentz and others (see above), and is put forwards for the kickoff time in an elaborate style by Gáspár Jékely in this outcome of Transactions [15]. Here, nervous system development starts from a sail of ciliated cells. Initially, cilia are both sensory and motile and reply to environmental cues autonomically with changes in their beating blueprint. Enhanced synchronization betwixt cells is so achieved via the basal release of neuropeptides that trigger autocrine and paracrine amplification. Via partitioning of labour, some of these cells specialize in sensory perception and neuropeptide release and become sensory-secretory cells interspersed among ciliary effector cells, every bit depicted in effigy viia. In this organisation, all tissue cells would be linked up into a chemical network made upwardly of diffusible neuropeptides [fifteen]. Withal, signalling via improvidence of peptides becomes inefficient in larger bodies. This prompts the gradual horizontal elongation of basal secretory processes until they overlap between distant neurosecretory cells. Finally, synapses would evolve betwixt these processes, thus interconnecting sensory-neurosecretory cells of the same blazon into coherent nerve nets as depicted in figure 7b. This fashion, the now physically interconnected network cells would be able to display rapid synchronized activity with pulsatile peptide release for the tissue-wide control of ciliary beating or contractions.

Figure 7. The neurosecretory network hypothesis. (a) Evolutionary forerunner state. Ciliated tissue with equally spaced sensory-neurosecretory cells that secrete neuropeptides. Sensory-neurosecretory cells form numerous basal projections. (b) Uncomplicated nerve cyberspace. Horizontal projections of sensory-neurosecretory interconnected via synapses. Synaptic distension of neurosecretion. Bluish circles indicate vesicles of secreted neuropeptides. (Online version in color.)

The neurosecretory network hypothesis finds support by the omnipresence of circuitous peptidergic signalling in all animals except sponges [65–67], and by the dispersed and widespread occurrence of sensory-neurosecretory cells in cnidarian nerve nets [49,50] (run across in a higher place) and in the echinoderm central nervous system [68]. While it is conceivable that such neurosecretory nerve nets initially controlled ciliary beating patterns, they might accept started to concomitantly control the behaviour of adjacent contractile tissues.

In line with this hypothesis, Béla Vigh and Ingeborg Vigh-Teichmann showed that the chordate neural tube harbours so-called fundamental spinal fluid (CSF)-contacting neurons. These are sensory-neurosecretory cells with ciliated upmost sensory protrusions that projection into the spinal fluid [13,14] and with basal secretory processes that terminate on the basal lamina. Similar cells are observed along the entire spinal cord in the basal chordate amphioxus [xiii]. Given that all epithelial cells of the chordate neural tube conduct motile cilia, such distributed and interconnected neurosecretory cells may have initially controlled ciliary chirapsia within an bequeathed mucociliary sole [37]. Later on, these cells would have started influencing wrinkle of the side by side longitudinal musculature—first in a paracrine mode, and finally via the more targeted synapses. In support of this scenario, the neuromuscular junctions of the amphioxus ventral motor roots have evolved across the neuroectodermal basement membrane [69]. Hence, a neurosecretory nerve net controlling ciliary beating of a mucociliary epithelium may accept represented the starting material for the evolution of the chordate neural tube [37].

(b) Neurosecretory centres: the apical nervous organization

Besides expanding into a neurosecretory network, at that place is a 2nd strategy for sensory-neurosecretory cells to maintain and enhance signalling efficiency, and to reduce the constraint imposed on chemical signalling by improvidence in an ever-increasing fauna trunk. Concomitant with the advent of circulatory systems, these cells can beginning secreting neuropeptides, henceforth called hormones, into the body fluid. To this end, their secretory endings get together into a prominent plexus, which is referred to as the neurosecretory center or neurohemal organ [xv].

Sensory-neurosecretory cells are found in the nervous arrangement of annelids [seventy] and other protostomes [71], and in the vertebrate hypothalamus (figure 8). In view of their possible ancestral nature, these cells are deemed protoneurons [13,xiv]. They bear diverse secretory and synaptic endings, which may reflect their evolutionary transition land between non-neural and neural cells. Nosotros accept postulated that the so-chosen apical nervous organisation represents an ancient neurosecretory centre that became part of the evolving bilaterian brain [47]. This brain centre is still predominantly chemically wired and coexists with the synaptic brain in extant bilaterians [72].

Figure 8. — Effigy 8. Sensory-neurosecretory cells in the vertebrate brain. Protoneuron-like cells from part of the periventricular ependyme with sensory endings responding to light, ions and menstruum. Basal neurosecretory processes release vesicles into external body fluids. Reproduced from Vigh *et al.* [14].

All in all, with the different variants of the neurosecretory versus contractile network hypotheses we are left with concurrent and seemingly conflicting views on nervous system origins—each of them well reasoned and plausible. This prompts the question: how tin can nosotros proceed from here?

5. Testing hypotheses via the comparing of cell blazon-specific molecular machinery and regulatory programmes

All of the in a higher place views on nervous system origins assume specific sis prison cell type relationships between neurons and other torso cells. The contractile network hypothesis considers some kind of myocytes to exist about closely related to neurons. In dissimilarity, the neurosecretory network hypothesis would see secretory cells in this position. Alternatively, allowed cells might exist the most closely related to neurons. These hypotheses tin can nowadays exist tested on molecular grounds.

Neurons comprise sophisticated molecular mechanism, which, piece past slice, have been dissected functionally and structurally in the past decades by molecular biology and biochemistry [73,74]. For example, different kinds of chemical synapses are distinguished, such as the glutamatergic, GABAergic or cholinergic synapses. Pre- and postsynapse have been shown to be equanimous of multiprotein signalling complexes, and the generation and conduction of activeness potentials has been shown to rely on synergizing ion channels with different ion specificities [35]. This wealth of molecular knowledge on neurons and related jail cell types can now be harvested to test the to a higher place hypotheses on nervous system origins. The rationale is that prison cell types that are evolutionarily related should apply related molecular mechanism, the expression of which should be controlled by similar regulatory programmes [75].

Towards this aim, the current epochal advances in single-cell genomics at present allow the body-wide characterization of cell type-specific regulatory and effector genes, and thus facilitate the comparison of all cell types within and beyond species, and ultimately beyond phyla.

(a) Hit heterogeneity of neurons

Several laboratories have pioneered whole-trunk single-prison cell sequencing for the comparative analysis of cell type inventories beyond metazoans [22–29]. These studies accept identified neural cell type inventories in nerve-net-equipped cnidarians, ctenophores and bilaterians, and in early-branching lineages that do not possess a nervous system [25–27]. With this new comparative field just forming, first insights are apparent.

Ane important ascertainment shared by all studies is the heterogeneity of neuronal cell clusters. In the ctenophore Mnemiopsis leidyi, synaptic scaffold components are expressed across multiple cell types, and none of them show significant co-expression of voltage-gated ion channels. This would propose that ctenophore neurons are both various and of unclear relationship to those of other animals [25]. In the cnidarian sea anemone Nematostella, neuronal prison cell populations are grossly subdivided into two subsets (N1 + N2), specified by unlike transcription factors and representing distinct nerve nets in the tentacle ectoderm and in the body column inner layer, the gastroderm [26]. Neuronal cell types representing three distinct nerve nets as well show divergent transcription factor identities in the cnidarian Hydra vulgaris [28,53]. Among bilaterians, whole-torso single-jail cell datasets have been reported for the annelid Platyynereis [22] and the planarian Schmidtea [23,24] and likewise exhibit heterogeneous populations of neurons. As of now, it has been difficult to chronicle neuronal jail cell populations between species [25,26]—which may improve with ongoing methodological progress in the comparison of single-cell genomics datasets across larger taxonomic distances [76]. In any case, the diversity of neuronal types that is manifest in early branching metazoans would suggest that the evolutionary transition from non-neural to neural may accept taken place more than once in singled-out tissues—and, possibly, in distinct evolutionary lineages.

(b) Support for the contractile network hypothesis

Given the remarkable heterogeneity of neuronal prison cell types—what do the single-cell datasets reveal about the relatedness of these neurons to other, not-neuronal types? Can we identify the neuronal sister cell types? And, what is more, can we identify neuron types that are more closely related to not-neuronal types than they are to other neurons? Such cases would be particularly relevant to examination the hypothesis of independent neuronal origins—and seem to indeed be. For example, a contempo single-cell study focusing on musculature in the sea anemone Nematostella reports extensive similarities betwixt the ectodermal N1 neurons and the ectodermal myocytes of the tentacle retractor muscles—both morphologically and molecularly [29]. Unlike the mesodermal myoepithelial cells, the ectodermal myocytes detach from the epithelium into a basiepithelial position similar to the N1 ganglion neurons [77]. They grade synapse-like neuromuscular junctions with postsynaptic densities and the conserved neuronal scaffolding protein Homer; and they are the only muscles to limited ionotropic glutamate receptors and the neuronal RNA-bounden protein ELAV [29]. Moreover, the ectodermal myocytes limited the neuronal transcription factors FoxL2, SoxB2 and Sox3 [29], which they share with the N1 neurons that innervate them [26]. These data are consequent with an evolutionary kinship of the tentacle N1 neurons and retractor muscles in Nematostella, possibly reflecting a partition of labour effect equally postulated by the contractile network hypothesis. Intriguingly, similarities are also apparent for the Nematostella gastrodermal myoepithelial cells and N2 neurons, which share combinatorial transcription factor expression involving the T-box factors tbx1/ten, tbx20 and the bHLH factor hand. In each case, the N1 and the N2 neurons appear to exist more closely related to the different contractile cell types than they are to each other. To strengthen the case, information technology will exist important to work out whether the cnidarian ectodermal and gastrodermal neuron and muscle types are conserved in the bilaterians or in the ctenophores, and whether similar cell type interrelationships hold true for these groups. Of notation, within the bilaterian superphylum ectodermal muscles are only reported for a few Spiralian groups—including some annelids, molluscs and flatworms [78]. Unravelling their molecular identity and possible relatedness to cnidarian ectodermal musculature appears peculiarly rewarding.

A kinship of glutamatergic neurons and myocytes finds support by the co-usage of postsynaptic modules such as the Homer-containing calcium-induced calcium release module and of the same conductive molecular machinery including all iv Shaker potassium channel paralogs K_vi to 4 [35]. This suggests that these modules were already present in the contractile-conductive precursor cells equally depicted in figure 4.

(c) Support for the neurosecretory network hypothesis

Other observations in plough strengthen the view that at least subsets of vertebrate neurons may have evolved from sensory-neurosecretory cells, every bit discussed above. Starting time and foremost are the many similarities that motor neurons in the ventral neural tube share with pancreatic secretory cells, including neuropeptide and neurotransmitter release, synaptic mechanism, and activeness potentials [35,79]. Furthermore, the combination of transcription factors specifying these neurons, including the homeodomain factors mnx, nk6, pax6 and Islet, and the onecut transcription gene hnf6 [80] closely matches that of the secretory pancreatic islet cells [81]. These data indicate that both the neurons of the vertebrate ventral neural tube and foregut-derived pancreatic islet cells may exist evolutionary derivatives of sensory-neurosecretory cells in a digestive mucociliary sole [37]. In line with this, a similar pancreatic/ventral neural tube-like transcription factor signature is also shared past selected groups of neurons and gut cells in the sea urchin [79], and is likewise characteristic for the pharyngeal ectoderm in the cnidarian Nematostella [26], which gives rise to secretory cells (and a small-scale number of neurons alike). Furthermore, in the demosponge Spongilla the nkx6+ secretory digestive choanocytes have been shown to specifically express orthologs of postsynaptic genes such as Homer and Shank, which may betoken some affinity of these cells to protoneurons [82].

6. Determination

One and a half centuries of comparative work and educated conjecture have helped to carve out important hypotheses regarding the origin of the nervous system. Early contributions envisaged local sensory-effector circuits as start manifestations of the nervous organization, referred to as elementary circuits. In these circuits, data transfer would take been mostly vertical, from sensory to effector cells, and mediated by the starting time neurons. Different kinds of effector cells have been considered for these circuits—from contractile to motile ciliary or even with immune functions.

Later authors instead emphasized horizontal information transfer and envisaged tissue-wide elementary nerve nets as first manifestations of the nervous system. These nets may accept acted as endogenous pacemakers, or they may accept integrated sensory input for the coordinated control of entire downstream effector tissues—which may have been contractile or bearing motile cilia. These contributions thus led to two major hypotheses for nervous organization origins, which survive until today. Following the contractile network hypothesis, the commencement nervus net originated by division of labour from a network of multipolar mesenchymal cells that were both conductive and contractile (figure 4). Alternatively, the elementary nerve net may have resulted from newly evolving synaptic communication between the basal processes of dispersed sensory-neurosecretory cells that formed part of an epithelium with motile cilia (figure seven).

Recent progress in sequencing the transcriptomes of single cells from entire bodies allows the testing of these hypotheses via comparison of cell blazon-specific transcriptional profiles within and across species. While this new field of comparative jail cell biology is just emerging and is however far from a comprehensive agreement of cell type genealogies beyond the fauna kingdom, first observations betoken back up for both the contractile network hypothesis and the neurosecretory network hypothesis. For example, while in cnidarians ectodermal neurons and myocytes appear closely related, vertebrates show a close molecular relationship between ventral neural tube neurons and pancreatic secretory cells. Futurity cross-phyla comparisons of cell types volition help in deciding whether these observations can be generalized. Equally it stands, the information back up at least two unlike origins of nerve nets in different trunk parts of ancestral metazoans. Also, molecular comparisons volition substantiate whether any of these nerve nets are related to the diverse nerve nets found in the enigmatic ctenophores.

According to all prevailing hypotheses the incipient nerve nets enabled some complex feeding or locomotor behaviour, and tin can thus be seen every bit an adaptation towards enabling such whole-torso movements nether the constraint of increasing body sizes. Besides the coordination of movement, such nerve nets would accept facilitated data integration in various ways and thus enhanced cognition. First, different external sensory modalities would accept fed into the nerve net and triggered ane integrated nerve internet response to ecology stimuli. Second, via reafferent sensing the nerve net would have besides perceived sensory stimuli generated past the animate being'southward own movement and thus integrated internal and external information [83]. This is especially of import for large animals that cannot properly move without such integration. Tertiary, the immediate effect of an elaborate nerve net with its increased speed of signalling and multiple synaptic contacts would be to profoundly increment the range of habituation and sensitization of different spontaneous exploratory patterns of activity. Overall, the coordinating and integrating effects of the evolving nerve nets cannot exist decoupled and sum upwardly to a substantial increase in knowledge that accompanied the rise of the elementary nervous organization. In conclusion, the origin of the nervous system immune early animals to ensure behavioural coordination and cerebral capacities in larger multicellular bodies. Without a nerve net, ever-increasing cell numbers would have inevitably led to reduced information menstruum between cells, and thus to a decrease in cognitive power and integration. The nervous system can thus exist seen every bit an evolutionary response to multicellularity and increasing torso sizes in early on animals.

Data accessibility

This commodity has no additional information.

Competing interests

I declare I have no competing interests.

Funding

The piece of work was supported past the Advanced grant 'NeuralCellTypeEvo' 788921 by the European Commission.

Acknowledgements

The author thank you all members of the Arendt laboratory for many discussions on nervous system evolution and Michael Levin and ii bearding reviewers for valuable and insightful comments on the manuscript.

Footnotes

I contribution of x to a theme outcome 'Basal knowledge: multicellularity, neurons and the cognitive lens'.

Published by the Regal Society under the terms of the Artistic Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original writer and source are credited.

References

1.
Satterlie RA
. 2002 Neuronal control of swimming in jellyfish: a comparative story. Can. J. Zool. 80 , 1654-1669. (doi:10.1139/z02-132) Crossref, ISI, Google Scholar
ii.
Jager M, Chiori R, Alie A, Dayraud C, Queinnec E, Manuel M
. 2010 New insights on ctenophore neural anatomy: immunofluorescence study in Pleurobrachia pileus (Muller, 1776). J. Exp. Zool. B 316 B, 171-187. (doi:ten.1002/jez.b.21386) Google Scholar
3.
Kapli P, Telford MJ
. 2020 Topology-dependent disproportion in systematic errors affects phylogenetic placement of Ctenophora and Xenacoelomorpha. Sci. Adv. half-dozen , eabc5162. (doi:10.1126/sciadv.abc5162) Crossref, PubMed, ISI, Google Scholar
4.
Kleinenberg N
. 1872 Hydra. Eine anatomisch-entwicklungsgeschichtliche Untersuchung . Leipzig, Germany: Verlag von Wilhelm Engelmann. Crossref, Google Scholar
5.
Hertwig O, Hertwig R
. 1879 Dice Actinien. Studien zur Blättertheorie . Jena, Germany: Gustav Fischer. Google Scholar
half-dozen.
Parker GH
. 1919 The elementary nervous system . Philadelphia, PA: Lippincott. Crossref, Google Scholar
seven.
Pantin CFA
. 1956 The origin of the nervous organisation. Pubbl. Staz. Zool. Napoli 28 , 171-181. Google Scholar
8.
Passano LM
. 1963 Archaic nervous systems. Proc. Natl Acad. Sci. USA 50 , 306-313. (doi:x.1073/pnas.50.2.306) Crossref, PubMed, ISI, Google Scholar
nine.
Mackie Become
. 1970 Neuroid conduction and the evolution of conducting tissues. Q. Rev. Biol. 45 , 319-332. (doi:10.1086/406645) Crossref, PubMed, ISI, Google Scholar
ten.
Pavans de Ceccatty M
. 1974 The origin of the integrative systems: a change in view derived from research on coelenterates and sponges. Perspect. Biol. Med. 17 , 379-391. (doi:10.1353/pbm.1974.0060) Crossref, PubMed, ISI, Google Scholar
xi.
Jékely G
. 2011 Origin and early evolution of neural circuits for the control of ciliary locomotion. Proc. R. Soc. B 278 , 914-922. (doi:10.1098/rspb.2010.2027) Link, ISI, Google Scholar
12.
Klimovich AV, Bosch TCG
. 2018 Rethinking the role of the nervous system: lessons from the Hydra holobiont. Bioessays forty , e1800060. (doi:10.1002/bies.201800060) Crossref, PubMed, ISI, Google Scholar
13.
Vigh-Teichmann I, Vigh B
. 1983 The system of cerebrospinal fluid-contacting neurons. Arch. Histol. Jpn 46 , 427-468. (doi:ten.1679/aohc.46.427) Crossref, PubMed, Google Scholar
14.
Vigh B, Manzano east Silva MJ, Frank CL, Vincze C, Czirok SJ, Szabo A, Lukats A, Szel A
. 2004 The arrangement of cerebrospinal fluid-contacting neurons. Its supposed part in the nonsynaptic betoken transmission of the brain. Histol. Histopathol. nineteen , 607-628. PubMed, ISI, Google Scholar
15.
Jékely G
. 2021 The chemical brain hypothesis for the origin of nervous systems. Phil. Trans. R. Soc. B 376 , 20190761. (doi:10.1098/rstb.2019.0761) Link, ISI, Google Scholar
16.
Arendt D, Nübler-Jung Thousand
. 1999 Comparison of early on nerve cord development in insects and vertebrates. Development 126 , 2309-2325. Crossref, PubMed, ISI, Google Scholar
17.
Jacobs DK, Nakanishi N, Yuan D, Camara A, Nichols SA, Hartenstein V
. 2007 Evolution of sensory structures in basal metazoa. Integr. Comp. Biol. 47 , 712-723. (doi:10.1093/icb/icm094) Crossref, PubMed, ISI, Google Scholar
18.
Arendt D
. 2008 The evolution of cell types in animals: emerging principles from molecular studies. Nat. Rev. Genet. ix , 868-882. (doi:10.1038/nrg2416) Crossref, PubMed, ISI, Google Scholar
19.
Moroz LL
. 2009 On the contained origins of complex brains and neurons. Encephalon Behav. Evol. 74 , 177-190. (doi:x.1159/000258665) Crossref, PubMed, ISI, Google Scholar
20.
Nakanishi N, Renfer E, Technau U, Rentzsch F
. 2012 Nervous systems of the body of water anemone Nematostella vectensis are generated by ectoderm and endoderm and shaped by distinct mechanisms. Development 139 , 347-357. (doi:x.1242/dev.071902) Crossref, PubMed, ISI, Google Scholar
21.
Arendt D
. 2016Evolution of neural prison cell types. In Structure and evolution of invertebrate nervous systems (eds A Schmidt-Rhaesa, Due south Harzsch, G Purschke), pp. eighteen–25. Oxford, UK: Oxford University Printing. Google Scholar
22.
Achim Thousandet al.
2018 Whole-torso single-jail cell sequencing reveals transcriptional domains in the annelid larval trunk. Mol. Biol. Evol. 35 , 1047-1062. (doi:ten.1093/molbev/msx336) Crossref, PubMed, ISI, Google Scholar
23.
Fincher CT, Wurtzel O, de Hoog T, Kravarik KM, Reddien Prisoner of war
. 2018 Cell blazon transcriptome atlas for the planarian Schmidtea mediterranea . Scientific discipline 360 , eaaq1736. (doi:x.1126/science.aaq1736) Crossref, PubMed, ISI, Google Scholar
24.
Plass Met al.
2018 Jail cell type atlas and lineage tree of a whole complex animal by single-cell transcriptomics. Science 360 , eaaq1723. (doi:ten.1126/science.aaq1723) Crossref, PubMed, ISI, Google Scholar
25.
Sebe-Pedros Aet al.
2018 Early metazoan cell blazon diversity and the evolution of multicellular gene regulation. Nat. Ecol. Evol. 2 , 1176-1188. (doi:10.1038/s41559-018-0575-6) Crossref, PubMed, ISI, Google Scholar
26.
Sebe-Pedros Aet al.
2018 Cnidarian cell type diversity and regulation revealed by whole-organism single-cell RNA-seq. Prison cell 173 , 1520-1534 e1520. (doi:10.1016/j.cell.2018.05.019) Crossref, PubMed, ISI, Google Scholar
27.
Musser JMet al.
. 2019Profiling cellular diversity in sponges informs animal cell blazon and nervous system evolution. bioRxiv 758276. (doi:10.1101/758276) Google Scholar
28.
Siebert S, Farrell JA, Cazet JF, Abeykoon Y, Primack Every bit, Schnitzler CE, Juliano CE
. 2019 Stem jail cell differentiation trajectories in Hydra resolved at single-jail cell resolution. Science 365 , eaav9314. (doi:ten.1126/science.aav9314) Crossref, PubMed, ISI, Google Scholar
29.
Cole AGet al.
2020Muscle prison cell type diversification facilitated by extensive gene duplications. bioRxiv 210658. (doi:10.1101/2020.07.nineteen.210658) Google Scholar
30.
Grimmelikhuijzen CJP
. 1983 FMRFamide immunoreactivity is generally occurring in the nervous systems of coelenterates. Histochemistry 78 , 361-381. (doi:x.1007/BF00496623) Crossref, PubMed, Google Scholar
31.
Anctil Chiliad
. 1985 Cholinergic and monoaminergic mechanisms associated with the control of bioluminescence in the ctenophore Mnemiopsis leidyi . J. Exp. Biol. 119 , 225-238. Crossref, ISI, Google Scholar
32.
Anctil K
. 1987 Bioactivity of FMRFamide and related peptides on a contractile system in the coelenterate Renilla koellikeri . J. Comp. Physiol. B 157 , 31-38. (doi:10.1007/BF00702725) Crossref, ISI, Google Scholar
33.
Emes RD, Grant SG
. 2012 Evolution of synapse complexity and diversity. Annu. Rev. Neurosci. 35 , 111-131. (doi:x.1146/annurev-neuro-062111-150433) Crossref, PubMed, ISI, Google Scholar
34.
Liebeskind BJ, Hillis DM, Zakon HH, Hofmann HA
. 2016 Complex homology and the evolution of nervous systems. Trends Ecol. Evol. 31 , 127-135. (doi:10.1016/j.tree.2015.12.005) Crossref, PubMed, ISI, Google Scholar
35.
Arendt D
. 2020 The evolutionary assembly of neuronal machinery. Curr. Biol. thirty , R603-R616. (doi:10.1016/j.cub.2020.04.008) Crossref, PubMed, ISI, Google Scholar
36.
Lentz TL
. 1966 Histochemical localization of neurohumors in a sponge. J. Exp. Zool. 162 , 171-180. (doi:x.1002/jez.1401620204) Crossref, Google Scholar
37.
Arendt D, Benito-Gutierrez E, Brunet T, Marlow H
. 2015 Gastric pouches and the mucociliary sole: setting the stage for nervous organisation evolution. Phil. Trans. R. Soc. B 370 , 20150286. (doi:x.1098/rstb.2015.0286) Link, ISI, Google Scholar
38.
Ramón y Cajal S
. 1899 Textura del sistema nervioso del hombre y de los vertebrados . Madrid, Spain: Consejo Superior de Investigationes Científicas. Google Scholar
39.
Westfall JA, Elliott CF, Carlin RW
. 2002 Ultrastructural show for two-prison cell and three-jail cell neural pathways in the tentacle epidermis of the ocean anemone Aiptasia pallida . J. Morphol. 251 , 83-92. (doi:10.1002/jmor.1075) Crossref, PubMed, ISI, Google Scholar
40.
Horridge GA
. 1964 Non-motile sensory cilia and neuromuscular junctions in a ctenophore independent effector organ. Proc. R. Soc. Lond. B 162 , 333-350. (doi:10.1098/rspb.1965.0042) ISI, Google Scholar
41.
Jékely G, Colombelli J, Hausen H, Guy Grand, Stelzer E, Nedelec F, Arendt D
. 2008 Machinery of phototaxis in marine zooplankton. Nature 456 , 395-399. (doi:ten.1038/nature07590) Crossref, PubMed, ISI, Google Scholar
42.
Randel North, Asadulina A, Bezares-Calderon LA, Veraszto C, Williams EA, Conzelmann M, Shahidi R, Jékely 1000
. 2014 Neuronal connectome of a sensory-motor circuit for visual navigation. Elife iii , e02730. (doi:10.7554/eLife.02730) Crossref, ISI, Google Scholar
43.
Bezares-Calderon LA, Berger J, Jasek S, Veraszto C, Mendes Due south, Guhmann Chiliad, Almeda R, Shahidi R, Jékely Thousand
. 2018 Neural circuitry of a polycystin-mediated hydrodynamic startle response for predator avoidance. Elife vii , e36262. (doi:10.7554/eLife.36262) Crossref, PubMed, ISI, Google Scholar
44.
Veraszto Cet al.
2018 Ciliary and rhabdomeric photoreceptor-cell circuits form a spectral depth gauge in marine zooplankton. Elife 7 , e36440. (doi:ten.7554/eLife.36440) Crossref, PubMed, ISI, Google Scholar
45.
Jager M, Chiori R, Alie A, Dayraud C, Queinnec East, Manuel Grand
. 2010 New insights on ctenophore neural anatomy: immunofluorescence study in Pleurobrachia pileus (Muller, 1776). J. Exp. Zool. B 316B, 171-187. (doi:10.1002/jez.b.21386) Crossref, Google Scholar
46.
Moroz LL
. 2015 Convergent evolution of neural systems in ctenophores. J. Exp. Biol. 218 , 598-611. (doi:10.1242/jeb.110692) Crossref, PubMed, ISI, Google Scholar
47.
Arendt D, Tosches MA, Marlow H
. 2015 From nerve net to nerve ring, nerve cord and brain—evolution of the nervous organisation. Nat. Rev. Neurosci. 17 , 61-72. (doi:10.1038/nrn.2015.15) Crossref, ISI, Google Scholar
48.
Grundfest H
. 1959Evolution of conduction in the nervous arrangement. In Evolution of nervous command from archaic organisms to man (ed. Advertizement Bass), pp. 43–86. Washington, DC: American Clan for the Advancement of Science. Google Scholar
49.
Horridge GA
. 1968The origins of the nervous organization. In The structure and role of nervous tissue, vol. 1 (ed. GH Bourne), pp. one–31. New York, NY: Academic Printing. Google Scholar
l.
Lentz TL
. 1968 Primitive nervous systems . New Haven, CT: Yale University Press. Google Scholar
51.
Sharon 1000, Sampson TR, Geschwind DH, Mazmanian SK
. 2016 The central nervous organization and the gut microbiome. Cell 167 , 915-932. (doi:ten.1016/j.cell.2016.10.027) Crossref, PubMed, ISI, Google Scholar
52.
Mackie GO
. 1990 The unproblematic nervous organization revisited. Am. Zool. thirty , 907-920. (doi:10.1093/icb/30.four.907) Crossref, Google Scholar
53.
Arendt D
. 2019 Many means to build a polyp. Trends Genet. 35 , 885-887. (doi:10.1016/j.tig.2019.09.003) Crossref, PubMed, ISI, Google Scholar
54.
Havrilak JA, Faltine-Gonzalez D, Wen Y, Fodera D, Simpson AC, Magie CR, Layden MJ
. 2017 Characterization of NvLWamide-like neurons reveals stereotypy in Nematostella nerve net development. Dev. Biol. 431 , 336-346. (doi:10.1016/j.ydbio.2017.08.028) Crossref, PubMed, ISI, Google Scholar
55.
Dupre C, Yuste R
. 2017 Not-overlapping neural networks in Hydra vulgaris . Curr. Biol. 27 , 1085-1097. (doi:10.1016/j.cub.2017.02.049) Crossref, PubMed, ISI, Google Scholar
56.
Keijzer F, van Duijn Chiliad, Lyon P
. 2013 What nervous systems practice: early evolution, input–output, and the skin encephalon thesis. Adapt. Behav. 21 , 67-85. (doi:10.1177/1059712312465330) Crossref, ISI, Google Scholar
57.
Jékely One thousand, Keijzer F, Godfrey-Smith P
. 2015 An option space for early neural evolution. Phil. Trans. R. Soc. B 370 , 20150181. (doi:x.1098/rstb.2015.0181) Link, ISI, Google Scholar
58.
Keijzer F, Arnellos A
. 2017 The animal sensorimotor organization: a challenge for the ecology complexity thesis. Biol. Philos. 32 , 421-441. (doi:10.1007/s10539-017-9565-3) Crossref, PubMed, ISI, Google Scholar
59.
Watanabe H, Fujisawa T, Holstein TW
. 2009 Cnidarians and the evolutionary origin of the nervous system. Dev. Growth Differ. 51 , 167-183. (doi:10.1111/j.1440-169X.2009.01103.x) Crossref, PubMed, ISI, Google Scholar
threescore.
McFarlane ID, Backyard ID
. 1972 Expansion and contraction of the oral disc in the body of water anemone Tealia felina . J. Exp. Biol. 57 , 633-649. Crossref, ISI, Google Scholar
61.
Cho K, McFarlane ID
. 1996 Physiological actions of the neuropeptide Antho-RNamide on antagonistic muscle systems in ocean anemones. Neurosci. Lett. 219 , 171-174. (doi:x.1016/S0304-3940(96)13193-1) Crossref, PubMed, ISI, Google Scholar
62.
Evans SD, Gehling JG, Droser ML
. 2019 Slime travelers: early evidence of beast mobility and feeding in an organic mat world. Geobiology 17 , 490-509. (doi:10.1111/gbi.12351) Crossref, PubMed, ISI, Google Scholar
63.
Ivantsov AY
. 2011 Feeding traces of proarticulata—the Vendian metazoa. Paleontol. J. 45 , 237-248. (doi:10.1134/S0031030111030063) Crossref, ISI, Google Scholar
64.
Sperling EA, Vinther J
. 2010 A placozoan analogousness for Dickinsonia and the evolution of late Proterozoic metazoan feeding modes. Evol. Dev. 12 , 201-209. (doi:10.1111/j.1525-142X.2010.00404.10) Crossref, PubMed, ISI, Google Scholar
65.
Jékely M
. 2013 Global view of the evolution and diversity of metazoan neuropeptide signaling. Proc. Natl Acad. Sci. USA 110 , 8702-8707. (doi:x.1073/pnas.1221833110) Crossref, PubMed, ISI, Google Scholar
66.
Elphick MR, Mirabeau O, Larhammar D
. 2018 Evolution of neuropeptide signalling systems. J. Exp. Biol. 221 , 151092. (doi:10.1242/jeb.151092) Crossref, ISI, Google Scholar
67.
Varoqueaux F, Williams EA, Grandemange South, Truscello L, Kamm Chiliad, Schierwater B, Jékely Thou, Fasshauer D
. 2018 High jail cell multifariousness and complex peptidergic signaling underlie placozoan behavior. Curr. Biol. 28 , 3495-3501; e3492. (doi:ten.1016/j.cub.2018.08.067) Crossref, PubMed, ISI, Google Scholar
68.
Vigh B, Vigh-Teichmann I
. 1982 Comparison between CSF-contacting neurons and cells of the radial nerve of some echinoderms. Verh. Anat. Ges. 76 , 461-463. Google Scholar
69.
Flood P
. 1966 A peculiar way of muscular innervation in amphioxus. J. Comp. Neurol. 126 , 181-218. (doi:10.1002/cne.901260204) Crossref, PubMed, ISI, Google Scholar
70.
Tessmar-Raible K, Raible F, Christodoulou F, Guy K, Rembold G, Hausen H, Arendt D
. 2007 Conserved sensory-neurosecretory cell types in annelid and fish forebrain: insights into hypothalamus evolution. Jail cell 129 , 1389-1400. (doi:ten.1016/j.cell.2007.04.041) Crossref, PubMed, ISI, Google Scholar
71.
He B, Buescher M, Farnworth MS, Strobl F, Stelzer EH, Koniszewski ND, Muehlen D, Bucher Grand
. 2019 An ancestral upmost brain region contributes to the central complex nether the command of foxQ2 in the beetle Tribolium . Elife 8 , e49065. (doi:10.7554/eLife.49065) Crossref, PubMed, ISI, Google Scholar
72.
Williams EA, Veraszto C, Jasek S, Conzelmann M, Shahidi R, Bauknecht P, Mirabeau O, Jékely Grand
. 2017 Synaptic and peptidergic connectome of a neurosecretory heart in the annelid brain. Elife 6 , e26349. (doi:10.7554/eLife.26349) Crossref, PubMed, ISI, Google Scholar
73.
Bayes A, van de Lagemaat LN, Collins MO, Croning MD, Whittle IR, Choudhary JS, Grant SG
. 2011 Characterization of the proteome, diseases and evolution of the human being postsynaptic density. Nat. Neurosci. 14 , 19-21. (doi:10.1038/nn.2719) Crossref, PubMed, ISI, Google Scholar
74.
Sudhof TC
. 2012 The presynaptic agile zone. Neuron 75 , eleven-25. (doi:10.1016/j.neuron.2012.06.012) Crossref, PubMed, ISI, Google Scholar
75.
Arendt Det al.
2016 Evolution of sister prison cell types by individuation. Nat. Rev. Genet. 17 , 744-757. (doi:x.1038/nrg.2016.127) Crossref, PubMed, ISI, Google Scholar
76.
Tarashansky AJ, Musser JM, Khariton Chiliad, Li P, Arendt D, Quake SR, Wang B
. 2020Mapping unmarried-cell atlases throughout Metazoa unravels jail cell blazon development. bioRxiv 317784. (doi:10.1101/2020.09.28.317784) Google Scholar
77.
Jahnel SM, Walzl M, Technau U
. 2014 Evolution and epithelial organization of muscle cells in the sea anemone Nematostella vectensis . Front end. Zool. 11 , 44. (doi:10.1186/1742-9994-11-44) Crossref, PubMed, ISI, Google Scholar
78.
Rieger RM, Ladurner P
. 2003 The significance of musculus cells for the origin of mesoderm in Bilateria. Integr. Comp. Biol. 43 , 47-54. (doi:x.1093/icb/43.i.47) Crossref, PubMed, ISI, Google Scholar
79.
Perillo M, Paganos P, Mattiello T, Cocurullo M, Oliveri P, Arnone MI
. 2018 New neuronal subtypes with a 'pre-pancreatic' signature in the sea urchin Stongylocentrotus purpuratus . Front. Endocrinol. (Lausanne) 9 , 650. (doi:10.3389/fendo.2018.00650) Crossref, PubMed, ISI, Google Scholar
fourscore.
Alaynick WA, Jessell TM, Pfaff SL
. 2011 SnapShot: spinal cord development. Cell 146 , 178-178; e171. (doi:10.1016/j.cell.2011.06.038) Crossref, PubMed, ISI, Google Scholar
81.
Arda HE, Benitez CM, Kim SK
. 2013 Factor regulatory networks governing pancreas evolution. Dev. Cell 25 , 5-13. (doi:ten.1016/j.devcel.2013.03.016) Crossref, PubMed, ISI, Google Scholar
82.
Musser JMet al.
2019 Profiling cellular diversity in sponges informs animal cell type and nervous organisation development. bioRxiv 758276. (doi:ten.1101/758276) Google Scholar
83.
Jékely G, Godfrey-Smith P, Keijzer F
. 2021 Reafference and the origin of the self in early on nervous arrangement development. Phil. Trans. R. Soc. B 376 , 20190764. (doi:10.1098/rstb.2019.0764) Link, ISI, Google Scholar

hayesinupoppeired.blogspot.com

Source: https://royalsocietypublishing.org/doi/10.1098/rstb.2020.0347

Hayes Inupoppeired