Invertebrate nervous systems are highly disparate between different taxa. This is reflected in the terminology used to describe them, which is very rich and often confusing. Even very general terms such as 'brain', 'nerve', and 'eye' have been used in various ways in the different animal groups, but no consensus on the exact meaning exists. This impedes our understanding of the architecture of the invertebrate nervous system in general and of evolutionary transformations of nervous system characters between different taxa. We provide a glossary of invertebrate neuroanatomical terms with a precise and consistent terminology, taxon-independent and free of homology assumptions. This terminology is intended to form a basis for new morphological descriptions. A total of 47 terms are defined. Each entry consists of a definition, discouraged terms, and a background/comment section. The use of our revised neuroanatomical terminology in any new descriptions of the anatomy of invertebrate nervous systems will improve the comparability of this organ system and its substructures between the various taxa, and finally even lead to better and more robust homology hypotheses.

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Invertebrate neurophylogeny: suggested terms and definitions for a neuroanatomical glossary

The simplest animal eyes are eyespots composed of two cells only: a photoreceptor and a shading pigment cell They resemble Darwin's 'proto-eyes', considered to be the first eyes to appear in animal evolution Eyespots cannot form images but enable the animal to sense the direction of light They are characteristic for the zooplankton larvae of marine invertebrates and are thought to mediate larval swimming towards the light Phototaxis of invertebrate larvae contributes to the vertical migration of marine plankton, which is thought to represent the biggest biomass transport on Earth Yet, despite its ecological and evolutionary importance, the mechanism by which eyespots regulate phototaxis is poorly understood Here we show how simple eyespots in marine zooplankton mediate phototactic swimming, using the marine annelid Platynereis dumerilii as a model We find that the selective illumination of one eyespot changes the beating of adjacent cilia by direct cholinergic innervation resulting in locally reduced water flow Computer simulations of larval swimming show that these local effects are sufficient to direct the helical swimming trajectories towards the light The computer model also shows that axial rotation of the larval body is essential for phototaxis and that helical swimming increases the precision of navigation These results provide, to our knowledge, the first mechanistic understanding of phototaxis in a marine zooplankton larva and show how simple eyespots regulate it We propose that the underlying direct coupling of light sensing and ciliary locomotor control was a principal feature of the proto-eye and an important landmark in the evolution of animal eyes

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Mechanism of phototaxis in marine zooplankton

The role of Pax6 in eye development in insects and vertebrates supports the view that their eyes evolved from simple pigment-cup ocelli present in their last common ancestors (Urbilateria). The cerebral eyes in errant polychaetes represent prototype invertebrate pigment-cup ocelli and thus resemble the presumed ancestral eyes. We have analysed expression of conserved eye specification genes in the early development of larval and adult pigment-cup eyes in Platynereis dumerilii (Polychaeta, Annelida, Lophotrochozoa). Both larval and adult eyes form in close vicinity of the optic anlagen on both sides of the developing brain ganglia. While pax6 is expressed in the larval, but not in the developing, adult eyes, expression of six1/2 from trochophora stages onwards specifically outlines the optic anlagen and thus covers both the developing larval and adult eyes. Using Platynereis rhabdomeric opsin as differentiation marker, we show that the first pair of adult eye photoreceptor cells is detected within bilateral clusters that transitorily express ath, the Platynereis atonal orthologue, thus resembling proneural sensory clusters. Our data indicate that--similar to insects, but different from the vertebrates--polychaete six1/2 expression outlines the entire visual system from early developmental stages onwards and ath-positive clusters generate the first photoreceptor cells to appear. We propose that pax6-, six1/2- and ath-positive larval eyes, as found in today's trochophora, were present already in Urbilateria.

Development of pigment-cup eyes in the polychaete Platynereis dumerilii and evolutionary conservation of larval eyes in Bilateria

The shared roles of Pax6 and Six homologues in the eye development of various bilaterians suggest that Urbilateria, the common ancestors of all Bilateria, already possessed some simple form of eyes. Here, we re-address the homology of bilaterian cerebral eyes at the level of eye anatomy, of eye-constituting cell types and of phototransductory molecules. The most widespread eye type found in Bilateria are the larval pigment-cup eyes located to the left and right of the apical organ in primary, ciliary larvae of Protostomia and Deuterostomia. They can be as simple as comprising a single pigment cell and a single photoreceptor cell in inverse orientation. Another more elaborate type of cerebral pigment-cup eyes with an everse arrangement of photoreceptor cells is found in adult Protostomia. Both inverse larval and everse adult eyes employ rhabdomeric photoreceptor cells and thus differ from the chordate cerebral eyes with ciliary photoreceptors. This is highly significant because on the molecular level we find that for phototransduction rhabdomeric versus ciliary photoreceptor cells employ divergent rhodopsins and non-orthologous G-proteins, rhodopsin kinases and arrestins. Our comparison supports homology of cerebral eyes in Protostomia; it challenges, however, homology of chordate and non-chordate cerebral eyes that employ photoreceptor cells with non-orthologous phototransductory cascades.

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Reconstructing the eyes of Urbilateria.

The polychaete annelid Platynereis dumerilii is an emerging model organism for the study of molecular developmental processes, evolution, neurobiology and marine biology. Annelids belong to the Lophotrochozoa, the so far understudied third major branch of bilaterian animals besides deuterostomes and ecdysozoans. P. dumerilii has proven highly relevant to explore ancient bilaterian conditions via comparison to the deuterostomes, because it has accumulated less evolutionary change than conventional ecdysozoan models. Previous staging was mainly referring to hours post fertilization but did not allow matching stages between studies performed at (even slightly) different temperatures. To overcome this, and to provide a first comprehensive description of P. dumerilii normal development, a temperature-independent staging system is needed. Platynereis dumerilii normal development is subdivided into 16 stages, starting with the zygote and ending with the death of the mature worms after delivering their gametes. The stages described can be easily identified by conventional light microscopy or even by dissecting scope. Developmental landmarks such as the beginning of phototaxis, the visibility of the stomodeal opening and of the chaetae, the first occurrence of the ciliary bands, the formation of the parapodia, the extension of antennae and cirri, the onset of feeding and other characteristics are used to define different developmental stages. The morphology of all larval stages as well as of juveniles and adults is documented by light microscopy. We also provide an overview of important steps in the development of the nervous system and of the musculature, using fluorescent labeling techniques and confocal laser-scanning microscopy. Timing of each developmental stage refers to hours post fertilization at 18 ± 0.1°C. For comparison, we determined the pace of development of larvae raised at 14°C, 16°C, 20°C, 25°C, 28°C and 30°C. A staging ontology representing the comprehensive list of developmental stages of P. dumerilii is available online. Our atlas of Platynereis dumerilii normal development represents an important resource for the growing Platynereis community and can also be applied to other nereidid annelids.

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The normal development of Platynereis dumerilii (Nereididae, Annelida)

The nereid polychaete, Platynereis dumerilii, possess two pairs of post-trochophoral eyes with one vitreous body each. The development of these eyes has first been observed in 2-day-old larvae. Whether the eye anlagen arise from stem cells or from undifferentiated ectodermal tissue was not determined. At first, the anlagen of the anterior and the posterior eyes adjoin each other. They separate in late 3-day-old larvae. The first separated eye complexes consist each of two supporting and two sensory cells. The supporting cells synthesize two different kinds of granules, the pigment granules of the pigment cup and the prospective tubules of the vitreous body. These tubules accumulate in the distal process of the supporting cell. The vitreous body is formed by compartments of the supporting cells filled with the osmiophilic vitreous body tubules. The short, bulbar photosensory processes bear microvilli that emerge into the ocular cavity. At the apex of each sensory cell process, a single cilium (or occasionally two) arises. The sensory cells contain a different kind of pigment granule within their necks at the level of the pigment cup. The rate of eye development and differentiation varies. New supporting cells are added to the rim of the eye cup. They contribute to the periphery of the vitreous body like onion skins, and sensory cells move between supporting cells. The older the individual compartments of the vitreous body are, the more densely packed is their content of vitreous body tubules. Elongation of the sensory and supporting cell processes of the older cells increases the volume of the eye. The eyespots of the trochophore are briefly described as of the two-celled rhabdomeric type with a single basal body with ciliary rootlet.

Development and differentiation of the eye in Platynereis dumerilii (Annelida, Polychaeta)

Larval and adult eyes of the capitellid Capitella spec. I have been investigated by electron microscopy. Developing larvae possess one pair of eyespots. Each eyespot is composed of one sensory cell, one pigment cell, and one supporting cell. The sensory cell bears a photosensory apparatus, an array of parallel microvilli containing a striking form of submicrovillar cisternae (SMC). A single basal body was observed near the basal end of the SMC only in 3–4-day-old larvae. This basal body was not observed in older larvae. A special, thus far unreported feature of the pigment cell is a ring of microvilli-like structures that project from the edge of the pigment cup and form a kind of diaphragm around the head of the sensory cell. Each of these microvilli-like structures is covered with closely packed rows of tiny plates, giving them a fimbriated appearance. After metamorphosis, the larval eyespots are reduced.



Adult specimens possess one pair of eyes. In juvenile worms the eye is built of 2–3 pigment cells and one sensory cell. The volume of adult eyes increases by the addition of 2–3 sensory cells. The pigment cells are deposited one upon the other, wrapping the sensory complex in the center. Each sensory cell forms a deep depression at its apical end where up to three cilia and numerous microvilli arise. The sensory processes project into a common ocular cavity. Long microvilli of the uppermost pigment cells project into an extracellular channel that reaches from the ocular cavity up to the cuticle. A single fourth sensory cell of identical structure may occur next to the eye directly beneath the cuticle and close to the opening of the ocular channel.



Signs of progressive disintegration of the pigment cells can be observed in adult specimens. Sensory cells are not affected by this reduction process. Eyes resembling those of Capitella spec. I have never been reported before. Their functional qualities are discussed. © 1993 Wiley-Liss, Inc.

Larval and adult eyes in Capitella spec. I (Annelida, Polychaeta)

Polychaetes normally possess one pair of nuchal organs at the posterior edge of the prostomium or peristomium. They have been regarded as chemosensory organs. The nuchal organs of four marine polychaete species with different habits were investigated by electron microscopy. Although the shapes of nuchal organs can vary greatly from simple ciliary bands (Scolelepis squamata, Spionidae) to retractile tongue-like, piston- or finger-shaped forms (Eteone longa, Anaitides mucosa, Phyllodocidae; Heteromastus filiformis, Capitellidae), the structural components, including the ciliated supporting cells, sensory cells, and nuchal epidermal cells, are essentially similar. The differences basically concern 1) the position of the sensory cells with relation to the ciliated supporting cells, 2) the location and structure of the nuchal nerve, and 3) the structure of the nuchal cuticle. The diverging nature of this modified cuticle is described and discussed in detail. Comparisons are made with the fine structure of nuchal organs of other polychaete species. Similarities of cellular components of nuchal organs are found not only in the four species studied here but also in all nuchal organs investigated so far. This is hypothesized to be due to the fact that the polychaete stem species already possessed nuchal organs with the respective cell types. Differences in the number and distribution of cellular components and in the overall shape of nuchal organs are thought to have evolved in correlation with the equipment of other cephalic appendages and with different habits and modes of nutrition.

Ultrastructure of nuchal organs in some marine polychaetes

The photoreceptors of four polychaete species were investigated by transmission electron microscopy: Eteone longa and Anaitides mucosa (Phyllodocidae), Scolelepis squamata (Spionidae), and Heteromastus filiformis (Capitellidae). Four different types of light-sensitive organs could be distinguished: 1) a simple, unpigmented rhabdomeric type; 2) a simple ocellus composed of a sensory and a pigmented cell; 3) complex eyes with a lens consisting of secretory granules; 4) a simple, unpigmented type with modified cilia. In spite of its simpler organization the fourth type is listed last, because its function as a photoreceptor seems dubious.



The first type (unpigmented rhabdomeric receptor) occurs in all four species investigated. It is the only type of photoreceptor in Heteromastus. Additionally, the two phyllodocids Eteone and Anaitides possess another kind of receptor (type 4) in close proximity to the type 1 receptor. Simple ocelli (type 2) are found in Scolelepis. A pair of complex eyes (type 3) is present in both Eteone and Anaitides, but they show important differences in the two species. First, the eyes in Eteone exhibit ciliary rudiments within the sensory processes, but such rudiments are absent in the eyes of Anaitides. Secondly, the sensory cells in Anaitides possess pigment granules, whereas in Eteone they do not. Thirdly, the lens in Eteone is composed of secretion granules of equal electron density, whereas in Anaitides the lens granules show increased electron density centrally. Lens material appears to be secreted from a single corneal cell in Eteone, and from several corneal cells in Anaitides. In both species these corneal cells are located distally outside the lens.

Ultrastructure of prostomial photoreceptors in four marine polychaete species (annelida).

The protandric hermaphrodite Ophryotrocha puerilis possesses one pair of eyes. They are located in the peristomium. Each light-sensitive organ consists of one sensory cell and one to two supporting cell(s) embedded in a cup-shaped reflector. The sensory-supporting cell complex is enveloped by a basal lamina. This lamina is supposed to be identical with the neural lamella. Thus the eyes proper have to be regarded as protrusions from the brain, while epidermal cells seem to differentiate to crystalline cells (reflector) and are deposited onto the sensory complex.



The reflector is built up by several cup-shaped cells (juveniles, 4–5; adults, 10–12). Each of these cells comprises a multilayer of parallel-oriented, membrane-bound crystalline platelets which are thought to be guanine. The sensory cell is of the inverted rhabdomere type. Submicrovillar cisternae, typical for most polychaete eyes, are lacking. The first and always present supporting cell entirely envelops the sensory cell, thus forming the extracellular space around the rhabdomere. It does not contain any pigment granules. Often but not always a second supporting cell has been observed surrounding the sensory cell and first supporting cell. It is interpreted as a glial cell.



In the sensory cell beneath the rhabdomere, pino- and phagocytosis can be observed and secondary lysosomes are found in high densities. Preliminary results seem to demonstrate that there is no distinct diurnal cycle of receptoral membrane recycling. In comparison with the ocelli of Dinophilidae, which have been interpreted as a dorvilleid-related family, morphological differences and their application to phylogenetic considerations are discussed.

Birgit Rhode

Papers

Development and differentiation of the eye in Platynereis dumerilii (Annelida, Polychaeta)

Larval and adult eyes in Capitella spec. I (Annelida, Polychaeta)

Ultrastructure of nuchal organs in some marine polychaetes

Ultrastructure of prostomial photoreceptors in four marine polychaete species (annelida).

Eye structure of Ophryotrocha puerilis (Polychaeta: Dorvilleidae)