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WIREs Dev Biol
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The central nervous system of ascidian larvae

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Ascidians are marine invertebrate chordates. Their tadpole larvae contain a dorsal tubular nervous system, resulting from the rolling up of a neural plate. Along the anterior–posterior (A‐P) axis, the central nervous system (CNS) is organized into a sensory vesicle, neck, trunk ganglion, and tail nerve cord and consists of approximately only 330 cells, of which around 100 are thought to be neurons. The organization of distinct neuronal cell types and neurotransmitter gene expression within the CNS has been described. The unique developmental mode of ascidians, with a small number of cells and a fixed cell division pattern, allows individual cells to be traced throughout development. This feature has led to the complete documentation of the cell lineages of certain cell types in the CNS. Thus, a step‐by‐step understanding of nervous system development from the initial stages of neural induction to the neurogenesis of individual neurons is a feasible goal. The genetic control of neural fate induction and early neural plate patterning are now well understood. The molecular mechanisms specifying the cholinergic neurons of the trunk ganglion as well as the pigment cells of the sensory organs are also well elucidated. In addition, studies have begun on the morphogenetic processes of neurulation. Remaining challenges include building an embryonic atlas integrating gene expression patterns, cell lineage, and neuronal cell types as well as developing the gene regulatory networks of cell fate specification and integrating them with the genetic control of morphogenesis. WIREs Dev Biol 2016, 5:538–561. doi: 10.1002/wdev.239

Cells of the nervous system. Highly schematized drawings of the larva and its neurons. Anterior is to the left. (a) The central nervous system. I, II, and III refer to the three types of photoreceptors with the position of their outer segments shown by red dots. Abbreviations are as follows: Oc, ocellus; Ls, lens cells; Ot, otolith; ac, antennal cells; cc, coronet cells; ec, eminens cell; L1, large ventroposterior interneuron; cp, contrapelo cells; cholinergic, the five pairs of ventrolateral cholinergic trunk ganglion neurons [including confirmed motoneurons (mn)]; on, ovoid neuron; ACIN, anterior caudal inhibitory neurons; pn, planate neurons. For the cholinergic and ACIN neurons, only one side is shown, but these neurons appear in pairs on both sides of the larvae (left and right). Below the central nervous system (CNS) drawing are the cholinergic neurons found in the ventrolateral trunk ganglion and their signature gene expression. A11.117 is characterized by cell body neurites as depicted. During larval development the A11.118 moves around the A11.117 cell with a ventral trajectory and finishes posterior to the A11.117 cell. (b) The peripheral nervous system. Abbreviations are as follows: pn, palp neurons; RTEN, rostral trunk epidermal neurons; ATEN, apical trunk epidermal neurons (a, anterior; p, posterior); CEN, caudal epidermal neurons (d, dorsal; v, ventral); BTN, bipolar tail neuron.
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Cell lineages of the cholinergic trunk ganglion neurons and anterior caudal inhibitory neurons. Cell lineages of A9.16, A9.30, and A9.29 from the six‐row neural plate stage until the birth of the cholinergic trunk ganglion neurons. A9.16 lineages are colored in yellow; A9.30 in tan; and A9.29 in brown. (a) Six‐row neural plate stage. (b) Neurula stage, note the A9.30 derivatives (A10.60, A10.59, tan) are now positioned posteriorly to the A9.16 derivatives (A10.32, A10.31, yellow). A10.57 is now postmitotic. (c) Drawing of an early tailbud stage embryo showing positions of these lineages in the lateral part of the posterior sensory vesicle (pSV), neck, trunk ganglion (tg), and tail nerve cord (tnc). A10.57 has moved into a ventrolateral position of the neural tube. A11.117 and A11.118 are now postmitotic. Below the embryo drawing are the further lineages of the column 3 cells (tan and brown) up until the stage when the five pairs of postmitotic cholinergic neurons are born. Only one side of the embryonic lineages are shown in lateral view. Noncholinergic neurons have been rendered partially transparent to highlight the neurons. Note A12.239 has now shifted ventrally and A11.118 shifts ventrally and posteriorly around A11.117. While A10.57 is depicted in the ‘tail nerve cord’ domain, it will finally reside in the trunk ganglion just posterior to A11.118/A11.117. (Early tailbud drawing: Reprinted with permission from Ref . Copyright 2009 Company of Biologists). Cell lineages and positions in (a) and (b) are drawn from observations described by Nicol and Meinertzhagen and lineages and positions in (c) follow those described by Cole and Meinertzhagen.
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Lineages of the central nervous system. (a) At the top is a photograph of a larval trunk and anterior part of the tail. The sensory vesicle is outlined with a dotted line. The two pigmented cells can clearly be seen (otolith anterior). The tail nerve cord, situated between the dorsal epidermis and notochord (No), is not visible owing to its very small size. Below the photo is a drawing in lateral view of an ascidian larval central nervous system (CNS) showing the sensory vesicle, neck, trunk ganglion, and tail nerve cord. For illustration, the CNS has been greatly enlarged within the larvae. The tail is truncated in this and all subsequent figures. To the right of the larva is shown a transverse section of the tail showing the organization of the nerve cord (colored), muscles (M), notochord (No), and endoderm (E). Below the larva are gene expression domains in the CNS represented by bars and, on the right, the corresponding region of the vertebrate CNS. (a–g) Although ascidian embryos are conventionally drawn in either vegetal or animal view with anterior up, the embryos drawings here are all shown with anterior to the left to maintain consistency throughout the figure. Lineages are identical on each side of the bilaterally symmetrical embryo. The side from which the embryo is viewed is indicated. Sister cell relationships are indicated by bars connecting the cells. The color code is as follows: red: a‐line lineage CNS‐fate restricted; pink: a‐line CNS lineages before fate restriction; gray: anterior non‐CNS a‐line neural plate; yellow: medial A‐line neural plate derivatives; tan: lateral A‐line neural plate derivatives; pale tan: A‐line neural lineages before neural fate restriction; green: b‐line CNS; pale green: b‐line neural lineages before fate restriction. Note: posterior–lateral A‐line ‘CNS lineages’ also contribute to muscle. For simplicity, this lineage is considered as ‘neural fate restricted’ here. The contribution of the posterior‐most b‐line (pale green in f–g) is not resolved. An asterisk marks the anterior‐most border of the CNS. Major events in CNS development are indicated below the drawings. The arrows on (d) indicate the FGF neural inducing signals. (g) On the right of the neural plate stage embryo drawing is a schematic representation of the neural plate. The neural plate is a grid‐like organization of cells aligned in four columns whereby column 1 is the medial‐most column and column 4 the lateral‐most. The six rows are named rows I to VI with row I the posterior most. ‘M’ is the muscle cell that derives from the A‐line neural lineages. Below the drawings is a six‐row stage embryo with nuclear staining. Nuclei are colored according to the lineages shown in the figure. (Larval drawing: Reprinted with permission from Ref . Copyright 2005 Company of Biologists; 112‐cell and neural plate drawings: Reprinted with permission from Ref . Copyright 2014 Elsevier). All other embryos were drawn with help from 3D virtual embryo.
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Patterning of the A‐line neural lineages up to neural plate stage. (a) All embryos shown in vegetal pole view. The anterior–posterior (A‐P) axis corresponds to the developing central nervous system (CNS). At the 32‐ to 64‐cell stage, Nodal induces lateral (columns 3 and 4) over medial (columns 1 and 2) neural fate and induces Delta‐like expression in a lateral domain. At the 64‐ to 76‐cell stage, Delta‐like/Notch signals induce column 4 fate. By the early gastrula stage, Delta‐like is now expressed in the lateral A‐line neural precursors themselves and induces column 2 over column 1 fate. At the six‐row neural plate stage, differential activation of ERK1/2 along the A‐P axis specifies row I over row II fates. Columns and rows are indicated on the schematics. M indicates the muscle cell that derives from the A‐line neural plate. (b) Summary of A‐line neural plate patterning. Each cell receives a unique combination of signals, which specifies its distinct cell identity.
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Patterning of the a‐line neural lineages. (a) Anterior is up, all embryos shown in dorsal (developing neural plate) view. a‐Lineages of the central nervous system (CNS) are shown in pink at the 64‐cell stage and red from fate restriction at the 112‐cell to neurula stages. At tailbud stages only the pigment cell precursors are shown. On the drawings, the pigment cell lineages are marked with a star. Below the drawings are schematics of a‐line neural cells with ERK1/2 activation shown by black dots. Each division of these cells takes place along the anterior–posterior axis. Sister cell relationships are shown by bars on the left‐hand side of the embryo drawings. On the far right drawing of a tailbud stage embryo, the Wnt7‐expressing dorsal neural tube is depicted by a green bar. The cell fate choices taking place are indicated below the schematics. Neural induction refers to the continuation of the neural induction process that began at the 32‐cell stage. (Reprinted with permission from Ref . Copyright 2014 Elsevier). (b) The role of Nodal during ocellus development. The photographs show a normal larva with the ocellus pigmented cell to the right side of the embryo and the photoreceptors (fluorescent color) to the right of the ocellus pigmented cell. When Nodal signals are inhibited, the ocellus becomes symmetrical, the pigmented cell stays in the center of the larva, and the photoreceptors form on both the left and the right. The schematic describes the role of Nodal during ocellus patterning. The double‐headed arrow represents Nodal‐dependent movement of the ocellus pigment cell to the right‐hand side of the sensory vesicle. Rx, Opsin1 and Arrestin genes are all expressed in the photoreceptors. (Reprinted with permission from Ref . Copyright 2011 Elsevier)
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Comparable fate maps between ascidians and vertebrates at the pregastrula stage. Lateral views of a Xenopus (frog) and ascidian embryo, with notochord forming side (traditionally termed ‘dorsal’) to the left. (Reprinted with permission from Ref . Copyright 2008 Elsevier)
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Patterning of the A‐line lineages: column 3 neurons. (a) The right‐hand side of the A‐line neural plate and its combinatorial signaling code is indicated. The A9.30 and A9.29 sister cells are colored in tan. (b) Only one side of the bilaterally symmetrical embryo is shown. Cellular interactions and part of the known gene regulatory network during the step‐by‐step specification of the five pairs of cholinergic neurons of the trunk ganglion are shown. The ACINs derive from A11.116 lineage. Cells that leave the cholinergic lineage are not colored. Circled cells indicate the postmitotic cholinergic neurons. White squares represent cell lineages that remain mitotic at least until the 13th cell division.
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Peripheral nervous system (PNS) lineages and the neural plate border cells. Anterior to the left. M, muscle cells. The yellow dashed line delimits the central nervous system (CNS) neural plate (including the A‐line‐derived muscle cell, M, and the posterior b9.33 lineage of which its contribution to the CNS is not resolved). Lineages are identical on both sides of the bilaterally symmetrical embryo. (a) Lineages of the PNS neurons are indicated by labels and different colors. The color code is: gray (medial) and pink (lateral): a‐line non‐CNS anterior neural plate; light blue: lateral b6.5 derivatives; dark blue: posterior b‐line. The aATEN lineage arises from the anterior lateral non‐CNS neural plate in Ciona as do both the aATENs and pATENs in Halocynthia (the pATEN lineage has not yet been delineated in Ciona). The RTEN lineages are described only in Halocynthia (Hr). Note the majority of PNS neurons arise from cells surrounding the CNS neural plate. In contrast, the vCEN lineage is found in the ventral epidermis on the other side of the embryo, far from the neural plate. Below the drawing is a cross section of a neural plate stage embryo showing the position of the ventral epidermal sensory neuron lineages compared to the neural plate. (Cross section photo: Reprinted with permission from Ref . Copyright 2002 Company of Biologists). (b) The border cells described by Stolfi et al., outlined in red on one side of the embryo. The border cells include the lateral a‐line non‐CNS neural plate (including the aATEN lineage), the lateral a‐line CNS (including pigmented cells), and the entire b6.5‐cell derivatives (dCEN, b‐line CNS, b‐line muscle). Color code is as above, except the posterior neural border (in dark blue) includes the posterior‐most b6.5 lineage. (Embryo drawing: Reprinted with permission from Ref . Copyright 2015 Elsevier)
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Patterning of the A‐line lineages: the posterior sensory vesicle versus neck fate choice is governed by Fgf8. (a) The right‐hand side of the A‐line neural plate and its combinatorial signaling code is indicated. The A9.16 (yellow) and A9.30 (tan) cells are colored. (b) Only one side of the bilaterally symmetrical embryo is shown. Interactions between the descendants of A9.16 and A9.30 govern the gene regulatory network that specifies neck over posterior sensory vesicle fate. During later stages of development, the Pax2/5/8a+ domain subdivides into a Pax2/5/8a+/Hox+ and a Pax2/5/8a+/Hox− domain. Fgf8, Fgf8/17/18.
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Gene Expression and Transcriptional Hierarchies > Gene Networks and Genomics
Signaling Pathways > Cell Fate Signaling
Early Embryonic Development > Development to the Basic Body Plan

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