Progressive neurogenesis defines lateralis somatotopy

Pujol-Martí, Jesús; Baudoin, Jean-Pierre; Faucherre, Adèle; Kawakami, Koichi; López‐Schier, Hernán

doi:10.1002/dvdy.22320

Cited by 25 publications

(26 citation statements)

References 40 publications

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“…Using a Gal4 enhancer trap line for rspo2 (hspGFFDMC131A) (24), we observed intense labeling in the dorsalmost neurons of the PLL ganglion (Fig. 4G), corresponding to the neurons that innervate the terminal neuromasts (25,26). Using the same transgenic combination to detect the axons of rspo2-expressing neurons, we found that at 7 dpf, shortly before the formation of the bud-neuromast ter2′, the axons innervating ter1 and ter2 express GFP (Fig.…”

Section: Resultsmentioning

confidence: 96%

“…For imaging, embryos were anesthetized with Tricain (3-amino Labeling and Imaging. Single-neuron labeling was achieved through plasmid injection in fertilized eggs, as previously described (25), using a Huc:memTdTomato construct (26). Tuna embryos were simultaneously labeled for actin by phalloidin labeling and for acetylated tubulin by immunolabeling, as described previously (37).…”

Section: Methodsmentioning

confidence: 99%

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Innervation is required for sense organ development in the lateral line system of adult zebrafish

Wada

Dambly‐Chaudière

Kawakami

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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Superficial mechanosensory organs (neuromasts) distributed over the head and body of fishes and amphibians form the "lateral line" system. During zebrafish adulthood, each neuromast of the body (posterior lateral line system, or PLL) produces "accessory" neuromasts that remain tightly clustered, thereby increasing the total number of PLL neuromasts by a factor of more than 10. This expansion is achieved by a budding process and is accompanied by branches of the afferent nerve that innervates the founder neuromast. Here we show that innervation is essential for the budding process, in complete contrast with the development of the embryonic PLL, where innervation is entirely dispensable. To obtain insight into the molecular mechanisms that underlie the budding process, we focused on the terminal system that develops at the posterior tip of the body and on the caudal fin. In this subset of PLL neuromasts, bud neuromasts form in a reproducible sequence over a few days, much faster than for other PLL neuromasts. We show that wingless/int (Wnt) signaling takes place during, and is required for, the budding process. We also show that the Wnt activator R-spondin is expressed by the axons that innervate budding neuromasts. We propose that the axon triggers Wnt signaling, which itself is involved in the proliferative phase that leads to bud formation. Finally, we show that innervation is required not only for budding, but also for long-term maintenance of all PLL neuromasts.Lgr | post-embryonic development | Thunnus thynnus | Danio rerio

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Section: Resultsmentioning

confidence: 96%

Section: Methodsmentioning

confidence: 99%

Innervation is required for sense organ development in the lateral line system of adult zebrafish

Wada

Dambly‐Chaudière

Kawakami

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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“…It is conceivable that this reduction reflects a specific defect in the leading afferent neurons. The leading axons that arborize extensively within the migrating primordium, and later innervate the posteriormost neuromasts (8), are extended by the earliest differentiating afferent neurons (27). A simple explanation for precocious nerve arrest would therefore be a deficit in those early neurons.…”

Section: Resultsmentioning

confidence: 99%

“…We relied on somite number, which is an accurate measure of developmental age, to asses the timing of afferent development. The earliest PLL differentiating neurons, as visualized in the Huc:kaede reporter line, can be detected around the 18-somite stage (27). We examined the presence of fluorescent cells in the PLL ganglion of 0.15 mM ret1-MO2, Huc:kaede embryos from the 18-to 20-somite stage.…”

Section: Resultsmentioning

confidence: 99%

Glial cell line-derived neurotrophic factor defines the path of developing and regenerating axons in the lateral line system of zebrafish

Schuster

Dambly‐Chaudière

Ghysen

2010

Proc. Natl. Acad. Sci. U.S.A.

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How the peripheral axons of sensory neurons are guided to distant target organs is not well understood. Here we examine this question in the case of the posterior lateral line (PLL) system of zebrafish, where sensory organs are deposited by a migrating primordium. Sensory neurites accompany this primordium during its migration and are thereby guided to their prospective target organs. We show that the inactivation of glial cell line-derived neurotrophic factor (GDNF) signaling leads to defects of innervation and that these defects are due to the inability of sensory axons to track the migrating primordium. GDNF signaling is also used as a guidance cue during axonal regeneration following nerve cut. We conclude that GDNF is a major determinant of directed neuritic growth and of target finding in this system, and we propose that GDNF acts by promoting local neurite outgrowth.axonal guidance | nerve regeneration | posterior lateral line | RET

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“…Zebrafish were maintained under standardized conditions and experiments were conducted in embryos of un-determined sex in accordance with protocols approved by the Parc de Recerca Biomèdica de Barcelona's Ethical Committee of Animal Experimentation. Tg [HuC:Kaede], HGn39D, and hspGFF53A transgenic lines have been published previously (Sato et al, 2006;Faucherre et al, 2009;Pujol-Martí et al, 2010). The hspGFFDMC130A was generated by random integration of an enhancer-trap construct .…”

Section: Methodsmentioning

confidence: 99%

Neuronal Birth Order Identifies a Dimorphic Sensorineural Map

Pujol-Martí¹,

Zecca²,

Baudoin³

et al. 2012

J. Neurosci.

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Spatially distributed sensory information is topographically mapped in the brain by point-to-point correspondence of connections between peripheral receptors and central target neurons. In fishes, for example, the axonal projections from the mechanosensory lateral line organize a somatotopic neural map. The lateral line provides hydrodynamic information for intricate behaviors such as navigation and prey detection. It also mediates fast startle reactions triggered by the Mauthner cell. However, it is not known how the lateralis neural map is built to subserve these contrasting behaviors. Here we reveal that birth order diversifies lateralis afferent neurons in the zebrafish. We demonstrate that early-and late-born lateralis afferents diverge along the main axes of the hindbrain to synapse with hundreds of second-order targets. However, early-born afferents projecting from primary neuromasts also assemble a separate map by converging on the lateral dendrite of the Mauthner cell, whereas projections from secondary neuromasts never make physical contact with the Mauthner cell. We also show that neuronal diversity and map topology occur normally in animals permanently deprived of mechanosensory activity. We conclude that neuronal birth order correlates with the assembly of neural submaps, whose combination is likely to govern appropriate behavioral reactions to the sensory context.

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Progressive neurogenesis defines lateralis somatotopy

Cited by 25 publications

References 40 publications

Innervation is required for sense organ development in the lateral line system of adult zebrafish

Innervation is required for sense organ development in the lateral line system of adult zebrafish

Glial cell line-derived neurotrophic factor defines the path of developing and regenerating axons in the lateral line system of zebrafish

Neuronal Birth Order Identifies a Dimorphic Sensorineural Map

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