Single‐cell analysis of somatotopic map formation in the zebrafish lateral line system

Sato, Akira; Koshida, Shinji; Takeda, Hiroyuki

doi:10.1002/dvdy.22324

Cited by 24 publications

(23 citation statements)

References 47 publications

(4 reference statements)

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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%

See 1 more Smart Citation

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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“…Mid-body neuromasts were the most likely to connect to the Mauthner series nodes, which, unlike most descending neurons, connected to all spinal segments. Somatotopic organization has recently been shown within the PLL ganglion [50], but it is not known whether it is maintained in the PLL projection to the hindbrain. The different sensorimotor path lengths associated with different hindbrain segments in the current model offer some initial hypotheses on how PLL somatotopy may be represented at downstream levels of the pathway.…”

Section: Discussionmentioning

confidence: 99%

Graph Theoretical Model of a Sensorimotor Connectome in Zebrafish

et al. 2012

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Mapping the detailed connectivity patterns (connectomes) of neural circuits is a central goal of neuroscience. The best quantitative approach to analyzing connectome data is still unclear but graph theory has been used with success. We present a graph theoretical model of the posterior lateral line sensorimotor pathway in zebrafish. The model includes 2,616 neurons and 167,114 synaptic connections. Model neurons represent known cell types in zebrafish larvae, and connections were set stochastically following rules based on biological literature. Thus, our model is a uniquely detailed computational representation of a vertebrate connectome. The connectome has low overall connection density, with 2.45% of all possible connections, a value within the physiological range. We used graph theoretical tools to compare the zebrafish connectome graph to small-world, random and structured random graphs of the same size. For each type of graph, 100 randomly generated instantiations were considered. Degree distribution (the number of connections per neuron) varied more in the zebrafish graph than in same size graphs with less biological detail. There was high local clustering and a short average path length between nodes, implying a small-world structure similar to other neural connectomes and complex networks. The graph was found not to be scale-free, in agreement with some other neural connectomes. An experimental lesion was performed that targeted three model brain neurons, including the Mauthner neuron, known to control fast escape turns. The lesion decreased the number of short paths between sensory and motor neurons analogous to the behavioral effects of the same lesion in zebrafish. This model is expandable and can be used to organize and interpret a growing database of information on the zebrafish connectome.

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“…The evidence from these experiments shows an asymmetric monosynaptic input of the lateral line to the Mauthner cell, with a disproportionate contribution from early-born/primary neuromasts. There is a temporal progression of lateralis neurogenesis in the zebrafish embryo Sarrazín et al, 2010;Sato et al, 2010). Therefore, one possibility to explain neuronal heterogeneity is that neurons with the indentation or direct contact with the Mauthner cell are born at different times than those without it.…”

Section: Neuronal Subclassification Based On Contacts With a Central mentioning

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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Single‐cell analysis of somatotopic map formation in the zebrafish lateral line system

Cited by 24 publications

References 47 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

Graph Theoretical Model of a Sensorimotor Connectome in Zebrafish

Neuronal Birth Order Identifies a Dimorphic Sensorineural Map

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