Identified motoneurons and their innervation of axial muscles in the zebrafish

Westerfield, Monte; McMurray, J.V.; Eisen, JS

doi:10.1523/jneurosci.06-08-02267.1986

Cited by 304 publications

(283 citation statements)

References 21 publications

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“…In the ventral spinal cord of the zebrafish embryo, primary MNs and sMNs, GABAergic KAЈ and KAЈЈ cells, and GABAergic ventral longitudinal descending neurons (VeLDs) cells emerge in a distinct spatial and temporal order from progenitor cells (4,5). To test whether Jagged-mediated signaling affects the specification of these ventral neurons, we attempted a loss-of-function study with morpholinos (MO) directed against jagged1b and jagged2 that are expressed in the ventral spinal cord.…”

Section: Resultsmentioning

confidence: 99%

“…The cellular diversity and complexity of neuronal organization in the CNS raises the question of how neuronal subtypes are generated at distinct locations and times by associating intrinsic factors with extrinsic signals during development (1)(2)(3). In the zebrafish embryo, distinct neurons, such as primary and secondary motor neurons (sMNs), GABAergic Kolmer-Agduhr (KA) cells, and RohonBeard (RB) sensory neurons emerge in a distinct spatiotemporal order from progenitors (4,5). The MNs and GABAergic KA cells are generated from progenitors in discrete compartments of the ventral spinal cord that are likely to be analogous to the p2, pMN, and p3 progenitor zones described in other vertebrate model systems in refs.…”

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confidence: 99%

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Jagged-mediated Notch signaling maintains proliferating neural progenitors and regulates cell diversity in the ventral spinal cord

Yeo

Chitnis

2007

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

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Previous studies have shown that Delta-mediated Notch signaling regulates the number of early differentiating neurons. However, the role of Notch activation and Jagged-mediated signaling during late neurogenesis remains poorly defined. In the developing spinal cord of zebrafish, GABAergic Kolmer-Agduhr (KA ) cells and motor neurons (MN) emerge sequentially from their progenitors in the p3 domain. Jagged2 is expressed uniformly in the pMN domain during late neurogenesis where Olig2 is required for its expression. We suggest that Jagged2 interacts ventrally with progenitors in the adjacent p3 domain, where it has a critical role in the maintenance of proliferating neural progenitors and in preventing differentiation of these progenitors as GABAergic KA cells or secondary MN. This study identifies a critical role for Jagged-Notch signaling in the maintenance of proliferating neural precursors in a discrete compartment of the neural tube during the continuing growth and development of the vertebrate nervous system.M olecular studies show that distinct subtypes of neurons are generated from different progenitors distributed along the dorsal-ventral axis of the spinal cord (1). The cellular diversity and complexity of neuronal organization in the CNS raises the question of how neuronal subtypes are generated at distinct locations and times by associating intrinsic factors with extrinsic signals during development (1-3). In the zebrafish embryo, distinct neurons, such as primary and secondary motor neurons (sMNs), GABAergic Kolmer-Agduhr (KA) cells, and RohonBeard (RB) sensory neurons emerge in a distinct spatiotemporal order from progenitors (4, 5). The MNs and GABAergic KA cells are generated from progenitors in discrete compartments of the ventral spinal cord that are likely to be analogous to the p2, pMN, and p3 progenitor zones described in other vertebrate model systems in refs. 1 and 6. To understand how specification of these neurons is regulated, we have examined how differentiation and proliferation of progenitors in discrete compartments of the ventral spinal cord

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Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

Jagged-mediated Notch signaling maintains proliferating neural progenitors and regulates cell diversity in the ventral spinal cord

Yeo

Chitnis

2007

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

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“…How does this developmental organization compare with other aquatic vertebrates? In zebrafish, the first MNs to reach the myotomes are the large primary MNs (of which there are only three to four per hemisegment) that selectively innervate dorsal, ventral, or lateral regions (21,22). Secondary MNs are smaller and more numerous (around 20 per hemisegment), and they innervate the muscle block later, tracking along one of the three pathways pioneered by the primary MNs (22).…”

Section: Discussionmentioning

confidence: 99%

Development of a spinal locomotor rheostat

Zhang

Issberner

Sillar

2011

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

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Locomotion in immature animals is often inflexible, but gradually acquires versatility to enable animals to maneuver efficiently through their environment. Locomotor activity in adults is produced by complex spinal cord networks that develop from simpler precursors. How does complexity and plasticity emerge during development to bestow flexibility upon motor behavior? And how does this complexity map onto the peripheral innervation fields of motorneurons during development? We show in postembryonic Xenopus laevis frog tadpoles that swim motorneurons initially form a homogenous pool discharging single action potential per swim cycle and innervating most of the dorsoventral extent of the swimming muscles. However, during early larval life, in the prelude to a free-swimming existence, the innervation fields of motorneurons become restricted to a more limited sector of each muscle block, with individual motorneurons reaching predominantly ventral, medial, or dorsal regions. Larval motorneurons then can also discharge multiple action potentials in each cycle of swimming and differentiate in terms of their firing reliability during swimming into relatively high-, medium-, or low-probability members. Many motorneurons fall silent during swimming but can be recruited with increasing locomotor frequency and intensity. Each region of the myotome is served by motorneurons spanning the full range of firing probabilities. This unfolding developmental plan, which occurs in the absence of movement, probably equips the organism with the neuronal substrate to bend, pitch, roll, and accelerate during swimming in ways that will be important for survival during the period of free-swimming larval life that ensues.motor system | central pattern generator | ontogeny A dult vertebrates navigate through their environment with incredible agility and flexibility, a feature of locomotory behavior that is often critical for survival. During locomotion, sensory information interacts with central pattern generator (CPG) networks in the spinal cord, which in turn provide command signals to motorneurons (MNs) to sequence and guide movements appropriately (1). CPGs develop before locomotion is possible (2-4). Initially, however, the output of immature CPGs lacks the precision and flexibility that typifies adult locomotion. Therefore, postembryonic development must involve a period during which the central motor control circuitry is modified to accommodate the behavioral requirements of later stages. Much is known about the molecular mechanisms responsible for the differentiation of neuronal components of the motor system, motor axon trajectories, and innervation patterns (5-7). However, how this links to the functional development of these components has not been fully resolved, although there is ample evidence that activity itself is influential as a developmental signal (8, 9).Recent evidence has revealed a topographic recruitment order for dorsoventrally arranged spinal premotor interneurons and MNs during changes in swimming speed in larval ...

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“…In another study, Lim et al (199 1) used general and cellspecific markers to assay the spatial patterning of early neuronal differentiation in the chicken embryo. The lack of any obvious segmental patterns contrasts with the indisputable segmental patterns of neuronal differentiation in the spinal cord of lower vertebrates (Westerfield et al, 1986;Hanneman et al, 1988;Kuwada et al, 1990; see also references in , and in the chicken embryo's hindbrain (Glover, 1989;Lumsden and Keynes, 1989;Baker and Noden, 1990). Lim et al (199 1) suggest that the spinal cord of higher vertebrates may have lost an ancestral segmental organization in parallel with the evolution of limbs and the resultant need for intersegmental integration.…”

Section: Functional Implicationsmentioning

confidence: 99%

“…In the zebrafish, the embryonic spinal cord contains primary motoneurons and interneurons that are segmentally iterated (Westerfield et al, 1986). In higher vertebrates, transplantation experiments have demonstrated autonomous regions of functional specificity in the spinal neural tube.…”

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confidence: 99%

Segmental patterning of rat and chicken sympathetic preganglionic neurons: correlation between soma position and axon projection pathway

et al. 1994

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The segmental organization of midthoracic rat and chicken sympathetic preganglionic neurons was examined by retrograde labeling in vivo and in vitro. The results demonstrate that individual sympathetic preganglionic neurons project only rostrally or caudally within the sympathetic chain, even though the spinal segment in which they reside provides innervation to both rostral and caudal ganglia. In addition, there is both a segmental and an intrasegmental pattern in the thoracic sympathetic column, in which the position of preganglionic neurons is related to the direction they project in the sympathetic chain. Thoracic sympathetic preganglionic neurons are organized into discrete segmental units, each of which exhibits an internal rostrocaudal polarity with respect to the direction of axon projection in the sympathetic chain. The rostrocaudal bias of this internal polarity is graded from segment to segment along the longitudinal axis. Since there is minimal overlap between thoracic segments, the transition from one segment to another entails a sharp change in the pathway choice of the preganglionic neurons. The organization of the preganglionic projections thus includes (1) segmental periodicity, (2) intrasegmental gradients of neuronal identity, and (3) an axial gradient of segment identity. The significance of these findings is twofold. First, they suggest a functional organization that may be related to the specificity of sympathetic reflex action. Second, they reveal a cellular organization that suggests an underlying segmental pattern in the developing spinal cord.

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Identified motoneurons and their innervation of axial muscles in the zebrafish

Cited by 304 publications

References 21 publications

Jagged-mediated Notch signaling maintains proliferating neural progenitors and regulates cell diversity in the ventral spinal cord

Jagged-mediated Notch signaling maintains proliferating neural progenitors and regulates cell diversity in the ventral spinal cord

Development of a spinal locomotor rheostat

Segmental patterning of rat and chicken sympathetic preganglionic neurons: correlation between soma position and axon projection pathway

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