Motoneurons of the axial swimming muscles in hatchlingXenopus tadpoles: Features, distribution, and central synapses

Roberts, Alan; Walford, A; Soffe, Stephen R; Yoshida, Masayuki

doi:10.1002/(sici)1096-9861(19990830)411:3<472::aid-cne9>3.0.co;2-b

Cited by 33 publications

(32 citation statements)

References 45 publications

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“…In X. laevis, primary motor neurons first form within the rostral spinal cord at stage 24͞25, coinciding closely with the onset of gRXR activation (52). Peak motor neuron density in newly hatched tadpoles is observed in the same region as our observed gRXR activation (53). In addition, Hb9, a homeobox gene involved in motor neuron specification, is expressed in the X. laevis nervous system in a highly similar spatiotemporal fashion (54).…”

Section: Discussionsupporting

confidence: 70%

Spatiotemporal retinoid-X receptor activation detected in live vertebrate embryos

Luria

Furlow

2004

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

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Most studies on the nuclear retinoid-X receptor (RXR) have focused on its role as a heterodimeric partner but less about its own activation pattern during development and the distribution of potential endogenous ligands. The aim of this study is to visualize the distribution of activated RXR␣ in live transgenic Xenopus laevis embryos across a wide range of developmental stages. We adopted a nuclear receptor-Gal4 fusion͞upstream activation sequence-based reporter system for our assay. Strong activation of the RXR␣ ligand-binding domain was observed in a segment of the spinal cord just posterior to the hindbrain. This activation is first detected in neurula stage embryos and persists up to swimming tadpole stages, after which activation strongly declines. Addition of exogenous ligands, such as 9-cis retinoic acid or all-trans retinoic acid, expands the activation of RXR throughout the spinal cord but not in the brain, whereas the RXR-specific ligand LG268 expanded the Gal4 -RXR activation into the brain and olfactory epithelia. Treatment with the RAR-specific ligand 4-(E-2-(5,6,7,8-tetrahydro-5,5,8,8-tetramethyl-2-naphthalenyl)-1-propenyl)benzoic acid or thyroid hormone had no effect on Gal4 -RXR activation, whereas these compounds significantly increased their corresponding Gal4͞ receptor fusion proteins under similar conditions. Embryos expressing a Gal4 -RXR fusion protein with a deletion in the liganddependent activation domain (AF2) show no reporter gene activation. The results shown in this paper reveal a specific activation pattern for Gal4 -RXR␣ specifically in the developing spinal cord and suggest the existence of RXR ligand ''hot-spots'' in this region.Gal4 ͉ transgenesis ͉ Xenopus laevis ͉ nuclear receptor

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Section: Discussionsupporting

confidence: 70%

Spatiotemporal retinoid-X receptor activation detected in live vertebrate embryos

Luria

Furlow

2004

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

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“…The overwhelming majority of neurons born during the second phase must be interneurons (in a wide sense, i.e., including secondorder sensory neurons and other projection neurons; e.g., Binor and Heathcote, 2001). This can be inferred, because the Xenopus spinal cord at stages 37/38 -42 contains at least 1,340 interneurons (Roberts, 1989) but only around 310 sensory (Rohon Beard and extramedullary) neurons (Lamborghini, 1980;Roberts, 1989) and around 540 motorneurons (Roberts et al, 1999), and most neurons of the latter two categories were already generated before stage 22 (Fig. 1).…”

Section: Discussion Neurogenesis In the Xenopus Spinal Cord Proceeds mentioning

confidence: 97%

“…Generation rates (neurons/hr) for primary sensory neurons (Rohon Beard neurons and extramedullary cells; stages 9 -26) are based on rates determined by Lamborghini (1980) and total counts of extramedullary cells (Lamborghini, 1980) and Rohon Beard cells (Roberts, 1989) for the spinal cord. Generation rates for primary motor neurons (stages 9 -46) are based on cell counts by Roberts et al (1999) and kinetics of van Mier (1986). Generation rates for sensory neurons of the dorsal root ganglia (DRG) at limb levels are estimated based on data by Hughes and Tschumi (1958) and Prestige (1965), and rates for secondary motor neurons of the lateral motor columns (later stages) are estimated from cell counts in Kollros (1968) and information on kinetics by Hughes (1961) and Thors et al (1982b).…”

Section: Introductionmentioning

confidence: 99%

Thyroid hormone promotes neurogenesis in the Xenopus spinal cord

Schlosser

Koyano-Nakagawa

Kintner

2002

Developmental Dynamics

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Three phases of neurogenesis can be recognized during Xenopus spinal cord development. An early peak during gastrulation/ neurulation is followed by a phase of low level neurogenesis throughout the remaining embryonic stages and a later peak at early larval stages. We show here that several genes known to be essential for early neurogenesis (X-NGNR-1, XNeuroD, XMyT1, X-Delta-1) are also expressed during later phases of neurogenesis in the spinal cord, suggesting that they are involved in regulating spinal neurogenesis at later stages. However, additional neuronal determination genes may be important during larval stages, because X-NGNR-1 shows only scant expression in the spinal cord during larval stages. Thyroid hormone treatment of early larvae promotes neurogenesis in the spinal cord, where thyroid hormone receptor xTR␣ is expressed from early larval stages onward and results in precocious up-regulation of XNeuroD, XMyT1, and N-Tubulin expression. Similarly, thyroid hormone treatments of Xenopus embryos, which were coinjected with xTR␣ and the retinoid X receptor xRXR␣, repeatedly resulted in increased numbers of neurons, whereas unliganded receptors repressed neurogenesis. Our findings show that thyroid hormones are sufficient to up-regulate neurogenesis in the Xenopus spinal cord.

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“…In amphibians, the terms "primary" and "secondary" MN pools have been used by some authors to refer to those innervating the axial muscles and the limb muscles, respectively (reviewed in ref. 20). At stage 37/ 38 in Xenopus tadpoles, however, there is no anatomical evidence for segregation of axial MNs into two subgroups based on MNs recorded in gray scale according to the firing probability during swimming (cf.…”

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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Motoneurons of the axial swimming muscles in hatchlingXenopus tadpoles: Features, distribution, and central synapses

Cited by 33 publications

References 45 publications

Spatiotemporal retinoid-X receptor activation detected in live vertebrate embryos

Spatiotemporal retinoid-X receptor activation detected in live vertebrate embryos

Thyroid hormone promotes neurogenesis in the Xenopus spinal cord

Development of a spinal locomotor rheostat

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