Functional limb muscle innervation prior to cholinergic transmitter specification during early metamorphosis in Xenopus
- CNRS Université de Bordeaux, France
- CNRS Muséum National d'Histoire Naturelle, France
Abstract
In vertebrates, functional motoneurons are defined as differentiated neurons that are connected to a central premotor network and activate peripheral muscle using acetylcholine. Generally, motoneurons and muscles develop simultaneously during embryogenesis. However, during Xenopus metamorphosis, developing limb motoneurons must reach their target muscles through the already established larval cholinergic axial neuromuscular system. Here, we demonstrate that at metamorphosis onset, spinal neurons retrogradely labeled from the emerging hindlimbs initially express neither choline acetyltransferase nor vesicular acetylcholine transporter. Nevertheless, they are positive for the motoneuronal transcription factor Islet1/2 and exhibit intrinsic and axial locomotor-driven electrophysiological activity. Moreover, the early appendicular motoneurons activate developing limb muscles via nicotinic antagonist-resistant, glutamate antagonist-sensitive, neuromuscular synapses. Coincidently, the hindlimb muscles transiently express glutamate, but not nicotinic receptors. Subsequently, both pre- and postsynaptic neuromuscular partners switch definitively to typical cholinergic transmitter signaling. Thus, our results demonstrate a novel context-dependent re-specification of neurotransmitter phenotype during neuromuscular system development.
Data availability
All data generated or analysed during this study are available via Dryad (doi:10.5061/dryad.9sj250q).
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Data from: Functional limb muscle innervation prior to cholinergic transmitter specification during early metamorphosis in XenopusAvailable at Dryad Digital Repository under a CC0 Public Domain Dedication.
Article and author information
Author details
Francois M Lambert
Muriel Thoby-Brisson
Funding
Centre National de la Recherche Scientifique
- Didier Le Ray
Muséum National d'Histoire Naturelle (Actions thématiques du Museum)
- Hervé Tostivint
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Carol A Mason, Columbia University, United States
Ethics
Animal experimentation: All procedures were carried out in accordance with, and approved by, the local ethics committee (protocols no. 68-019) to H. Tostivint and no. 2016011518042273 APAFIS no. 3612 to DLR)
Version history
- Received: July 25, 2017
- Accepted: May 6, 2018
- Accepted Manuscript published: May 30, 2018 (version 1)
- Version of Record published: June 12, 2018 (version 2)
Copyright
© 2018, Lambert et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Functional limb muscle innervation prior to cholinergic transmitter specification during early metamorphosis in Xenopus
eLife 7:e30693.
https://doi.org/10.7554/eLife.30693
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