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Functional limb muscle innervation prior to cholinergic transmitter specification during early metamorphosis in Xenopus

View ORCID ProfileF. M. Lambert, L. Cardoit, E. Courty, M. Bougerol, View ORCID ProfileM. Thoby-Brisson, J. Simmers, H. Tostivint, D. Le Ray
doi: https://doi.org/10.1101/173328
F. M. Lambert
1Institut de Neurosciences Cognitives et Intégratives d’Aquitaine (INCIA, CNRS UMR 5287), Université de Bordeaux;
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  • For correspondence: francois.lambert@u-bordeaux.fr didier.leray@u-bordeaux.fr
L. Cardoit
1Institut de Neurosciences Cognitives et Intégratives d’Aquitaine (INCIA, CNRS UMR 5287), Université de Bordeaux;
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E. Courty
1Institut de Neurosciences Cognitives et Intégratives d’Aquitaine (INCIA, CNRS UMR 5287), Université de Bordeaux;
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M. Bougerol
2Evolution des Régulations Endocriniennes (ERE, CNRS UMR 7221), Muséum National d’Histoire Naturelle, Paris.
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M. Thoby-Brisson
1Institut de Neurosciences Cognitives et Intégratives d’Aquitaine (INCIA, CNRS UMR 5287), Université de Bordeaux;
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J. Simmers
1Institut de Neurosciences Cognitives et Intégratives d’Aquitaine (INCIA, CNRS UMR 5287), Université de Bordeaux;
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H. Tostivint
2Evolution des Régulations Endocriniennes (ERE, CNRS UMR 7221), Muséum National d’Histoire Naturelle, Paris.
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D. Le Ray
1Institut de Neurosciences Cognitives et Intégratives d’Aquitaine (INCIA, CNRS UMR 5287), Université de Bordeaux;
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  • For correspondence: francois.lambert@u-bordeaux.fr didier.leray@u-bordeaux.fr
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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.

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  • Competing Interests: The authors declare no competing interests.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted August 08, 2017.
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Functional limb muscle innervation prior to cholinergic transmitter specification during early metamorphosis in Xenopus
F. M. Lambert, L. Cardoit, E. Courty, M. Bougerol, M. Thoby-Brisson, J. Simmers, H. Tostivint, D. Le Ray
bioRxiv 173328; doi: https://doi.org/10.1101/173328
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Functional limb muscle innervation prior to cholinergic transmitter specification during early metamorphosis in Xenopus
F. M. Lambert, L. Cardoit, E. Courty, M. Bougerol, M. Thoby-Brisson, J. Simmers, H. Tostivint, D. Le Ray
bioRxiv 173328; doi: https://doi.org/10.1101/173328

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