Functional organization of vestibulospinal inputs on thoracic motoneurons responsible for trunk postural control in Xenopus.

KEY POINTS: Vestibulospinal reflexes participate in postural control. How this is achieved has not been investigated fully. We combined electrophysiological, neuroanatomical and imaging techniques to decipher the vestibulospinal network controlling the activation of back and limb muscles responsible for postural adjustments. We describe two distinct pathways activating either thoracic postural motoneurons alone or thoracic and lumbar motoneurons together, with the latter co-ordinating specifically hindlimb extensors and postural back muscles. ABSTRACT: In vertebrates, trunk postural stabilization is known to rely mainly on direct vestibulospinal inputs on spinal axial motoneurons. However, a substantial role of central spinal commands ascending from lumbar segments is not excluded during active locomotion. In the adult Xenopus, a lumbar drive dramatically overwhelms the descending inputs onto thoracic postural motoneurons during swimming. Given that vestibulospinal fibres also project onto the lumbar segments that shelter the locomotor generators, we investigated whether such a lumbo-thoracic pathway may relay vestibular information and consequently, also be involved in the control of posture at rest. We show that thoracic postural motoneurons exhibit particular dendritic spatial organization allowing them to gather information from both sides of the cord. In response to passive head motion, these motoneurons display both early and delayed discharges, with the latter occurring in phase with ipsilateral hindlimb extensor bursts. We demonstrate that both vestibulospinal and lumbar ascending fibres converge onto postural motoneurons, and that thoracic motoneurons monosynaptically respond to the electrical stimulation of either pathway. Finally, we show that vestibulospinal fibres project to and activate lumbar interneurons with thoracic projections. Taken together, our results complete the scheme of the vestibulospinal control of posture by illustrating the existence of a novel, indirect pathway, which implicates lumbar interneurons relaying vestibular inputs to thoracic motoneurons, and participating in global body postural stabilization in the absence of active locomotion.

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

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.