Abstract

Activity-dependent synaptic plasticity (ADSP) is paramount to synaptic processing and maturation. However, identifying the ADSP capabilities of the numerous synapses converging onto spinal motoneurons (MNs) remain elusive. Using spinal cord slices from mice at two developmental stages, 1–4 and 8–12 postnatal days (P1–P4; P8–P12), we found that high-frequency stimulation of presumed reticulospinal neuron axons in the ventrolateral funiculus (VLF) induced either an NMDA receptor-dependent-long-term depression (LTD), a short-term depression (STD) or no synaptic modulation in limb MNs. Our study shows that P1–P4 cervical MNs expressed the same plasticity profiles as P8–P12 lumbar MNs rather than P1–P4 lumbar MNs indicating that ADSP expression at VLF-MN synapses is linked to the rostrocaudal development of spinal motor circuitry. Interestingly, we observed that the ADSP expressed at VLF-MN was related to the functional flexor or extensor MN subtype. Moreover, heterosynaptic plasticity was triggered in MNs by VLF axon tetanisation at neighbouring synapses not directly involved in the plasticity induction. ADSP at VLF-MN synapses specify differential integrative synaptic processing by flexor and extensor MNs and could contribute to the maturation of spinal motor circuits and developmental acquisition of weight-bearing locomotion.

Highlights

  • In this context, the aim of the present study was to decipher the activity-dependent synaptic plasticity (ADSP) capabilities of ventrolateral funiculus (VLF)-MN synapses and to assess how spinal cord circuit development impacts on ADSP expression in these connections

  • Irrespective of age, under baseline conditions of VLF stimulation (0.03 Hz), AMPA/kainate receptor-mediated excitatory postsynaptic currents (VLF-Excitatory postsynaptic currents (EPSCs)) were recorded in the presence of GABAergic and glycinergic receptor antagonists from lumbar motoneurons held at −​60 mV in spinal cord slices (Fig. 1A,B)

  • We chose to assess the plasticity-inducing effects of 50 Hz high frequency stimulations applied in 2 s trains to VLF axons (VLF-HFS)

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Summary

Introduction

The aim of the present study was to decipher the ADSP capabilities of VLF-MN synapses and to assess how spinal cord circuit development impacts on ADSP expression in these connections. For this purpose, the plasticity-inducing effects of physiologically relevant high frequency stimulation applied to VLF axons (VLF-HFS) were explored at VLF-MN synapses in spinal cord slices during the acquisition of postural control in P1–P4 and P8–P12 mouse pups. We identified a rostrocaudal maturation of ADSP expression in MNs during development and revealed that ADSP expression is a function of their flexor and extensor phenotype

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