In neuronal networks, synaptic strength is not constant but depends on the past activity of the synapse. This change in synaptic efficacy called 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 undergoes a rostrocaudal maturation in the developing spinal cord. Interestingly, we observed that the form of ADSP expressed was related to the functional flexor or extensor MN subtype. In the spinal cord, metabotropic glutamate receptors (mGluRs) modulate synaptic transmission and undergo subtype-specific regulation of their expression and localization during development. In the second part of this study, we then investigated the impact of mGluR activation on ADSP expression in P1–P3 and P8–P12 MNs. We found that mGluR agonists differentially and selectively modulated ADSP at VLF-MN synapses and that this modulation is developmentally regulated. We then used mGluR activation as a tool to indirectly access the functional role of high-frequency-induced-synaptic plasticity at VLF-MN synapses in locomotor pattern generation.