Spinal lamina I projection neurons that transmit nociceptive information to the brain play a pivotal role in hyperalgesia in various animal models of inflammatory and neuropathic pain. Consistently, activity-dependent long-term potentiation can be induced at synapses between primary afferent C-fibres and lamina I projection neurons but not unidentified neurons in lamina I. The specific properties that enable projection neurons to undergo long-term potentiation and mediate hyperalgesia are not fully understood. Here, we have tested if lamina I projection neurons differ from unidentified neurons in types or strength of primary afferent input and/or action potential-independent excitatory and inhibitory input. We used the whole-cell patch-clamp technique to record synaptic currents in projection and unidentified lamina I neurons in a transverse lumbar spinal cord slice preparation from rats between postnatal day 18 and 37. Lamina I neurons with a projection to the parabrachial area or the periaqueductal grey were identified by retrograde labelling with a fluorescent tracer. The relative contribution of NMDA- versus AMPA/kainate receptors to C-fibre-evoked excitatory postsynaptic currents of lamina I neurons significantly decreased with age between postnatal day 18 and 27, but was independent of the neurons’ supraspinal projection. We did not find a significant contribution of kainate receptors to C-fibre evoked excitatory postsynaptic currents. Lamina I projection and unidentified neurons possessed functional GABAA- and glycine receptors but received scarce action potential-independent spontaneous GABAergic and glycinergic inhibitory input as measured by miniature inhibitory postsynaptic currents. The miniature excitatory postsynaptic current frequencies were five times higher in projection than in unidentified neurons. The predominance of excitatory synaptic input to projection neurons, taken together with the previous finding that their membranes are more easily excitable than those of unidentified neurons, may facilitate the induction of synaptic long-term potentiation.