Spinal lamina I is a key element of the pain processing system relaying primary afferent input to supraspinal areas. However, little is known about how the signal is modulated by its intrinsic network including local‐circuit neurones (LCNs) and much less numerous anterolateral‐tract projection neurones (PNs). Here, we used whole‐cell patch‐clamp recordings in an isolated spinal cord preparation to examine properties of identified LCNs (n = 85) and PNs (n = 73) in their functionally preserved local networks. Forty LCNs showed spontaneous rhythmic firing (2–7 Hz) at zero current injection, which persisted in the presence of blockers of fast synaptic transmission. In remaining cases, most LCNs and PNs fired tonically in response to depolarizing current injections. We identified LCNs and PNs receiving low‐threshold primary afferent driven inhibitory inputs, which in many cases were disynaptic and temporally preceded classical high‐threshold excitatory inputs. This direct inhibitory link between the low‐threshold afferents and PNs can function as a postsynaptic gate controlling the nociceptive information flow in the spinal cord. The LCNs were found to be integrated into the superficial dorsal horn network by receiving monosynaptic and disynaptic inputs from other lamina I and II neurones. One‐third of LCNs and two‐thirds of PNs tested responded to substance P application. Thus, substance P released by a noxious afferent stimulation could excite PNs in two ways, directly and via activation of their presynaptic LCN circuitries. In conclusion, we have described important properties of identified lamina I neurones and their role in a new circuit for gating pain responses. This article is protected by copyright. All rights reserved