Most lamina I neurons with a projection to the brainstem express the neurokinin 1 receptor and thus belong to a small subgroup of lamina I neurons that are necessary for the development of hyperalgesia in rat models of persisting pain. These neurons are prone to synaptic plasticity following primary afferent stimulation in the noxious range while other nociceptive lamina I neurons are not. Here, we used whole-cell patch-clamp recordings from lamina I neurons in young rat spinal cord transverse slices to test if projection neurons possess membrane properties that set them apart from other lamina I neurons. Neurons with a projection to the parabrachial area or the periaqueductal grey (PAG) were identified by retrograde labelling with the fluorescent tracer DiI. The properties of lamina I projection neurons were found to be fundamentally different from those of unidentified, presumably propriospinal lamina I neurons. Two firing patterns, the gap and the bursting firing pattern, occurred almost exclusively in projection neurons. Most spino-parabrachial neurons showed the gap firing pattern while the bursting firing pattern was characteristic of spino-PAG neurons. The underlying membrane currents had the properties of an A-type K+-current and a Ca2+-current with a low activation threshold, respectively. Projection neurons, especially those of the burst firing type, were more easily excitable than unidentified neurons and received a larger proportion of monosynaptic input from primary afferent C-fibres. Intracellular labelling with lucifer yellow showed that projection neurons had larger somata than unidentified neurons and many had a considerable extension in the mediolateral plane.