Dual representation of pain in the operculo-insular cortex in humans

We report the response properties of the suprasylvian opercular and insular cortices to a painful stimulation delivered by a CO(2) laser recorded by depth intracerebral electrodes in epileptic patients. We defined two cortical areas of activation in the operculo-insular cortex in response to a painful laser stimulation: a suprasylvian opercular area, where we recorded responses peaking 140-170 ms after a painful stimulation (N140-P170), and a deeper insular area, where responses with a similar pattern peaked 180-230 ms after the stimulus (N180-P230). The average delay of 50 ms measured between the opercular and insular responses may reflect either sequential activation of the suprasylvian cortex then of the insula via corticocortical connections, or direct activation of the insula by inputs conveyed via thalamocortical projections through distinct fibres with different conduction times. We also recorded similar insular and opercular responses in the hemisphere ipsilateral to the stimulation, peaking 15 ms later than contralateral responses; this delay is compatible with transcallosal input transmission between these cortices. The mean stereotactic coordinates of the suprasylvian opercular N140-P170 and insular N180-P230 responses were found to be very similar to those of the maximal blood-flow responses to pain reported by previous PET and functional MRI studies in these cortical areas. We were able to distinguish the suprasylvian opercular and insular cortices in terms of response latencies evoked by a painful stimulus and in terms of stereotactic coordinates of the sources of these responses. The sequential timing of activation of the suprasylvian and insular cortices shown in this study thus complements in the time domain the spatial information provided by neuroimaging studies of the cortical processing of pain. It strongly suggests that these cortical areas are those responding with the shortest latency to peripheral pain inputs in the human brain.