Somatotopic organisation of the human insula to painful heat studied with high resolution functional imaging

Pain perception is a multidimensional phenomenon, derived from sensory, affective, cognitive-evaluative and homeostatic information. Neuroimaging studies of pain perception have investigated the role of primary somatosensory cortex (SI); however, they have typically failed to demonstrate the expected somatotopy. An alternative network for the sensory component of pain has been proposed, involving a temperature and pain-specific nucleus of the thalamus (VMpo) and its projections to dorsal posterior insula (dpIns). According to this hypothesis, projections to the insula should be arranged somatotopically. In order to test for the presence of somatotopy in the operculo-insular brain region, we delivered moderately painful thermal stimuli to the right face, hand and foot in 14 healthy subjects and recorded brain responses using high resolution functional magnetic resonance imaging at 3 T. For each subject, the thermode temperature was adjusted to produce pain ratings of 5 to 6 out of 10, which corresponded to average temperatures for the face, hand and foot of 49.6, 48.5 and 48.5 degrees C, respectively. Examination of mixed effects group activation maps suggested a pain-related somatotopy in the contralateral posterior insula and putamen. Construction of frequency maps revealed that face activation within the posterior insula was anterior to both hand and foot, whilst foot activation was located medially in the circular sulcus. Single subject analysis demonstrated that only coordinates for dpIns activation were significantly dependent on stimulus location (Hotelling's Trace, P = 0.012). Coordinates for face (paired t test, P = 0.004) and hand (P < 0.001) activity were more lateral than those for foot, whilst face activation was anterior to the foot (P = 0.037). Based on single subject analyses, the average standard space (MNI) coordinates for face, hand and foot activity were (-40,-16,11), (-40,-19,14) and (-35,-21,11) respectively.

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