Segregation of visceral and somatosensory afferents: an fMRI and cytoarchitectonic mapping study

Ano-rectal stimulation provides an important model for the processing of somatosensory and visceral sensations in the human nervous system. In spite of their anatomical proximity, the anal canal is innervated by somatosensory afferents whereas the rectum is innervated by the visceral nervous system. In a functional magnetic resonance (fMRI) experiment, we examined the cerebral responses to pneumatic balloon distension of these two structures to test whether somatosensory and visceral stimulation elicited distinct brain activations in spite of their spinal convergence. The specificity of the identified activations was analyzed by Bayesian mixed effects modeling. Activations in the parietal operculum were also compared to the location of cytoarchitectonically defined areas OP 1-4, which are part of the secondary somatosensory cortex (SII), to analyze whether the SII region was activated by anal and/or rectal stimulation. The lowest segregation between visceral and somatosensory stimuli was in the insular cortex, which supports the interpretation of the insula as an integrative region, receiving input from different sensory modalities. The most distinct segregation was found in the fronto-parietal operculum. Here the activations following anal and rectal stimulation were not only functionally but also anatomically distinct. Anal sensations were processed similar to other somatosensory stimuli in the SII cortex (area OP 4). Rectal afferents on the other hand were not processed in SII. Rather, they evoked activation at a more anterior location on the precentral operculum. These results demonstrate a functionally and anatomically distinct processing of somatosensory and visceral afferents in the human cerebral cortex.