Cortical processing of human somatic and visceral sensation

Abstract

Somatic sensation can be localized precisely, whereas localization of visceral sensation is vague, possibly reflecting differences in the pattern of somatic and visceral input to the cerebral cortex. We used functional magnetic resonance imaging to study the cortical processing of sensation arising from the proximal (somatic) and distal (visceral) esophagus in six healthy male subjects. Esophageal stimulation was performed by phasic distension of a 2 cm balloon at 0.5 Hz. For each esophageal region, five separate 30 sec periods of nonpainful distension were alternated with five periods of similar duration without distension. Gradient echoplanar images depicting bold contrast were acquired using a 1.5 T GE scanner. Distension of the proximal esophagus was localized precisely to the upper chest and was represented in the trunk region of the left primary somatosensory cortex. In contrast, distension of the distal esophagus was perceived diffusely over the lower chest and was represented bilaterally at the junction of the primary and secondary somatosensory cortices. Different activation patterns were also observed in the anterior cingulate gyrus with the proximal esophagus being represented in the right midanterior cingulate cortex (BA 24) and the distal esophagus in the perigenual area (BA32). Differences in the activation of the dorsolateral prefrontal cortex and cerebellum were also observed for the two esophageal regions. These findings suggest that cortical specialization in the sensory-discriminative, affective, and cognitive areas of the cortex accounts for the perceptual differences observed between the two sensory modalities.

Fig. 1.

Brain activation after esophageal stimulation. The figure shows the brain regions activated after stimulation of the proximal (somatic) and the distal (visceral) regions of the esophagus.a shows activation of the left cerebellum for the distal but not for the proximal esophagus. b shows activation of the right insula for both the proximal and the distal esophagus.c shows activation of the right inferior frontal gyrus for the proximal esophagus and the inferior part of the left primary somatosensory cortex, the left secondary somatosensory cortex, the left inferior frontal gyrus, and the right premotor cortex for the distal esophagus. d shows activation of the right anterior midcingulate gyrus, the left dorsolateral prefrontal cortex, the left premotor and supplementary motor cortices, and the right premotor cortex for the proximal esophagus, and the left premotor and supplementary motor cortices for the distal esophagus. eshows activation of the right dorsolateral prefrontal cortex, right anterior midcingulate gyrus for the proximal esophagus and right anterior cingulate gyrus, the right precuneus, left motor, premotor, and supplementary cortices for the visceral esophagus. Fshows activation of the left motor and supplementary motor cortices, the left primary somatosensory cortex, left precuneus and the right premotor cortex, and supplementary cortex for the proximal esophagus, and that of the right precuneus, the right premotor, and supplementary cortices for the visceral esophagus.

Fig. 2.

Three-dimensional brain representation of esophageal sensation. The figure shows the brain loci that process proximal (A) and the distal (B) esophageal sensation, superimposed on three-dimensionally rendered images of the brain. In comparison to the distal esophagus, the proximal esophagus shows representation in the more rostral regions of the primary somatosensory and motor cortex. Furthermore, differential representation of the two esophageal regions over the secondary somatosensory cortex, premotor, frontal, and prefrontal cortices and the cerebellum is notable.