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.

Regional brain activation in conscious, nonrestrained rats in response to noxious visceral stimulation

“…To date, the majority of human studies in this field have used distension of the rectosigmoid colon [4,5,8,41,44,48,52,62], stomach [37,69], and esophagus [2,3,9,73]. Activation of the insular and dorsal anterior cingulate cortex (dACC) has been most consistently reported, with other brain regions, including the prefrontal cortex, thalamus and brainstem being reported in some, but not in other studies.…”

Startle responding in the context of visceral pain

“…Although the insertion itself was invariably experienced as unpleasant, once the catheter was in its proper position, we did not continue with the next steps of the procedure, until subjects reported they became habituated to any sensations due to the presence of the catheter, which never took more than a few minutes. This procedure has been used extensively in previous research (e.g., Aziz et al, 2000;Coen et al, 2009). …”

“…Additionally, during threshold determination, we assured ourselves that the balloon was in the distal part of the esophagus by asking participants if they could indicate where they felt a sensation: if their answer indicated they could feel the sensation somewhere around their chest level, but that they could not locate it at a specific site, this was taken to indicate the balloon was indeed in the autonomously innervated, i.e. visceral part of the esophagus (Aziz et al, 2000). After threshold determination, a 3-minute baseline measure of skin conductance was obtained, and subjects were exposed to 10 startle probes in order to habituate them before proceeding to the 7 | Startle responding in the context of visceral pain 7 actual experiment.…”

“…The choice for distal esophageal stimulation was in part motivated by the ability to stimulate solely visceral tissue without involving stimulation of any overlying somatic tissue (Aziz et al, 2000), thus being classified as an interoceptive stimulation even by those who define interoception in its strictest sense (e.g., Dworkin, 2007). Opting for the esophagus as the site of stimulation also allows for future research to expand upon the current research findings, for example contrasting purely visceral stimulation (distal esophagus) with purely somatic stimulation (proximal esophagus) (Aziz et al, 2000).…”

“…Opting for the esophagus as the site of stimulation also allows for future research to expand upon the current research findings, for example contrasting purely visceral stimulation (distal esophagus) with purely somatic stimulation (proximal esophagus) (Aziz et al, 2000). We decided to stimulate at first pain threshold for our stimulus to qualify as aversive; pain by definition comprises a component of unpleasant affect according to the International Association for the Study of Pain (Merskey and Bogduk, 1994).…”