Differences in Brain Responses to Visceral and Somatic Pain Stimuli

Extensive visceral (esophageal balloon distension) and somatic (contact heat on the midline chest) animal and human experimental studies have demonstrated that the perceptual, auto-nomic, and behavioral responses to noxious stimulation of somatic structures differ from those of the viscera (28,29). These differences have been explained based on the functional neuro-anatomic differences between visceral and somatic pain processing. Experimentally induced aversive visceral sensations in humans are generally described as more unpleasant than somatic sensations (30,31). A series of studies from Bushnell's laboratory evaluated perceptual and central nervous system responses to visceral and cutaneous painful stimuli to the chest. In these studies, the authors used controlled balloon distension of the esophagus as a visceral stimulus and contact heat exposure of the chest as a corresponding somatic stimulus, matched in terms of perceived intensity within the same dermatome (30,32,33). In an initial psychophysi-cal study in healthy volunteers, they found that the visceral, mechanical stimulus was experienced as more unpleasant, diffuse, and variable than cutaneous thermal pain of similar intensity, independent of the duration of the stimulus (30). Using the same stimulation paradigm, Strigo et al. studied regional brain responses and associated behavioral responses in seven healthy subjects with fMRI during visceral and somatic stimulation (32). A similar set of regions, including secondary somatosensory and parietal cortices, thalamus, basal ganglia, and cerebellum was activated by both stimuli. However, preferential activation of certain regions by visceral versus somatic stimuli was observed. For example, cutaneous heat pain evoked higher activations in the bilateral anterior insular cortex and ventrolateral PFC. On the other hand, visceral mechanical pain evoked in the same dermatome was associated with activation of bilateral inferior primary somatosensory cortex, bilateral primary motor cortex, and a more rostral region within the dACC. As in previous psychophysiological studies, subjects rated esophageal pain with higher affective scores than cutaneous pain. In a follow-up study, the authors provided evidence for a segregation of nociceptive inputs from the cutaneous trunk and distal esophagus with the parasylvian cortex in the parietal opercula (33). Visceral stimulation of the esophagus resulted in the activation of a more lateral region in the parasylvian cortex than cutaneous stimulation of the trunk. Evaluating differential brain responses to visceral and somatic stimuli of the lower body, Hobday et al. found similar brain activation to visceral (rectal) and somatic (anal) distension, even though a greater activation of motor cortex by the somatic stimulus was observed (17). Tracey's group used fMRI scanning of the brain to evaluate the cortical processing of visceral (rectal) and somatic stimuli in 10 healthy control subjects (34). Each subject received noxious somatic stimulation (in the form of cutaneous contact heat) to the left foot and midline lower back and noxious visceral stimulation (controlled balloon distension of the rectum). Stimulus unpleasantness was matched for visceral and somatic stimuli, resulting in different stimulus intensities: Somatic stimuli were rated as mild to moderately painful, while visceral stimuli did not reach the pain threshold. Thus, similar to the findings in the chest, the relative unpleasantness of the subjective experience of the visceral mechanical stimuli was higher than that of the somatic thermal stimuli. Visceral stimuli were associated with deactivation of the perigenual anterior cingulate cortex (pACC; a finding also reported in somatic pain studies) (35), with a relatively greater activation of the right anterior insula. Somatic (but not visceral) pain was associated with left dorsolateral PFC, a region concerned with cognitive processes. In a follow-up study (36), the authors compared brain stem responses to the same two stimuli. Ten healthy subjects (five females) were studied twice with 3T fMRI, during which they received matched, moderately painful, electrical stimuli to either the midline lower abdomen or the rectum. Significant activation associated with both stimuli was observed in several brain stem regions including the PAG, the parabrachial nucleus, the locus coeruleus complex (LCC), and the nucleus cuneifor-mis (NCF). Marked spatial similarities in activation were observed for the visceral and somatic pain conditions. However, two regions showed greater responses during the visceral pain condition: A significantly greater activation of a region identified as the NCF and a significant correlation of the right PAG with anxiety ratings. The authors concluded from these findings that the observed differences may represent a greater nocifensive response and a greater emotive salience of visceral pain. It needs to be kept in mind that in all of the studies comparing brain and subjective responses to visceral and somatic pain stimuli, these stimuli also differed in the pain modality used (mechanical vs. thermal), and that placement of a stimulus device into the upper or lower GI tract by itself is an uncomfortable procedure, regardless of the actual stimulus delivered.

Two studies have looked at differences in central processing of somatic and visceral experimental stimuli in patients with IBS. These studies follow from a series of psychophysiological studies showing increased perception of visceral stimulation in IBS, but less consistent findings regarding IBS sensitivity to noxious somatic stimuli. However, depending on the somatic pain stimulus used, different investigators have reported normal (37-40), reduced (41), and enhanced (31) perceptual responses to somatic pain stimuli. One of the two imaging studies done to date comparing visceral and somatic stimuli in IBS used thermal pain (31) and the other cutaneous pressure (41). Verne et al. studied brain responses with fMRI to rectal distension (35-55 mmHg) and to cutaneous heat (foot immersion in 45°C and 47°C water bath) in nine IBS patients (six females) and in a group of healthy age- and sex-matched controls (31). They report that both noxious stimuli evoked greater neural activity in brain regions of patients compared to controls. These regions included both those related to somatosensory processing (thalamus, somatosensory, and insular cortices) and those more related to cognitive and emotional modulation (anterior and posterior cingulate and prefrontal cortices). Enhanced brain responses to both types of stimuli were observed within the same brain structures. The authors interpreted these findings as supporting their original hypothesis that visceral and cutaneous hypersensitivity in IBS patients is related to increased afferent processing in ascending pathways, rather than to altered cognitive and/or emotional modulation at higher brain levels. Chang et al. reached a somewhat different conclusion based on findings in female patients with IBS with (n = 10) and without (n = 10) a comorbid diagnosis of fibromyalgia (42). Brain responses to somatic pressure (administered with a dolorimeter) and rectal distension (via barostat) were evaluated with H215O-PET; subjective stimulus ratings were quantified by rating scales. The somatic stimulus was perceived as less aversive than the visceral stimulus by the IBS patients, while IBS + fibromyalgia patients rated both stimuli as equally aversive. Group differences in regional brain activation were only observed within the dACC, where IBS patients showed a greater response to visceral stimuli and IBS + fibro-myalgia patients showed a greater response to somatic stimuli. The authors concluded from their findings that chronic stimulus-specific enhancement of dACC responses to sensory stimuli in both syndromes may be associated with cognitive enhancement of either visceral (IBS) or somatic (IBS + fibromyalgia) sensory input. The fact that no group differences were observed in primary sensory areas (thalamus, somatosensory cortex, and insula) is consistent with the concept that afferent input that reaches the brain is not different between the two patient populations, while arousal and attentional mechanisms may differ.

In summary, a growing number of brain imaging studies have addressed the question of how brain responses to somatic and visceral pain stimuli may differ, in both healthy control subjects and patients with IBS. The literature on differences in the greater subjective affective rating of visceral pain stimuli (in terms of unpleasantness) has been fairly consistent. This perceptual difference may be related in part to the difference in response options for the two stimuli (inescapable for visceral pain; requirement for motor response for somatic pain) and to the greater unpleasantness related to the placement of the visceral stimulus device. In contrast, a consistent difference in brain processing of visceral and somatic stimuli has not emerged from published studies. For example, consistent evidence for an expected greater activation of limbic and paralimbic brain regions for visceral stimuli (correlating with the greater affective responses) or differences in arousal and antinociceptive mechanisms between visceral and somatic stimuli have not been reported. This lack of consistency may be due, in large part, to differences in study design (imaging modality, study paradigms, nature of stimuli used, previous exposure of subjects to similar stimuli, sex of participants, etc.) and the relatively small number of studies reported for upper and lower GI tract so far.

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