Gastroenterology

Gastroenterology

Volume 139, Issue 4, October 2010, Pages 1310-1319.e4
Gastroenterology

Basic—Alimentary Tract
Patients With Irritable Bowel Syndrome Have Altered Emotional Modulation of Neural Responses to Visceral Stimuli

https://doi.org/10.1053/j.gastro.2010.06.054Get rights and content

Background & Aims

In patients with irritable bowel syndrome (IBS), pain amplification and hypervigilance might result from altered affective-motivational modulation of the pain response. We investigated the effects of emotional context on the behavioral and neural response to visceral stimuli in IBS patients.

Methods

We used functional magnetic resonance imaging (fMRI) to assess the blood oxygen level-dependent response to nonpainful and painful rectal distensions in 15 female IBS patients and 12 healthy women. Distensions were delivered during psychologic stress or relaxation; data were compared with those in a neutral condition (control). Group and context-dependent differences in the processing of visceral stimulation were assessed at behavioral and the neuronal levels. Secondary analyses of group differences were performed using anxiety scores as a covariate because of higher anxiety symptoms among patients with IBS.

Results

During rectal stimulation, IBS patients demonstrated more pronounced stress-induced modulation of neural activation in multiple brain regions, including the insula, midcingulate cortex, and ventrolateral prefrontal cortex. In response to relaxation, IBS patients demonstrated reduced modulation of distension-induced activation in the insula. During relaxation, the difference observed between groups could be accounted for by higher anxiety symptoms in patients with IBS; differential effects of stress in the insula and prefrontal regions were not attributable to anxiety.

Conclusions

IBS patients appear to have disrupted emotional modulation of neural responses to visceral stimuli, possibly reflecting the neural basis for altered visceral interoception by stress and negative emotions.

Section snippets

Inclusion and Exclusion Criteria

IBS patients meeting the Rome III criteria with an established diagnosis were recruited from 2 collaborating gastroenterology outpatient clinics and 1 gastroenterologist practice. General exclusion criteria included age <18 years and >50 years; body mass index ≥30; any concurrent medical condition, including neurologic, cardiovascular, immunologic; endocrine conditions; or medications known to affect the parameters of interest (eg, neuroleptics, antipsychotics, β-adrenergic medications). All

Participants

Fifteen IBS patients and 13 healthy controls participated. Because 1 healthy subject withdrew from participation after the second study day, full data sets were available from 12 healthy women serving as the control group. IBS patients did not differ in sociodemographic parameters from controls, with the exception of age and, expectedly demonstrated higher scores on various psychologic scales (Table 1). Two patients had a previous clinical diagnosis of depression. Based on the HADS, 1 patient

Discussion

This is the first study to assess effects of emotional context on behavioral and neural responses to visceral stimuli in IBS patients compared with controls. In summary, we found that IBS patients experienced markedly more distension-induced pain and discomfort irrespective of emotional condition, despite unaltered rectal sensory thresholds. IBS patients further demonstrated altered emotional modulation of distension-induced neural activation in anterior cingulate cortex, insula, and prefrontal

Acknowledgments

The authors thank A. Scholle and A. de Greiff for their excellent technical support in conducting this project.

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    Conflicts of interest The authors disclose no conflicts.

    Funding Supported by a grant from the German Research Foundation (Deutsche Forschungsgemeinschaft [DFG]) (DFG EL 236/5-2) (to S.E. and E.R.G.).

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