Gastroenterology

Gastroenterology

Volume 141, Issue 3, September 2011, Pages 909-917.e1
Gastroenterology

Original Research
Basic and Translational—Alimentary Tract
Neuroticism Influences Brain Activity During the Experience of Visceral Pain

https://doi.org/10.1053/j.gastro.2011.06.008Get rights and content

Background & Aims

One particularly important individual dynamic known to influence the experience of pain is neuroticism, of which little is known about in visceral pain research. Our aim was to study the relationship between neuroticism, psychophysiologic response, and brain processing of visceral pain.

Methods

Thirty-one healthy volunteers (15 male; age range, 22–38 years) participated in the study. The Eysenck Personality Questionnaire was used to assess neuroticism. Skin conductance level, pain ratings, and functional magnetic resonance imaging data were acquired during anticipation of pain and painful esophageal distention. The effect of neuroticism was assessed using correlation analysis.

Results

There was a wide spread of neuroticism scores (range, 0–22) but no influence of neuroticism on skin conductance level and pain tolerance or pain ratings. However, a positive correlation between brain activity and neuroticism during anticipation was found in regions associated with emotional and cognitive pain processing, including the parahippocampus, insula, thalamus, and anterior cingulate cortex. These regions showed a negative correlation with neuroticism during pain (P < .001).

Conclusions

This study provides novel data suggesting higher neuroticism is associated with engagement of brain regions responsible for emotional and cognitive appraisal during anticipation of pain but reduced activity in these regions during pain. This may reflect a maladaptive mechanism in those with higher neuroticism that promotes overarousal during anticipation and avoidance coping during pain.

Section snippets

Volunteers

Thirty-one healthy volunteers (15 male; mean age, 30 years; range, 22–38 years; all right-handed) participated in the study after providing informed written consent and approval was obtained from the local ethics committee (reference CREC/07/08-7). All volunteers were screened for a history of psychiatric or gastrointestinal symptoms and were not taking any medications. Subjects completed the Eysenck Personality Questionnaire-Revised (EPQ-R)21 to assess neuroticism level (neuroticism range,

Group Psychometric Data

All 31 volunteers tolerated the study well. There was a wide range of neuroticism scores (mean, 8.1 ± 1.2; range, 0–22) with no significant difference between male and female subjects (mean neuroticism ± SEM; male, 9 ± 1.7 [range, 0–20]; female, 7.4 ± 1.4 [range, 1–20]; P = .49, t = 0.68, df 29). There was also a scope of state/trait anxiety scores across the group (mean state anxiety, 29.7 ± 1.2 [range, 20–41]; mean trait anxiety, 34.4 ± 1.7 [range, 20–58]).

Group Physiologic Data

All volunteers rated the esophageal

Discussion

To our knowledge, this is the first study to report a significant effect of neuroticism on brain processing during visceral pain stimulation and anticipation. The level of brain activity during anticipation and pain varied depending on neuroticism score in several brain regions previously shown to be involved in pain processing, including the mid-ACC (BA24), perigenual ACC (BA32), insula, thalamus, inferior frontal gyrus, PCC, and supplementary motor area (SMA).

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    Conflicts of interest The authors disclose the following: Q.A. has received educational grants from GlaxoSmithKline, Pfizer, and Novartis, none of which are relevant to the work described in this report. S.J.C., M.K. A.D.F., V.K., V.G., M.B., and S.C.R.W. disclose no conflicts.

    Funding Supported jointly by a Medical Research Council grant (to Q.A.) and a British Academy grant (to S.J.C.).

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