The effect of negative emotional context on neural and behavioural responses to oesophageal stimulation

Abstract

Sensory experience is influenced by emotional context. Although perception of emotion and unpleasant visceral sensation are associated with activation within the insula and dorsal and ventral anterior cingulate gyri (ACG), regions important for attention to and perception of sensory and emotional information, the neural mechanisms underlying the effect of emotional context upon visceral sensation remain unexplored. Using functional MRI, we examined neural responses to phasic, non-painful oesophageal sensation (OS) in eight healthy subjects (seven male; age range 27-36 years) either during neutral or negative emotional contexts produced, respectively, by presentation of neutral or fearful facial expressions. Activation within right insular and bilateral dorsal ACG was significantly greater (P < 0.01) during OS with fearful than with neutral faces. In a second experiment, we measured anxiety, discomfort and neural responses in eight healthy male subjects (age range 22-41 years) to phasic, non-painful OS during presentation of faces depicting either low, moderate or high intensities of fear. Significantly greater (P < 0.01) discomfort, anxiety and activation predominantly within the left dorsal ACG and bilateral anterior insulae occurred with high-intensity compared with low-intensity expressions. Clusters of voxels were also detected in this region, which exhibited a positive correlation between subjective behaviour and blood oxygenation level-dependent effect (P < 0.05). We report the first evidence for a modulation of neural responses, and perceived discomfort during, non-painful visceral stimulation by the intensity of the negative emotional context in which the stimulation occurs, and suggest a mechanism for the effect of negative context on symptoms in functional pain disorders.

Reproducibility of human brain activity evoked by esophageal stimulation using functional magnetic resonance imaging

“…The decision to continue with analysis and interpretation on seven subjects was based on several reasons: 1) Brain activity reported in the present experiment is analogous to previous studies that demonstrated that between six to eight volunteers provide adequate statistical power to produce a network of brain activity consistent with that of pain processing (3,25,53,68). 2) It is also important to note the consistency in activation across four intensities of stimulation and three scanning sessions.…”

“…However, data from the present study show that insula activity is consistent, regardless of stimulation level, suggesting that this region does not encode the intensity of visceral sensation. It may be more likely that the role of the anterior insula is in processing emotional responses to visceral sensation, as some previous studies suggest (51,53).…”

Brain-based Correlations Between Psychological Factors and Functional Dyspepsia

“…Therefore, our results may suggest the importance of the insula, ACC, MCC and midFC in dyspepsia-related sensations. In a previous study, Phillips et al 27 showed significantly higher brain activation in the insula and ACC as well as significantly greater discomfort and anxiety during esophageal stimuli with fearful faces than with neutral faces, providing first evidence for the neural mechanism underlying the influence of emotional context on symptoms in functional disorders. Although our results may not directly verify the role of psychological factors in visceral sensation, we showed the overlapping regions between dyspepsia symptoms and anxiety/depression.…”

Sex differences in brain response to anticipated and experienced visceral pain in healthy subjects

“…Psychological factors are considered to play a major role in mediating the differences in pain perception observed between men and women (23) and also influence the brain processing of pain (11,22,(42)(43)(44)54). For instance, it has been reported that personality, in particular neuroticism, modulates the brain processing of visceral pain and anticipation of pain (11).…”

“…The posterior insula processes information about the physiological condition of the body, whereas the anterior insula cortex processes subjective feelings from the body and emotional awareness through interoception (13). Activity in the anterior insula increases when visceral pain is delivered during negative emotional arousal (12,42). Mayer et al (34) have proposed a concept of homeostatic emotions, which are the motivations and feelings associated with changes in the body's physiological condition and are the background emotions that affect our mood and disposition.…”