Gender differences in regional brain response to visceral pressure in IBS patients

Berman, Steven M.; Munakata, Julie; Naliboff, Bruce D.; Chang, Lin; Mandelkern, M.; Silverman, D. H. S.; Kovalik, Edward; Mayer, Emeran A.

doi:10.1053/eujp.2000.0167

Cited by 158 publications

(118 citation statements)

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“…In the present study, we did not observe any activations and/or deactivations in ACC, hippocampus, and amygdala, which could be due to the sex differences in brain activation patterns in response to rectal distension as supported by the previous studies reporting on the gender differences in visceral pain perception. [61][62][63][64] Furthermore, some studies reported activations in ACC during non-painful visceral distension implicating the role of this region in the control of autonomic visceral responses rather than to pain perception. 18,27,65,66 However, we observed the activations only during painful visceral distension, which might be another reason for the absence of activations in ACC.…”

Section: Discussionmentioning

confidence: 99%

Mapping of Brain Activations to Rectal Balloon Distension Stimuli in Male Patients with Irritable Bowel Syndrome Using Functional Magnetic Resonance Imaging

Guleria

Karyampudi

Singh

et al. 2017

J Neurogastroenterol Motil

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Background/AimsIrritable bowel syndrome (IBS) is associated with exaggerated cerebral response including emotional processing following visceral stimulation; though data on this issue is available in female IBS patients, it is scanty among males. Hence, we aimed to study brain response of male IBS patients following rectal balloon distension as compared to healthy controls using functional magnetic resonance imaging (fMRI). Data between diarrhea and constipation predominant IBS (IBS-D and IBS-C) were also compared. MethodsRectal balloon distension threshold was assessed in 20 male IBS patients (10 IBS-C and 10 IBS-D) and 10 age-matched male healthy controls. Subsequently, fMRI on all the participants was performed at their respective rectal pain threshold. The fMRI data were analysed using the Statistical Parametric Mapping software. ResultsIBS patients showed greater cerebral activations in insula, middle temporal gyrus, and cerebellum in the left hemisphere compared to healthy controls. Neural activation was found in bilateral precuneus/superior parietal lobules in controls but not in patients with IBS. The brain activation differed among IBS-C and IBS-D patients; while the right mid-cingulate cortex was activated in IBS-C, the left inferior orbito-frontal cortex, left calcarine, and bilateral fusiform gyri were activated among patients with IBS-D following rectal balloon distension. Conclusions

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Section: Discussionmentioning

confidence: 99%

Mapping of Brain Activations to Rectal Balloon Distension Stimuli in Male Patients with Irritable Bowel Syndrome Using Functional Magnetic Resonance Imaging

Guleria

Karyampudi

Singh

et al. 2017

J Neurogastroenterol Motil

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“…When comparing male and female IBS patients, greater mid-pINS and aINS activation was found during INF in male patients in two different samples (Berman et al, 2000;Naliboff et al, 2003) and greater activation of mOFC, dACC and amygdala in female patients in one study (Naliboff et al, 2003). The greater aINS activation in men was replicated in a third sample of healthy men and women using fMRI .…”

Section: Possible Correlation Of Findings With Previously Reported Spmentioning

confidence: 99%

“…Using SPM analysis of [ 15 O] water PET data, we have previously reported sex-related differences in the brain's response to an aversive visceral stimulus, despite overall similarity of activated regions (Berman et al, 2000;Berman et al, 2006;Naliboff et al, 2003). When comparing male and female IBS patients, greater mid-pINS and aINS activation was found during INF in male patients in two different samples (Berman et al, 2000;Naliboff et al, 2003) and greater activation of mOFC, dACC and amygdala in female patients in one study (Naliboff et al, 2003).…”

Section: Possible Correlation Of Findings With Previously Reported Spmentioning

confidence: 99%

“…The greater subjective responses in female IBS patients may be related to sex differences in brain responses to visceral stimuli (Berman et al, 2000;Naliboff et al, 2003;Berman et al, 2006). For example, female patients showed greater activation of limbic and paralimbic regions, including the amygdala and the closely connected anterior cingulate cortex (ACC) while male patients demonstrated greater activation of the insula (INS).…”

Section: Introductionmentioning

confidence: 99%

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Sex differences in brain activity during aversive visceral stimulation and its expectation in patients with chronic abdominal pain: A network analysis

Labus¹,

Naliboff²,

Fallon³

et al. 2008

NeuroImage

127

115

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Differences in brain responses to aversive visceral stimuli may underlie previously reported sex differences in symptoms as well as perceptual and emotional responses to such stimuli in patients with Irritable Bowel Syndrome (IBS). The goal of the current study was to identify brain networks activated by expected and delivered aversive visceral stimuli in male and female patients with chronic abdominal pain, and to test for sex differences in the effective connectivity of the circuitry comprising these networks. Network analysis was applied to assess the brain response of 46 IBS patients (22 men and 24 women) recorded using [ 15 O] water positron emission tomography during rest/baseline and expected and delivered aversive rectal distension. Functional connectivity results from partial least squares analyses provided support for the hypothesized involvement of 3 networks corresponding to: 1) visceral afferent information processing (thalamus, insula and dorsal anterior cingulate cortex, orbital frontal cortex), 2) emotional arousal (amygdala, rostral and subgenual cingulate regions, and locus coeruleus complex) and 3) cortical modulation (frontal and parietal cortices). Effective connectivity results obtained via structural equation modeling indicated that sex-related differences in brain response are largely due to alterations in the effective connectivity of emotional-arousal circuitry rather than visceral afferent processing circuits. Sex differences in the cortico-limbic circuitry involved in emotional-arousal, pain facilitation and autonomic responses may underlie the observed differences in symptoms, and in perceptual and emotional responses to aversive visceral stimuli.

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“…8 While peripheral mediators likely affect GI motility, gender-associated differences in visceral pain perception in IBS patients have been demonstrated using brain imaging techniques such as positron emission tomography. 84 A study by Naliboff et al 85 has shown that compared to men with IBS, women with IBS utilized different areas of their brain, such as the amygdala, while experiencing a rectal distension they perceived as aversive. Moreover, other clinical studies have provided evidence that women's perception of visceral pain can be influenced by their cyclical changes in gonadal hormones.…”

Section: Sex Linked Differences In Visceral Sensitivitymentioning

confidence: 99%

Mechanisms of Stress-induced Visceral Pain

Meerveld

Johnson

2018

J Neurogastroenterol Motil

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Evidence suggests that long-term stress facilitates visceral pain through sensitization of pain pathways and promotes chronic visceral pain disorders such as the irritable bowel syndrome (IBS). This review will describe the importance of stress in exacerbating IBS-induced abdominal pain. Additionally, we will briefly review our understanding of the activation of the hypothalamic-pituitary-adrenal axis by both chronic adult stress and following early life stress in the pathogenesis of IBS. The review will focus on the glucocorticoid receptor and corticotropin-releasing hormone-mediated mechanisms in the amygdala involved in stress-induced visceral hypersensitivity. One potential mechanism underlying persistent effects of stress on visceral sensitivity could be epigenetic modulation of gene expression. While there are relatively few studies examining epigenetically mediated mechanisms involved in stress-induced visceral nociception, alterations in DNA methylation and histone acetylation patterns within the brain, have been linked to alterations in nociceptive signaling via increased expression of pro-nociceptive neurotransmitters. This review will discuss the latest studies investigating the long-term effects of stress on visceral sensitivity. Additionally, we will critically review the importance of experimental models of adult stress and early life stress in enhancing our understanding of the basic molecular mechanisms of nociceptive processing. Taken together, the complex clinical phenotype makes recapitulating IBS in rodent models extremely challenging. However, an aim of this review will be to describe how the use of rodent models of adult stress, early life stress (ELS), and a dysregulated HPA axis has improved our understanding of stress in the pathophysiology of IBS. Pathophysiology of Irritable Bowel Syndrome: Activation of the Brain-Gut AxisEvidence from clinical and basic research points to dysregulation of the bidirectional communication between the brain-gut axis in IBS. 21 The brain-gut axis represents a dynamic interplay between central circuits and peripheral mechanisms. The messengers of this complex circuit include neural, endocrine, metabolic, and immune mediators that are activated by central factors such as stress (Fig. 1). Although IBS is not an inflammatory disorder, the immune system plays a role in the pathogenesis of IBS in at least a subset of patients and likely contributes to the etiology of IBS symptoms. 22,23 A subset of IBS patients display a low grade chronic inflammation, and there is also evidence that following an enteric infection and combined with stressful life events, there is an increased risk of developed post-infectious IBS. [24][25][26][27] Clearly, the immune system and inflammatory processes are modulated by the HPA and autonomic nervous systems. In support, IBS patients also show increased number and reactivity of mast cells. 28,29 Data from peripheral blood mononuclear cells, as well as in mucosal biopsies, from IBS patients show that cytokines levels including TNF-α...

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Gender differences in regional brain response to visceral pressure in IBS patients

Cited by 158 publications

References 50 publications

Mapping of Brain Activations to Rectal Balloon Distension Stimuli in Male Patients with Irritable Bowel Syndrome Using Functional Magnetic Resonance Imaging

Mapping of Brain Activations to Rectal Balloon Distension Stimuli in Male Patients with Irritable Bowel Syndrome Using Functional Magnetic Resonance Imaging

Sex differences in brain activity during aversive visceral stimulation and its expectation in patients with chronic abdominal pain: A network analysis

Mechanisms of Stress-induced Visceral Pain

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