Influence of Uncertain Anticipation on Brain Responses to Aversive Rectal Distension in Patients With Irritable Bowel Syndrome

Kano, Michiko; Muratsubaki, Tomohiko; Morishita, Joe; Kono, Keiji; Mugikura, Shunji; Takase, Kei; Ly, Huynh Giao; Dupont, Patrick; Oudenhove, Lukas Van; Fukudo, Shin

doi:10.1097/psy.0000000000000484

Cited by 22 publications

(23 citation statements)

References 47 publications

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“…39 Uncertain anticipation induced stronger MCC activation during the anticipation phase and in the MCC, PCC, and precuneus during subsequent rectal stimulation. 40 The anticipation of visceral pain is considered preparatory for cognitive coping strategies that affect the neural processing of the visceral sensation itself. FGID patients may show failure of this preparatory modulation.…”

Section: Anticipation Of Visceral Painmentioning

confidence: 99%

Understanding Neurogastroenterology From Neuroimaging Perspective: A Comprehensive Review of Functional and Structural Brain Imaging in Functional Gastrointestinal Disorders

Kano

Dupont

Aziz

et al. 2018

J Neurogastroenterol Motil

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This review provides a comprehensive overview of brain imaging studies of the brain-gut interaction in functional gastrointestinal disorders (FGIDs). Functional neuroimaging studies during gut stimulation have shown enhanced brain responses in regions related to sensory processing of the homeostatic condition of the gut (homeostatic afferent) and responses to salience stimuli (salience network), as well as increased and decreased brain activity in the emotional response areas and reduced activation in areas associated with the top-down modulation of visceral afferent signals. Altered central regulation of the endocrine and autonomic nervous responses, the key mediators of the brain-gut axis, has been demonstrated. Studies using resting-state functional magnetic resonance imaging reported abnormal local and global connectivity in the areas related to pain processing and the default mode network (a physiological baseline of brain activity at rest associated with self-awareness and memory) in FGIDs. Structural imaging with brain morphometry and diffusion imaging demonstrated altered gray- and white-matter structures in areas that also showed changes in functional imaging studies, although this requires replication. Molecular imaging by magnetic resonance spectroscopy and positron emission tomography in FGIDs remains relatively sparse. Progress using analytical methods such as machine learning algorithms may shift neuroimaging studies from brain mapping to predicting clinical outcomes. Because several factors contribute to the pathophysiology of FGIDs and because its population is quite heterogeneous, a new model is needed in future studies to assess the importance of the factors and brain functions that are responsible for an optimal homeostatic state.

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Section: Anticipation Of Visceral Painmentioning

confidence: 99%

Understanding Neurogastroenterology From Neuroimaging Perspective: A Comprehensive Review of Functional and Structural Brain Imaging in Functional Gastrointestinal Disorders

Kano

Dupont

Aziz

et al. 2018

J Neurogastroenterol Motil

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“…Brain responses to distention were similar for normosensitive patients and healthy controls, but hypersensitive patients showed greater insula response to visceral stimulation than healthy controls and normosensitive IBS patients (Larsson et al 2012). In our fMRI study, which matched patients and controls on subjective discomfort, brain responses were similar between healthy controls and patients with IBS (Kano et al 2017a).…”

Section: Initial Brain Imaging Approach To Reveal the Visceral Hypersmentioning

confidence: 47%

Imaging Brain Mechanisms of Functional Somatic Syndromes: Potential as a Biomarker?

Kano

Oudenhove

Dupont

et al. 2020

Tohoku J. Exp. Med.

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When patients present with persistent bodily complaints that cannot be explained by a symptom-linked organic pathology (medically unexplained symptoms), they are diagnosed with 'functional' somatic syndromes (FSS). Despite their prevalence, the management of FSS is notoriously challenging in clinical practice. This may be because FSS are heterogeneous disorders in terms of etiopathogenesis. They include patients with primarily peripheral dysfunction, primarily centrally driven somatic symptoms, and a mix of both. Brain-imaging studies, particularly data-driven pattern recognition methods using machine learning algorithms, could provide brain-based biomarkers for these clinical conditions. In this review, we provide an overview of our brain imaging data on brain-body interactions in one of the most well-known FSS, irritable bowel syndrome (IBS), and discuss the possible development of a brain-based biomarker for FSS. Anticipation of unpredictable pain, which commonly elicits fear in FSS patients, induced increased activity in brain areas associated with hypervigilance during rectal distention and non-distention conditions in IBS. This was coupled with dysfunctional inhibitory influence of the medial prefrontal cortex (mPFC) and pregenual anterior cingulate cortex (pACC) on stress regulation systems, resulting in the activated autonomic nervous system (ANS) and neuroendocrine system stimulated by corticotropin-releasing hormone (CRH). IBS subjects with higher alexithymia, a risk factor for FSS, showed stronger activity in the insula during rectal distention but reduced subjective sensitivity. Reduced top-down regulation of the ANS and CRH system by mPFC and pACC, discordance between the insula response to stimulation and subjective sensation of pain, and stronger threat responses in hypervigilance-related areas may be a candidate brain-based biomarker.

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“…Studies have reported that IBS patients showed high activation in the precuneus and surrounding areas under rectal stimulation, and decreased blood perfusion in this region and its functional connection with multiple brain regions under resting state, which were partially related to the depression score of patients. (27)(28)(29)(30). Therapeutic studies have shown that abnormal activity and recovery of DMN, especially in the left precuneus, may be a state indicator for predicting anxiety and depression (31)(32)(33).…”

Section: Discussionmentioning

confidence: 99%

Short-Term Effects of Flupentixol-Melitracen on Regional Brain Function in Patients with Irritable Bowel Syndrome: An fMRI Study

et al. 2020

Iran J Radiol

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Background: The efficacy of the treatment for irritable bowel syndrome (IBS) with the combination of anxiolytic/antidepressant has been confirmed by clinical studies, but the central mechanism is unclear. Objectives: To investigate the effects of flupentixol-melitracen, a mixture of tricyclic antidepressant and a classical antipsychotic component, on resting-state brain function in IBS patients by using functional magnetic resonance imaging (fMRI). Patients and Methods: Thirty-two patients with IBS were randomly divided into an observation group (OG, n = 16) and control group (CG, n = 16). All patients in both groups were given spasmolytic agent (pinaverium bromide). For the OG group, flupentixolmelitracen was added. FMRI scans were performed in all patients before and four weeks after the therapy. The scores of gastrointestinal symptom rating scale (GSRS), Hamilton depression scale (HAMD-17) and anxiety scale (HAMA-14) were evaluated at the same time. FMRI regional homogeneity (ReHo) parameters were compared between the two groups before and after treatment using a 2 (therapy) × 2 (time) mixed model analysis of variance (ANOVA) statistical method, and were correlated with the changes of GSRS, HAMD and HAMA scores in the two groups. Results: The fMRI results of the mixed-model analysis of covariance (ANCOVA) and post analyses were as follows. When the therapeutic factor was the main effect, ReHo was increased in the left superior and middle occipital gyrus, and the left parietal gyrus, and decreased in the left thalamus and the lenticular nucleus in both groups after treatment when compared to the unmedicated state. In addition, the OG group showed decreased ReHo in the left superior temporal gyrus, the right lenticular-putamen nucleus, the right inferior frontal gyrus, the right insula, the right gyrus rectus and subcallosal gyrus. The CG group showed increased ReHo in the right angular gyrus. When the interaction between therapy and time was the main effect, the brain region with different ReHo values was in the left precuneus. In the OG group, the change of ReHo in the left precuneus was negatively correlated with the decrease of HAMD and HAMA scores. Conclusion: Flupentixol-melitracen can effectively improve anxiety, depression and gastrointestinal symptoms in patients with IBS, which may be related to the reversal of abnormal neural activity in the brain regions within the default network and the prefrontal-limbic-temporal emotional circuit in IBS patients.

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Influence of Uncertain Anticipation on Brain Responses to Aversive Rectal Distension in Patients With Irritable Bowel Syndrome

Abstract: Preceding uncertainty differentially modulates the brain processing of physiologically identical rectal stimulation in IBS patients. Cue-dependent alterations in brain responses may underlie hypervigilance to visceral sensations in IBS patients.

Cited by 22 publications

References 47 publications

Understanding Neurogastroenterology From Neuroimaging Perspective: A Comprehensive Review of Functional and Structural Brain Imaging in Functional Gastrointestinal Disorders

Understanding Neurogastroenterology From Neuroimaging Perspective: A Comprehensive Review of Functional and Structural Brain Imaging in Functional Gastrointestinal Disorders

Imaging Brain Mechanisms of Functional Somatic Syndromes: Potential as a Biomarker?

Short-Term Effects of Flupentixol-Melitracen on Regional Brain Function in Patients with Irritable Bowel Syndrome: An fMRI Study

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