Abstract
Despite recent advances, there is still a major need to better understand the interactions between brain function and chronic gut inflammation and its clinical implications. Alterations in executive function have previously been identified in several chronic inflammatory conditions, including inflammatory bowel diseases. Inflammation-associated brain alterations can be captured by connectome analysis. Here, we used the resting-state fMRI data from 222 participants comprising three groups (ulcerative colitis (UC), irritable bowel syndrome (IBS), and healthy controls (HC), N = 74 each) to investigate the alterations in functional brain wiring and cortical stability in UC compared to the two control groups and identify possible correlations of these alterations with clinical parameters. Globally, UC participants showed increased functional connectivity and decreased modularity compared to IBS and HC groups. Regionally, UC showed decreased eigenvector centrality in the executive control network (UC < IBS < HC) and increased eigenvector centrality in the visual network (UC > IBS > HC). UC also showed increased connectivity in dorsal attention, somatomotor network, and visual networks, and these enhanced subnetwork connectivities were able to distinguish UC participants from HCs and IBS with high accuracy. Dynamic functional connectome analysis revealed that UC showed enhanced cortical stability in the medial prefrontal cortex (mPFC), which correlated with severe depression and anxiety-related measures. None of the observed brain changes were correlated with disease duration. Together, these findings are consistent with compromised functioning of networks involved in executive function and sensory integration in UC.
Highlights
Ulcerative colitis (UC) is an inflammatory bowel disease (IBD) characterized by chronically recurring episodes of inflammation of the colon’s mucosal lining followed by variable periods of remission
UC participants compared to either irritable bowel syndrome (IBS) or Healthy control (HC) were found to have a greater thickness in cingulate cortex subregions and primary somatosensory cortex but reduced thickness in the orbitofrontal cortex involved in executive functioning and the posterior insula, the primary interoceptive cortex [8]
Subnetworks differences Network-based statistics identified two subnetworks that differed between UC and HC participants. (Fig. 4a-d)
Summary
Ulcerative colitis (UC) is an inflammatory bowel disease (IBD) characterized by chronically recurring episodes of inflammation of the colon’s mucosal lining followed by variable periods of remission. Irritable bowel syndrome (IBS) is a disorder of brain-gut interactions that is characterized by chronically recurring abdominal pain and altered bowel habits in the absence of gastrointestinal (GI) inflammation [3, 4] Both gut disorders often show comorbid symptoms of anxiety and depression, and symptom flares are often triggered by psychosocial stress, suggesting that both diseases share dysregulation in the brain-gut axis [4,5,6]. Even though the altered brain responses were observed in response to an acute aversive rectal stimulus, one may speculate that these alterations may play a role in reduced perception of pain during chronic inflammation Consistent with these observations, increased functional connectivity in corticolimbic regions involving the bilateral middle frontal gyrus, anterior cingulate cortex (ACC), and the left caudate nucleus has been reported in UC patients with active inflammation [2].
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