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      Elucidating the putative link between prefrontal neurotransmission, functional connectivity, and affective symptoms in irritable bowel syndrome

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          Abstract

          Altered neural mechanisms are well-acknowledged in irritable bowel syndrome (IBS), a disorder of brain-gut-communication highly comorbid with anxiety and depression. As a key hub in corticolimbic inhibition, medial prefrontal cortex (mPFC) may be involved in disturbed emotion regulation in IBS. However, aberrant mPFC excitatory and inhibitory neurotransmission potentially contributing to psychological symptoms in IBS remains unknown. Using quantitative magnetic resonance spectroscopy (qMRS), we compared mPFC glutamate + glutamine (Glx) and γ-aminobutyric acid (GABA+) concentrations in 64 women with IBS and 32 age-matched healthy women (HCs) and investigated their association with anxiety and depression in correlational and subgroup analyses. Applying functional magnetic resonance imaging (fMRI), we explored whether altered neurotransmission was paralleled by aberrant mPFC resting-state functional connectivity (FC). IBS patients did not differ from HCs with respect to mPFC GABA+ or Glx levels. Anxiety was positively associated with mPFC GABA+ concentrations in IBS, whereas Glx was unrelated to psychological or gastrointestinal symptoms. Subgroup comparisons of patients with high or low anxiety symptom severity and HCs revealed increased GABA+ in patients with high symptom severity, and lower mPFC FC with adjacent anterior cingulate cortex (ACC), a crucial region of emotion modulation. Our findings provide novel evidence that altered prefrontal inhibitory neurotransmission may be linked to anxiety in IBS.

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          Most cited references55

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          Emotional processing in anterior cingulate and medial prefrontal cortex.

          Negative emotional stimuli activate a broad network of brain regions, including the medial prefrontal (mPFC) and anterior cingulate (ACC) cortices. An early influential view dichotomized these regions into dorsal-caudal cognitive and ventral-rostral affective subdivisions. In this review, we examine a wealth of recent research on negative emotions in animals and humans, using the example of fear or anxiety, and conclude that, contrary to the traditional dichotomy, both subdivisions make key contributions to emotional processing. Specifically, dorsal-caudal regions of the ACC and mPFC are involved in appraisal and expression of negative emotion, whereas ventral-rostral portions of the ACC and mPFC have a regulatory role with respect to limbic regions involved in generating emotional responses. Moreover, this new framework is broadly consistent with emerging data on other negative and positive emotions. Published by Elsevier Ltd.
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            The irritable bowel severity scoring system: a simple method of monitoring irritable bowel syndrome and its progress.

            The clinical assessment and investigation of irritable bowel syndrome would be greatly facilitated by the introduction of a simple, easy to use severity scoring system. Such a system, developed in our department over a number of years, has been submitted to validation in a total of 141 patients and 40 healthy controls. The system, incorporating pain, distension, bowel dysfunction and quality of life/global well-being, was assessed for its ability to reliably score patients previously classified as mild, moderate or severe. The reproducibility and sensitivity to change of the system was also assessed. The maximum achievable score was 500. Mild, moderate and severe cases were indicated by scores of 75 to 175, 175 to 300 and > 300 respectively. Controls scored below 75 and patients scoring in this range can be considered to be in remission. There was a highly significant difference between controls and patients as a whole (P = 0.0001) as well as significant differences (P < 0.01) between all severity categories. Scores repeated within 24 h were very reproducible and sensitivity to change was also extremely good (P < 0.001) with a change of 50 reliably indicating improvement. These results suggest that this scoring system should prove to be a valuable instrument in helping to meet the many challenges offered by irritable bowel syndrome.
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              Simultaneous in vivo spectral editing and water suppression.

              Water suppression is typically performed in vivo by exciting the longitudinal magnetization in combination with dephasing, or by using frequency-selective coherence generation. MEGA, a frequency-selective refocusing technique, can be placed into any pulse sequence element designed to generate a Hahn spin-echo or stimulated echo, to dephase transverse water coherences with minimal spectral distortions. Water suppression performance was verified in vivo using stimulated echo acquisition mode (STEAM) localization, which provided water suppression comparable with that achieved with four selective pulses in 3,1-DRYSTEAM. The advantage of the proposed method was exploited for editing J-coupled resonances. Using a double-banded pulse that selectively inverts a J-coupling partner and simultaneously suppresses water, efficient metabolite editing was achieved in the point resolved spectroscopy (PRESS) and STEAM sequences in which MEGA was incorporated. To illustrate the efficiency of the method, the detection of gamma-aminobutyric acid (GABA) was demonstrated, with minimal contributions from macromolecules and overlying singlet peaks at 4 T. The estimated occipital GABA concentration was consistent with previous reports, suggesting that editing for GABA is efficient when based on MEGA at high field strengths.
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                Author and article information

                Contributors
                adriane.icenhour@uk-essen.de
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                19 September 2019
                19 September 2019
                2019
                : 9
                : 13590
                Affiliations
                [1 ]ISNI 0000 0001 2162 9922, GRID grid.5640.7, Department of Gastroenterology and Department of Clinical and Experimental Medicine, , Linköping University, ; Linköping, Sweden
                [2 ]ISNI 0000 0001 2162 9922, GRID grid.5640.7, Center for Medical Image Science and Visualization (CMIV), , Linköping University, ; Linköping, Sweden
                [3 ]ISNI 0000 0001 2162 9922, GRID grid.5640.7, Department of Medical and Health Sciences, , Linköping University, ; Linköping, Sweden
                [4 ]ISNI 0000 0001 2162 9922, GRID grid.5640.7, Department of Radiation Physics, Department of Medical and Health Sciences, , Linköping University, ; Linköping, Sweden
                [5 ]ISNI 0000 0001 2162 9922, GRID grid.5640.7, Department of Radiology, Department of Medical and Health Sciences, , Linköping University, ; Linköping, Sweden
                [6 ]Institute of Medical Psychology and Behavioral Immunobiology, University Hospital Essen, University of Duisburg-Essen, Essen, Germany
                Article
                50024
                10.1038/s41598-019-50024-3
                6753205
                31537890
                41d693d8-3977-47a7-9884-bb4148f84e3b
                © The Author(s) 2019

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 4 February 2019
                : 15 August 2019
                Funding
                Funded by: FundRef https://doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft (German Research Foundation);
                Award ID: IC 81/1-1
                Award ID: project number 316803389 – SFB 1280
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/501100004063, Knut och Alice Wallenbergs Stiftelse (Knut and Alice Wallenberg Foundation);
                Funded by: Kurt and Helena Widéns Research fund
                Funded by: FundRef https://doi.org/10.13039/501100002706, AFA Försäkring (AFA Insurance Foundation);
                Funded by: FundRef https://doi.org/10.13039/501100009336, Bengt Ihres Foundation;
                Funded by: County Council Östergötland
                Categories
                Article
                Custom metadata
                © The Author(s) 2019

                Uncategorized
                human behaviour,comorbidities
                Uncategorized
                human behaviour, comorbidities

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