Journal of Neurogastroenterology and Motility

The Korean Society of Neurogastroenterology and Motility (대한소화기 기능성질환 운동학회)
권호 표지
DOI QR코드

DOI QR Code

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

  • Kano, Michiko (Frontier Research Institute for Interdisciplinary Sciences (FRIS), Tohoku University) ;
  • Dupont, Patrick (Laboratory for Cognitive Neurology, KU Leuven) ;
  • Aziz, Qasim (Center for Digestive Diseases, Wingate Institute of Neurogastroenterology, Barts and the London School of Medicine and Dentistry, Queen Mary College, University of London) ;
  • Fukudo, Shin (Behavioral Medicine, Graduate School of Medicine, Tohoku University)
  • Received : 2018.04.10
  • Accepted : 2018.05.21
  • Published : 2018.10.30
⟨ Previous Next ⟩

Abstract

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.

Keywords

Acknowledgement

Supported by : Japanese Ministry of Education, Science and Culture

References

  1. Drossman DA. Functional gastrointestinal disorders: history, pathophysiology, clinical features and Rome IV. Gastroenterology 2016;150:1262-1279, e2. https://doi.org/10.1053/j.gastro.2016.02.032
  2. Aziz Q, Thompson DG. Brain-gut axis in health and disease. Gastroenterology 1998;114:559-578. https://doi.org/10.1016/S0016-5085(98)70540-2
  3. Mayer EA. Gut feelings: the emerging biology of gut-brain communication. Nat Rev Neurosci 2011;12:453-466.
  4. Fukudo S, Nomura T, Muranaka M, Taguchi F. Brain-gut response to stress and cholinergic stimulation in irritable bowel syndrome. A preliminary study. J Clin Gastroenterol 1993;17:133-141. https://doi.org/10.1097/00004836-199309000-00009
  5. Silverman DH, Munakata JA, Ennes H, Mandelkern MA, Hoh CK, Mayer EA. Regional cerebral activity in normal and pathological perception of visceral pain. Gastroenterology 1997;112:64-72. https://doi.org/10.1016/S0016-5085(97)70220-8
  6. Aziz Q, Andersson JL, Valind S, et al. Identification of human brain loci processing esophageal sensation using positron emission tomography. Gastroenterology 1997;113:50-59. https://doi.org/10.1016/S0016-5085(97)70079-9
  7. Vandenberghe J, Dupont P, Van Oudenhove L, et al. Regional cerebral blood flow during gastric balloon distention in functional dyspepsia. Gastroenterology 2007;132:1684-1693. https://doi.org/10.1053/j.gastro.2007.03.037
  8. Mahadeva S, Goh KL. Epidemiology of functional dyspepsia: a global perspective. World J Gastroenterol 2006;12:2661-2666. https://doi.org/10.3748/wjg.v12.i17.2661
  9. Lovell RM, Ford AC. Global prevalence of and risk factors for irritable bowel syndrome: a meta-analysis. Clin Gastroenterol Hepatol 2012;10:712-721, e4. https://doi.org/10.1016/j.cgh.2012.02.029
  10. Van Oudenhove L, Crowell MD, Drossman DA, et al. Biopsychosocial aspects of functional gastrointestinal disorders: how central and environmental processes contribute to the development and expression of functional gastrointerinal disorders. Gastroenterology 2016;150:1355-1367, e2. https://doi.org/10.1053/j.gastro.2016.02.027
  11. Drossman DA, Hasler WL. Rome IV-functional GI disorders: disorders of gut-brain interaction. Gastroenterology 2016;150:1257-1261. https://doi.org/10.1053/j.gastro.2016.03.035
  12. Enck P, Aziz Q, Barbara G, et al. Irritable bowel syndrome. Nat Rev Dis Primers 2016;2:16014. https://doi.org/10.1038/nrdp.2016.14
  13. Fukudo S. IBS: Autonomic dysregulation in IBS. Nat Rev Gastroenterol Hepatol 2013;10:569-571. https://doi.org/10.1038/nrgastro.2013.166
  14. Cawthon CR, de La Serre CB. Gut bacteria interaction with vagal afferents. Brain Res 2018;pii:S0006-8993(18)30020-9.
  15. Vanner S, Greenwood-Van Meerveld B, Mawe G, et al. Fundamentals of neurogastroenterology: basic science. Gastroenterology 2016;150:1280-1291. https://doi.org/10.1053/j.gastro.2016.02.018
  16. Mayer EA, Labus JS, Tillisch K, Cole SW, Baldi P. Towards a systems view of IBS. Nat Rev Gastroenterol Hepatol 2015;12:592-605. https://doi.org/10.1038/nrgastro.2015.121
  17. Fukudo S. Role of corticotropin-releasing hormone in irritable bowel syndrome and intestinal inflammation. J Gastroenterol 2007;42(suppl 17):48-51. https://doi.org/10.1007/s00535-006-1942-7
  18. Ulrich-Lai YM, Herman JP. Neural regulation of endocrine and autonomic stress responses. Nat Rev Neurosci 2009;10:397-409. https://doi.org/10.1038/nrn2647
  19. Chang L. The role of stress on physiologic responses and clinical symptoms in irritable bowel syndrome. Gastroenterology 2011;140:761-765. https://doi.org/10.1053/j.gastro.2011.01.032
  20. Stengel A, Tache Y. CRF and urocortin peptides as modulators of energy balance and feeding behavior during stress. Front Neurosci 2014;8:52.
  21. Mayer EA, Gupta A, Kilpatrick LA, Hong JY. Imaging brain mechanisms in chronic visceral pain. Pain 2015;156(suppl 1):S50-S63. https://doi.org/10.1097/j.pain.0000000000000106
  22. Mayer EA, Aziz Q, Coen S, et al. Brain imaging approaches to the study of functional GI disorders: a rome working team report. Neurogastroenterol Motil 2009;21:579-596. https://doi.org/10.1111/j.1365-2982.2009.01304.x
  23. Al Omran Y, Aziz Q. Functional brain imaging in gastroenterology: to new beginnings. Nat Rev Gastroenterol Hepatol 2014;11:565-576. https://doi.org/10.1038/nrgastro.2014.89
  24. Legrain V, Iannetti GD, Plaghki L, Mouraux A. The pain matrix reloaded: a salience detection system for the body. Prog Neurobiol 2011;93:111-124. https://doi.org/10.1016/j.pneurobio.2010.10.005
  25. Tillisch K, Mayer EA, Labus JS. Quantitative meta-analysis identifies brain regions activated during rectal distension in irritable bowel syndrome. Gastroenterology 2011;140:91-100. https://doi.org/10.1053/j.gastro.2010.07.053
  26. Sheehan J, Gaman A, Vangel M, Kuo B. Pooled analysis of brain activity in irritable bowel syndrome and controls during rectal balloon distension. Neurogastroenterol Motil 2011;23:336-346, e158. https://doi.org/10.1111/j.1365-2982.2010.01635.x
  27. Van Oudenhove L, Vandenberghe J, Dupont P, et al. Regional brain activity in functional dyspepsia: a $H_2^{15}O$-PET study on the role of gastric sensitivity and abuse history. Gastroenterology 2010;139:36-47. https://doi.org/10.1053/j.gastro.2010.04.015
  28. Larsson MB, Tillisch K, Craig AD, et al. Brain responses to visceral stimuli reflect visceral sensitivity thresholds in patients with irritable bowel syndrome. Gastroenterology 2012;142:463-472, e3. https://doi.org/10.1053/j.gastro.2011.11.022
  29. Phillips ML, Gregory LJ, Cullen S, et al. The effect of negative emotional context on neural and behavioural responses to oesophageal stimulation. Brain 2003;126:669-684. https://doi.org/10.1093/brain/awg065
  30. Coen SJ, Yaguez L, Aziz Q, et al. Negative mood affects brain processing of visceral sensation. Gastroenterology 2009;137:253-261, e1-e2. https://doi.org/10.1053/j.gastro.2009.02.052
  31. Elsenbruch S, Rosenberger C, Bingel U, Forsting M, Schedlowski M, Gizewski ER. Patients with irritable bowel syndrome have altered emotional modulation of neural responses to visceral stimuli. Gastroenterology 2010;139:1310-1319. https://doi.org/10.1053/j.gastro.2010.06.054
  32. Van Oudenhove L, McKie S, Lassman D, et al. Fatty acid-induced gutbrain signaling attenuates neural and behavioral effects of sad emotion in humans. J Clin Invest 2011;121:3094-3099. https://doi.org/10.1172/JCI46380
  33. Coen SJ, Kano M, Farmer AD, et al. Neuroticism influences brain activity during the experience of visceral pain. Gastroenterology 2011;141:909-917, e1. https://doi.org/10.1053/j.gastro.2011.06.008
  34. Van Oudenhove L, Vandenberghe J, Dupont P, et al. Abnormal regional brain activity during rest and (anticipated) gastric distension in functional dyspepsia and the role of anxiety: a H2 15O-PET study. Am J Gastroenterol 2010;105:913-924. https://doi.org/10.1038/ajg.2010.39
  35. Ringel Y, Drossman DA, Leserman JL, et al. Effect of abuse history on pain reports and brain responses to aversive visceral stimulation: an FMRI study. Gastroenterology 2008;134:396-404. https://doi.org/10.1053/j.gastro.2007.11.011
  36. Videlock EJ, Adeyemo M, Licudine A, et al. Childhood trauma is associated with hypothalamic-pituitary-adrenal axis responsiveness in irritable bowel syndrome. Gastroenterology 2009;137:1954-1962. https://doi.org/10.1053/j.gastro.2009.08.058
  37. Provencal N, Suderman MJ, Guillemin C, et al. The signature of maternal rearing in the methylome in rhesus macaque prefrontal cortex and T cells. J Neurosci 2012;32:15626-15642. https://doi.org/10.1523/JNEUROSCI.1470-12.2012
  38. Provencal N, Binder EB. The effects of early life stress on the epigenome: from the womb to adulthood and even before. Exp Neurol 2015;268:10-20. https://doi.org/10.1016/j.expneurol.2014.09.001
  39. Berman SM, Naliboff BD, Suyenobu B, et al. Reduced brainstem inhibition during anticipated pelvic visceral pain correlates with enhanced brain response to the visceral stimulus in women with irritable bowel syndrome. J Neurosci 2008;28:349-359. https://doi.org/10.1523/JNEUROSCI.2500-07.2008
  40. Kano M, Muratsubaki T, Morishita J, et al. Influence of uncertain anticipation on brain responses to aversive rectal distension in patients with irritable bowel syndrome. Psychosom Med 2017;79:988-999. https://doi.org/10.1097/PSY.0000000000000484
  41. Yaguez L, Coen S, Gregory LJ, et al. Brain response to visceral aversive conditioning: a functional magnetic resonance imaging study. Gastroenterology 2005;128:1819-1829. https://doi.org/10.1053/j.gastro.2005.02.068
  42. Icenhour A, Langhorst J, Benson S, et al. Neural circuitry of abdominal pain-related fear learning and reinstatement in irritable bowel syndrome. Neurogastroenterol Motil 2015;27:114-127. https://doi.org/10.1111/nmo.12489
  43. Lu HC, Hsieh JC, Lu CL, et al. Neuronal correlates in the modulation of placebo analgesia in experimentally-induced esophageal pain: a 3TfMRI study. Pain 2010;148:75-83. https://doi.org/10.1016/j.pain.2009.10.012
  44. Kotsis V, Benson S, Bingel U, et al. Perceived treatment group affects behavioral and neural responses to visceral pain in a deceptive placebo study. Neurogastroenterol Motil 2012;24:935-e462. https://doi.org/10.1111/j.1365-2982.2012.01968.x
  45. Price DD, Craggs J, Verne GN, Perlstein WM, Robinson ME. Placebo analgesia is accompanied by large reductions in pain-related brain activity in irritable bowel syndrome patients. Pain 2007;127:63-72. https://doi.org/10.1016/j.pain.2006.08.001
  46. Lee HF, Hsieh JC, Lu CL, et al. Enhanced affect/cognition-related brain responses during visceral placebo analgesia in irritable bowel syndrome patients. Pain 2012;153:1301-1310. https://doi.org/10.1016/j.pain.2012.03.018
  47. Schmid J, Langhorst J, Gass F, et al. Placebo analgesia in patients with functional and organic abdominal pain: a fMRI study in IBS, UC and healthy volunteers. Gut 2015;64:418-427. https://doi.org/10.1136/gutjnl-2013-306648
  48. Labus JS, Naliboff BD, Berman SM, et al. Brain networks underlying perceptual habituation to repeated aversive visceral stimuli in patients with irritable bowel syndrome. Neuroimage 2009;47:952-960. https://doi.org/10.1016/j.neuroimage.2009.05.078
  49. Aizawa E, Sato Y, Kochiyama T, et al. Altered cognitive function of prefrontal cortex during error feedback in patients with irritable bowel syndrome, based on FMRI and dynamic causal modeling. Gastroenterology 2012;143:1188-1198. https://doi.org/10.1053/j.gastro.2012.07.104
  50. Wilder-Smith CH. The balancing act: endogenous modulation of pain in functional gastrointestinal disorders. Gut 2011;60:1589-1599. https://doi.org/10.1136/gutjnl-2011-300253
  51. Tanaka Y, Kanazawa M, Kano M, et al. Differential activation in amygdala and plasma noradrenaline during colorectal distention by administration of corticotropin-releasing hormone between healthy individuals and patients with irritable bowel syndrome. PLoS One 2016;11:e0157347. https://doi.org/10.1371/journal.pone.0157347
  52. Farmer AD, Coen SJ, Kano M, et al. Psychophysiological responses to pain identify reproducible human clusters. Pain 2013;154:2266-2276. https://doi.org/10.1016/j.pain.2013.05.016
  53. Fukudo S, Kanazawa M, Mizuno T, et al. Impact of serotonin transporter gene polymorphism on brain activation by colorectal distention. Neuroimage 2009;47:946-951. https://doi.org/10.1016/j.neuroimage.2009.04.083
  54. Kano M, Muratsubaki T, Van Oudenhove L, et al. Altered brain and gut responses to corticotropin-releasing hormone (CRH) in patients with irritable bowel syndrome. Sci Rep 2017;7:12425. https://doi.org/10.1038/s41598-017-09635-x
  55. Kano M, Farmer AD, Aziz Q, et al. Sex differences in brain response to anticipated and experienced visceral pain in healthy subjects. Am J Physiol Gastrointest Liver Physiol 2013;304:G687-G699. https://doi.org/10.1152/ajpgi.00385.2012
  56. Labus JS, Naliboff BN, Fallon J, et al. Sex differences in brain activity during aversive visceral stimulation and its expectation in patients with chronic abdominal pain: a network analysis. Neuroimage 2008;41:1032-1043. https://doi.org/10.1016/j.neuroimage.2008.03.009
  57. van den Heuvel MP, Hulshoff Pol HE. Exploring the brain network: a review on resting-state fMRI functional connectivity. Eur Neuropsychopharmacol 2010;20:519-534. https://doi.org/10.1016/j.euroneuro.2010.03.008
  58. Raichle ME. The restless brain; how intrinsic activity organizes brain function. Philos Trans R Soc Lond B Biol Sci 2015;370:20140172. https://doi.org/10.1098/rstb.2014.0172
  59. Zhan X, Yu R. A window into the brain: advances in psychiatric fMRI. Biomed Research International 2015;2015:542467.
  60. Bijsterbosch J, Harrison S, Duff E, Alfaro-Almagro F, Woolrich M, Smith S. Investigations into within- and between-subject resting-state amplitude variations. Neuroimage 2017;159:57-69. https://doi.org/10.1016/j.neuroimage.2017.07.014
  61. Hong JY, Kilpatrick LA, Labus J, et al. Patients with chronic visceral pain show sex-related alterations in intrinsic oscillations of the resting brain. J Neurosci 2013;33:11994-12002. https://doi.org/10.1523/JNEUROSCI.5733-12.2013
  62. Qi R, Liu C, Ke J, et al. Abnormal amygdala resting-state functional connectivity in irritable bowel syndrome. AJNR Am J Neuroradiol 2016;37:1139-1145. https://doi.org/10.3174/ajnr.A4655
  63. Icenhour A, Witt ST, Elsenbruch S, et al. Brain functional connectivity is associated with visceral sensitivity in women with irritable bowel syndrome. Neuroimage Clin 2017;15:449-457. https://doi.org/10.1016/j.nicl.2017.06.001
  64. Ma X, Li S, Tian J, et al. Altered brain spontaneous activity and connectivity network in irritable bowel syndrome patients: a resting-state fMRI study. Clin Neurophysiol 2015;126:1190-1197. https://doi.org/10.1016/j.clinph.2014.10.004
  65. Qi R, Liu C, Ke J, et al. Intrinsic brain abnormalities in irritable bowel syndrome and effect of anxiety and depression. Brain Imaging Behav 2016;10:1127-1134. https://doi.org/10.1007/s11682-015-9478-1
  66. Ke J, Qi R, Liu C, et al. Abnormal regional homogeneity in patients with irritable bowel syndrome: a resting-state functional MRI study. Neurogastroenterol Motil 2015;27:1796-1803. https://doi.org/10.1111/nmo.12692
  67. Weng Y, Qi R, Liu C, et al. Disrupted functional connectivity density in irritable bowel syndrome patients. Brain Imaging Behav 2017;11:1812-1822. https://doi.org/10.1007/s11682-016-9653-z
  68. Qi R, Ke J, Schoepf UJ, et al. Topological reorganization of the default mode network in irritable bowel syndrome. Mol Neurobiol 2016;53:6585-6593. https://doi.org/10.1007/s12035-015-9558-7
  69. Liu P, Wang G, Liu Y, et al. Disrupted intrinsic connectivity of the periaqueductal gray in patients with functional dyspepsia: a resting-state fMRI study. Neurogastroenterol Motil Published Online First: 24 Mar 2017. doi: 10.1111/nmo.13060.
  70. Zhou G, Liu P, Zeng F, et al. Increased interhemispheric resting-state functional connectivity in functional dyspepsia: a pilot study. NMR Biomed 2013;26:410-415. https://doi.org/10.1002/nbm.2878
  71. Liu P, Zeng F, Zhou G, et al. Alterations of the default mode network in functional dyspepsia patients: a resting-state fmri study. Neurogastroenterol Motil 2013;25:e382-e388. https://doi.org/10.1111/nmo.12131
  72. Nan J, Liu J, Li G, et al. Whole-brain functional connectivity identification of functional dyspepsia. PLoS One 2013;8:e65870. https://doi.org/10.1371/journal.pone.0065870
  73. Zhou G, Liu P, Wang J, et al. Fractional amplitude of low-frequency fluctuation changes in functional dyspepsia: a resting-state fMRI study. Magn Reson Imaging 2013;31:996-1000. https://doi.org/10.1016/j.mri.2013.03.019
  74. Liu P, Qin W, Wang J, et al. Identifying neural patterns of functional dyspepsia using multivariate pattern analysis: a resting-state FMRI study. PLoS One 2013;8:e68205. https://doi.org/10.1371/journal.pone.0068205
  75. Nan J, Liu J, Zhang D, et al. Altered intrinsic regional activity and corresponding brain pathways reflect the symptom severity of functional dyspepsia. Neurogastroenterol Motil 2014;26:660-669. https://doi.org/10.1111/nmo.12311
  76. Kanai R, Rees G. The structural basis of inter-individual differences in human behaviour and cognition. Nat Rev Neurosci 2011;12:231-242.
  77. Blankstein U, Chen J, Diamant NE, Davis KD. Altered brain structure in irritable bowel syndrome: potential contributions of pre-existing and disease-driven factors. Gastroenterology 2010;138:1783-1789. https://doi.org/10.1053/j.gastro.2009.12.043
  78. Seminowicz DA, Labus JS, Bueller JA, et al. Regional gray matter density changes in brains of patients with irritable bowel syndrome. Gastroenterology 2010;139:48-57, e2. https://doi.org/10.1053/j.gastro.2010.03.049
  79. Jiang Z, Dinov ID, Labus J, et al. Sex-related differences of cortical thickness in patients with chronic abdominal pain. PLoS One 2013;8:e73932. https://doi.org/10.1371/journal.pone.0073932
  80. Labus JS, Dinov ID, Jiang Z, et al. Irritable bowel syndrome in female patients is associated with alterations in structural brain networks. Pain 2014;155:137-149. https://doi.org/10.1016/j.pain.2013.09.020
  81. Piche M, Chen JI, Roy M, Poitras P, Bouin M, Rainville P. Thicker posterior insula is associated with disease duration in women with irritable bowel syndrome (IBS) whereas thicker orbitofrontal cortex predicts reduced pain inhibition in both IBS patients and controls. J Pain 2013;14:1217-1226. https://doi.org/10.1016/j.jpain.2013.05.009
  82. Elsenbruch S, Schmid J, Kullmann JS, et al. Visceral sensitivity correlates with decreased regional gray matter volume in healthy volunteers: a voxel-based morphometry study. Pain 2014;155:244-249. https://doi.org/10.1016/j.pain.2013.09.027
  83. Orand A, Gupta A, Shih W, et al. Catecholaminergic gene polymorphisms are associated with GI symptoms and morphological brain changes in irritable bowel syndrome. PLoS One 2015;10:e0135910. https://doi.org/10.1371/journal.pone.0135910
  84. Labus JS, Van Horn JD, Gupta A, et al. Multivariate morphological brain signatures predict patients with chronic abdominal pain from healthy control subjects. Pain 2015;156:1545-1554. https://doi.org/10.1097/j.pain.0000000000000196
  85. Zeng F, Qin W, Yang Y, et al. Regional brain structural abnormality in meal-related functional dyspepsia patients: a voxel-based morphometry study. PLoS One 2013;8:e68383. https://doi.org/10.1371/journal.pone.0068383
  86. Liu P, Zeng F, Yang F, et al. Altered structural covariance of the striatum in functional dyspepsia patients. Neurogastroenterol Motil 2014;26:1144-1154. https://doi.org/10.1111/nmo.12372
  87. Nan J, Liu J, Mu J, et al. Anatomically related gray and white matter alterations in the brains of functional dyspepsia patients. Neurogastroenterol Motil 2015;27:856-864. https://doi.org/10.1111/nmo.12560
  88. Assaf Y, Pasternak O. Diffusion tensor imaging (DTI)-based white matter mapping in brain research: a review. J Mol Neurosci 2008;34:51-61. https://doi.org/10.1007/s12031-007-0029-0
  89. Behrens TE, Johansen-Berg H, Woolrich MW, et al. Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci 2003;6:750-757. https://doi.org/10.1038/nn1075
  90. Chen JY, Blankstein U, Diamant NE, Davis KD. White matter abnormalities in irritable bowel syndrome and relation to individual factors. Brain Res 2011;1392:121-131. https://doi.org/10.1016/j.brainres.2011.03.069
  91. Ellingson BM, Mayer E, Harris RJ, et al. Diffusion tensor imaging detects microstructural reorganization in the brain associated with chronic irritable bowel syndrome. Pain 2013;154:1528-1541. https://doi.org/10.1016/j.pain.2013.04.010
  92. Irimia A, Labus JS, Torgerson CM, Van Horn JD, Mayer EA. Altered viscerotopic cortical innervation in patients with irritable bowel syndrome. Neurogastroenterol Motil 2015;27:1075-1081. https://doi.org/10.1111/nmo.12586
  93. Fang J, Li S, Li M, et al. Altered white matter microstructure identified with tract-based spatial statistics in irritable bowel syndrome: a diffusion tensor imaging study. Brain Imaging Behav 2017;11:1110-1116. https://doi.org/10.1007/s11682-016-9573-y
  94. Nan J, Zhang L, Chen Q, et al. White matter microstructural similarity and diversity of functional constipation and constipation-predominant irritable bowel syndrome. J Neurogastroenterol Motil 2018;24:107-118. https://doi.org/10.5056/jnm17038
  95. Zhou G, Qin W, Zeng F, et al. White-matter microstructural changes in functional dyspepsia: a diffusion tensor imaging study. Am J Gastroenterol 2013;108:260-269. https://doi.org/10.1038/ajg.2012.405
  96. Niddam DM, Tsai SY, Lu CL, Ko CW, Hsieh JC. Reduced hippocampal glutamate-glutamine levels in irritable bowel syndrome: preliminary findings using magnetic resonance spectroscopy. Am J Gastroenterol 2011;106:1503-1511. https://doi.org/10.1038/ajg.2011.120
  97. Nakai A, Kumakura Y, Boivin M, et al. Sex differences of brain serotonin synthesis in patients with irritable bowel syndrome using alpha-[C11]methyl-L-tryptophan, positron emission tomography and statistical parametric mapping. Can J Gastroenterol 2003;17:191-196. https://doi.org/10.1155/2003/572127
  98. Nakai A, Diksic M, Kumakura Y, D'Souza D, Kersey K. The effects of the 5-HT3 antagonist, alosetron, on brain serotonin synthesis in patients with irritable bowel syndrome. Neurogastroenterol Motil 2005;17:212-221. https://doi.org/10.1111/j.1365-2982.2004.00615.x
  99. Mak ADP, Northoff G, Yeung DKW, et al. Increased glutamate in somatosensory cortex in functional dyspepsia. Sci Rep 2017;7:3926. https://doi.org/10.1038/s41598-017-04405-1
  100. Tominaga K, Tsumoto C, Ataka S, et al. Regional brain disorders of serotonin neurotransmission are associated with functional dyspepsia. Life Sci 2015;137:150-157. https://doi.org/10.1016/j.lfs.2015.07.023
  101. Ly HG, Ceccarini J, Weltens N, et al. Increased cerebral cannabinoid-1 receptor availability is a stable feature of functional dyspepsia: a [18F] MK-9470 PET study. Psychother Psychosom 2015;84:149-158. https://doi.org/10.1159/000375454
  102. Fregni F, Potvin K, DaSilva D, et al. Clinical effects and brain metabolic correlates in non-invasive cortical neuromodulation for visceral pain. Eur J Pain 2011;15:53-60. https://doi.org/10.1016/j.ejpain.2010.08.002
  103. Eisenstein M. Microbiome: bacterial broadband. Nature 2016;533:S104-S106. https://doi.org/10.1038/533S104a
  104. Hsiao EY, McBride SW, Hsien S, et al. Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 2013;155:1451-1463. https://doi.org/10.1016/j.cell.2013.11.024
  105. Sampson TR, Debelius JW, Thron T, et al. Gut microbiota regulate motor deficits and neuroinflammation in a model of parkinson's disease. Cell 2016;167:1469-1480, e12. https://doi.org/10.1016/j.cell.2016.11.018
  106. Park AJ, Collins J, Blennerhassett PA, et al. Altered colonic function and microbiota profile in a mouse model of chronic depression. Neurogastroenterol Motil 2013;25:733-e575. https://doi.org/10.1111/nmo.12153
  107. Goyal MS, Venkatesh S, Milbrandt J, Gordon JI, Raichle ME. Feeding the brain and nurturing the mind: linking nutrition and the gut microbiota to brain development. Proc Natl Acad Sci USA 2015;112:14105-14112. https://doi.org/10.1073/pnas.1511465112
  108. Sudo N, Chida Y, Aiba Y, et al. Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J Physiol 2004;558(Pt 1):263-275. https://doi.org/10.1113/jphysiol.2004.063388
  109. Dinan TG, Cryan JF, Stanton C. Gut microbes and brain development have black box connectivity. Biol Psychiatry 2018;83:97-99. https://doi.org/10.1016/j.biopsych.2017.11.005
  110. Mayer EA, Tillisch K, Gupta A. Gut/brain axis and the microbiota. J Clin Invest 2015;125:926-938. https://doi.org/10.1172/JCI76304
  111. Moloney RD, Johnson AC, O'Mahony SM, Dinan TG, Greenwood- Van Meerveld B, Cryan JF. Stress and the microbiota-gut-brain axis in visceral pain: relevance to irritable bowel syndrome. CNS Neurosci Ther 2016;22:102-117. https://doi.org/10.1111/cns.12490
  112. Tillisch K, Labus J, Kilpatrick L, et al. Consumption of fermented milk product with probiotic modulates brain activity. Gastroenterology 2013;144:1394-1401, e1-e4. https://doi.org/10.1053/j.gastro.2013.02.043
  113. Tillisch K, Mayer EA, Gupta A, et al. Brain structure and response to emotional stimuli as related to gut microbial profiles in healthy women. Psychosom Med 2017;79:905-913. https://doi.org/10.1097/PSY.0000000000000493
  114. Pinto-Sanchez MI, Hall GB, Ghajar K, et al. Probiotic bifidobacterium longum NCC3001 reduces depression scores and alters brain activity: a pilot study in patients with irritable bowel syndrome. Gastroenterology 2017;153:448-459, e8. https://doi.org/10.1053/j.gastro.2017.05.003
  115. Labus JS, Hollister EB, Jacobs J, et al. Differences in gut microbial composition correlate with regional brain volumes in irritable bowel syndrome. Microbiome 2017;5:49. https://doi.org/10.1186/s40168-017-0260-z
  116. Frost G, Sleeth ML, Sahuri-Arisoylu M, et al. The short-chain fatty acid acetate reduces appetite via a central homeostatic mechanism. Nat Commun 2014;5:3611. https://doi.org/10.1038/ncomms4611
  117. Byrne CS, Chambers ES, Alhabeeb H, et al. Increased colonic propionate reduces anticipatory reward responses in the human striatum to high-energy foods. Am J Clin Nutr 2016;104:5-14. https://doi.org/10.3945/ajcn.115.126706
  118. Zanchi D, Meyer-Gerspach AC, Suenderhauf C, et al. Differential effects of L-tryptophan and L-leucine administration on brain resting state functional networks and plasma hormone levels. Sci Rep 2016;6:35727. https://doi.org/10.1038/srep35727
  119. Smith SM, Nichols TE. Statistical challenges in "big data" human neuroimaging. Neuron 2018;97:263-268. https://doi.org/10.1016/j.neuron.2017.12.018
  120. Labus JS, Mayer EA, Jarcho J, et al. Acute tryptophan depletion alters the effective connectivity of emotional arousal circuitry during visceral stimuli in healthy women. Gut 2011;60:1196-1203. https://doi.org/10.1136/gut.2010.213447

Cited by

  1. Parasympathetic activity correlates with subjective and brain responses to rectal distension in healthy subjects but not in non-constipated patients with irritable bowel syndrome vol.9, pp.None, 2019, https://doi.org/10.1038/s41598-019-43455-5
  2. Crosstalk Between the Gut Microbiota and the Brain: An Update on Neuroimaging Findings vol.10, pp.None, 2018, https://doi.org/10.3389/fneur.2019.00883
  3. Effect and cerebral mechanism of acupuncture treatment for functional constipation: study protocol for a randomized controlled clinical trial vol.20, pp.None, 2019, https://doi.org/10.1186/s13063-019-3410-8
  4. From Biological Rhythms to the Default Mode Network: What Lies beneath the Tip of the Iceberg of Mind? vol.9, pp.4, 2018, https://doi.org/10.4236/wjns.2019.94020
  5. Imaging Brain Mechanisms of Functional Somatic Syndromes: Potential as a Biomarker? vol.250, pp.3, 2018, https://doi.org/10.1620/tjem.250.137
  6. Effects and mechanisms of acupuncture and electroacupuncture for functional dyspepsia: A systematic review vol.26, pp.19, 2018, https://doi.org/10.3748/wjg.v26.i19.2439
  7. Similarity and diversity of spontaneous brain activity in functional dyspepsia subtypes vol.61, pp.7, 2020, https://doi.org/10.1177/0284185119883391
  8. Functional Dyspepsia: Diagnostic and Therapeutic Approaches vol.80, pp.13, 2020, https://doi.org/10.1007/s40265-020-01362-4
  9. The effects of gastrointestinal symptoms on structural grey matter volume in youth vol.80, pp.6, 2018, https://doi.org/10.1002/jdn.10044
  10. Resting state functional connectivity of the pain matrix and default mode network in irritable bowel syndrome: a graph theoretical analysis vol.10, pp.None, 2018, https://doi.org/10.1038/s41598-020-67048-9
  11. Evaluation of the short-term efficacy of local analgesic (lidocaine) and opioid analgesic (sufentanil) on patients with centrally mediated abdominal pain syndrome: a randomized controlled trial vol.14, pp.None, 2018, https://doi.org/10.1177/17562848211021783
  12. Altered Brain Structure in Chronic Visceral Pain: Specific Differences in Gray Matter Volume and Associations With Visceral Symptoms and Chronic Stress vol.12, pp.None, 2021, https://doi.org/10.3389/fneur.2021.733035
  13. Altered Functional Connectivity Within and Between Salience and Sensorimotor Networks in Patients With Functional Constipation vol.15, pp.None, 2018, https://doi.org/10.3389/fnins.2021.628880
  14. Disrupted Regional Homogeneity in Major Depressive Disorder With Gastrointestinal Symptoms at Rest vol.12, pp.None, 2018, https://doi.org/10.3389/fpsyt.2021.636820
  15. The Microbiota-Gut-Brain Axis: From Motility to Mood vol.160, pp.5, 2018, https://doi.org/10.1053/j.gastro.2020.10.066
  16. Global research trends in the microbiome related to irritable bowel syndrome: A bibliometric and visualized study vol.27, pp.13, 2021, https://doi.org/10.3748/wjg.v27.i13.1341
  17. High Frequency of Concomitant Bladder, Bowel, and Sexual Symptoms in Huntington’s Disease: A Self-Reported Questionnaire Study vol.11, pp.8, 2021, https://doi.org/10.3390/jpm11080714
  18. Neuroinflammatory remodeling of the anterior cingulate cortex as a key driver of mood disorders in gastrointestinal disease and disorders vol.133, pp.None, 2018, https://doi.org/10.1016/j.neubiorev.2021.12.020
  19. Microbiota links to neural dynamics supporting threat processing vol.43, pp.2, 2022, https://doi.org/10.1002/hbm.25682