Absence of increasing cortical fMRI activity volume in response to increasing visceral stimulation in IBS patients.

Cerebral cortical activity associated with perceived visceral sensation represents registration of afferent transduction and cognitive processes related to perception. Abnormalities of gut sensory function can involve either or both of these processes. Cortical registration of subliminal viscerosensory signals represents cerebral cortical activity induced by stimulation of intestinal sensory neurocircuitry without the influence of perception-related cortical activity, whereas those associated with perception represent both neural circuitry and cognitive processes. Our aims were to determine and compare quantitatively cerebral cortical functional magnetic resonance imaging (fMRI) activity in response to subliminal, liminal, and nonpainful supraliminal rectal distension between a group of irritable bowel syndrome (IBS) patients and age/gender-matched controls. Eight female IBS patients and eight age-matched healthy female control subjects were studied using brain fMRI techniques. Three barostat-controlled distension levels were tested: 1) 10 mmHg below perception (subliminal), 2) at perception (liminal), and 3) 10 mmHg above perception (supraliminal). In control subjects, there was a direct relationship between stimulus intensity and cortical activity volumes, ie., the volume of fMRI cortical activity in response to subliminal (3,226 +/- 335 microl), liminal (5,751 +/- 396 microl), and supraliminal nonpainful stimulation (8,246 +/- 624 microl) were significantly different (P < 0.05). In contrast, in IBS patients this relationship was absent and fMRI activity volumes for subliminal (2,985 +/- 332 microl), liminal (2,457 +/- 342 microl), and supraliminal nonpainful stimulation (2,493 +/- 351 microl) were similar. Additional recruitment of cortical fMRI activity volume in response to increasing stimulation from subliminal to liminal and supraliminal domains is absent in IBS patients, suggesting a difference in the processing of perceived stimulation compared with controls.

[1]  K. Forster,et al.  REPETITION PRIMING AND FREQUENCY ATTENUATION IN LEXICAL ACCESS , 1984 .

[2]  M. Farthing,et al.  Selective affective biasing in recognition memory in the irritable bowel syndrome. , 1993, Gut.

[3]  A. K. Jones,et al.  Cerebral responses to a continual tonic pain stimulus measured using positron emission tomography , 1998, Pain.

[4]  M. Bushnell,et al.  Pain perception: is there a role for primary somatosensory cortex? , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[5]  M. Bushnell,et al.  Cortical representation of the sensory dimension of pain. , 2001, Journal of neurophysiology.

[6]  R. Leiguarda,et al.  Asymbolia for pain: A sensory‐limbic disconnection syndrome , 1988, Annals of neurology.

[7]  P. Merikle,et al.  Perception without awareness. Critical issues. , 1992, The American psychologist.

[8]  J. Mcghee,et al.  T helper type-2 cells induce ileal villus atrophy, goblet cell metaplasia, and wasting disease in T cell-deficient mice. , 2003, Gastroenterology.

[9]  A Sundin,et al.  Identification of human brain loci processing esophageal sensation using positron emission tomography. , 1997, Gastroenterology.

[10]  R. Cox,et al.  Identification and characterization of cerebral cortical response to esophageal mucosal acid exposure and distention. , 1998, Gastroenterology.

[11]  D. Drossman,et al.  Selective recall of gastrointestinal-sensation words : Evidence for a cognitive-behavioral contribution to irritable bowel syndrome , 2001 .

[12]  A Jesmanowicz,et al.  Swallow-related cerebral cortical activity maps are not specific to deglutition. , 2001, American journal of physiology. Gastrointestinal and liver physiology.

[13]  I. Tracey,et al.  Cortical Processing of Human Somatic and Visceral Sensation , 1999, The Journal of Neuroscience.

[14]  R. Kessler,et al.  Regional cerebral activation in irritable bowel syndrome and control subjects with painful and nonpainful rectal distention. , 2000, Gastroenterology.

[15]  M. L. Wood,et al.  Functional MRI of pain- and attention-related activations in the human cingulate cortex. , 1997, Journal of neurophysiology.

[16]  Meuwissen,et al.  Rectal visceral sensitivity in healthy volunteers: influences of gender, age and methods , 2000, Neurogastroenterology and motility : the official journal of the European Gastrointestinal Motility Society.

[17]  Lagier,et al.  Influence of age on rectal tone and sensitivity to distension in healthy subjects , 1999, Neurogastroenterology and motility : the official journal of the European Gastrointestinal Motility Society.

[18]  G. Curio,et al.  Imperceptible Stimuli and Sensory Processing Impediment , 2003, Science.

[19]  E A Mayer,et al.  Altered rectal perception is a biological marker of patients with irritable bowel syndrome. , 1995, Gastroenterology.

[20]  E A Mayer,et al.  Regional cerebral activity in normal and pathological perception of visceral pain. , 1997, Gastroenterology.

[21]  R. Shaker,et al.  Cerebral cortical registration of subliminal visceral stimulation. , 2002, Gastroenterology.

[22]  J. Le Bas,et al.  Central processing of rectal pain: a functional MR imaging study. , 1999, AJNR. American journal of neuroradiology.

[23]  G. Gebhart,et al.  Mechanosensitive properties of pelvic nerve afferent fibers innervating the urinary bladder of the rat. , 1994, Journal of neurophysiology.

[24]  R. J. Seitz,et al.  Somatic and limbic cortex activation in esophageal distention: A functional imaging study , 1998, Annals of neurology.

[25]  H. Fields,et al.  Pain: Mechanisms and Management , 1989 .

[26]  E A Mayer,et al.  Repetitive sigmoid stimulation induces rectal hyperalgesia in patients with irritable bowel syndrome. , 1997, Gastroenterology.

[27]  R P Lesser,et al.  Painful stimuli evoke potentials recorded over the human anterior cingulate gyrus. , 1998, Journal of neurophysiology.

[28]  B. Vogt,et al.  Pain Processing in Four Regions of Human Cingulate Cortex Localized with Co‐registered PET and MR Imaging , 1996, The European journal of neuroscience.

[29]  N. Read,et al.  Irritable bowel syndrome: differences between patients who show rectal sensitivity and those who do not , 1993 .

[30]  D. Drossman,et al.  What determines severity among patients with painful functional bowel disorders , 2000 .

[31]  Apkar Apkarian,et al.  Thalamocortical connections of the cingulate and insula in relation to nociceptive inputs to the cortex , 1998 .

[32]  E. Carmichael,et al.  SOME SENSORY SYNDROMES IN CHILDREN: INDIFFERENCE TO PAIN AND SENSORY NEUROPATHY , 1959, Journal of neurology, neurosurgery, and psychiatry.

[33]  J. Ritchie Pain from distension of the pelvic colon by inflating a balloon in the irritable colon syndrome 1 , 1973, Gut.

[34]  B. Vogt,et al.  Pain and Stroop interference tasks activate separate processing modules in anterior cingulate cortex , 1998, Experimental Brain Research.

[35]  A. Page,et al.  An in vitro study of the properties of vagal afferent fibres innervating the ferret oesophagus and stomach , 1998, The Journal of physiology.

[36]  Pavel Jurák,et al.  Intracerebral event-related potentials to subthreshold target stimuli , 2001, Clinical Neurophysiology.

[37]  E. G. Jones,et al.  Chemically distinct compartments of the thalamic VPM nucleus in monkeys relay principal and spinal trigeminal pathways to different layers of the somatosensory cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  Alan C. Evans,et al.  Functional imaging of an illusion of pain , 1996, Nature.

[39]  W. Whitehead,et al.  Is rectal pain sensitivity a biological marker for irritable bowel syndrome: psychological influences on pain perception. , 1998, Gastroenterology.

[40]  Alan C. Evans,et al.  Distributed processing of pain and vibration by the human brain , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[41]  G. Nicholas Verne,et al.  Hypersensitivity to visceral and cutaneous pain in the irritable bowel syndrome , 2001, Pain.

[42]  S. Dehaene,et al.  Imaging unconscious semantic priming , 1998, Nature.

[43]  A Schnitzler,et al.  Somatic and limbic cortex activation in esophageal distention: a functional magnetic resonance imaging study. , 1998, Annals of neurology.

[44]  A. Marcel Conscious and unconscious perception: Experiments on visual masking and word recognition , 1983, Cognitive Psychology.

[45]  R. Peyron,et al.  Functional imaging of brain responses to pain. A review and meta-analysis (2000) , 2000, Neurophysiologie Clinique/Clinical Neurophysiology.

[46]  L. Chang,et al.  Perceptual responses in patients with inflammatory and functional bowel disease , 2000, Gut.

[47]  E A Mayer,et al.  Basic and clinical aspects of visceral hyperalgesia. , 1994, Gastroenterology.

[48]  Anthony K. P. Jones,et al.  Pain processing during three levels of noxious stimulation produces differential patterns of central activity , 1997, Pain.

[49]  T. Shi,et al.  Morphology of thalamocortical neurons projecting to the primary somatosensory cortex and their relationship to spinothalamic terminals in the squirrel monkey , 1995, The Journal of comparative neurology.

[50]  A. Schnitzler,et al.  Functional Neuroimaging of Visceral Sensation , 2000, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.