Functional Neuroimaging of Visceral Sensation

Summary The use of functional brain imaging techniques has led to considerable advances in our understanding of brain processing of human visceral sensation. The use of complementary techniques such as functional MRI, positron emission tomography, magnetoencephalography, and EEG has led to the identification of a network of brain areas that process visceral sensation. These studies suggest that unlike somatic sensation, which has an intense homuncular representation in the primary somatosensory cortex (SI), visceral sensation is primarily represented in the secondary somatosensory cortex, whereas representation in SI is vague. This difference could account for the poor localization of visceral sensation in comparison with somatic sensation. However, in a manner similar to that of somatic sensation, visceral sensation is represented in the paralimbic and limbic structures such as the insular, anterior cingulate, and prefrontal cortices. These areas are likely to mediate the affective and cognitive components of visceral sensation. Recent studies suggest that negative emotional factors such as fear, and cognitive factors such as attention can modulate the brain processing of visceral sensation in the insular and anterior cingulate cortices. In addition, alterations in the pattern of cortical processing of visceral sensation have been described in patients with functional gastrointestinal pain. It is likely that future research into the factors that modulate the brain processing of visceral sensation in health and disease are likely to improve further our understanding of the pathophysiology of functional visceral pain disorders.

[1]  William Beaumont,et al.  Experiments and Observations on the Gastric Juice, and the Physiology of Digestion , 1834, The Medico-chirurgical review.

[2]  I. Pavlov,et al.  The Work of the Digestive Glands , 1903, Bristol Medico-Chirurgical Journal (1883).

[3]  M. Washburn,et al.  Bodily Changes in Pain, Hunger, Fear, and Rage. , 1917 .

[4]  A. L. Bloomfield,et al.  EXPERIMENTAL REFERRED PAIN FROM THE GASTRO-INTESTINAL TRACT. PART I. THE ESOPHAGUS. , 1931, The Journal of clinical investigation.

[5]  E. A. Linell Human Gastric Function. An Experimental Study of a Man and His Stomach , 1944 .

[6]  Z. Sery [Anatomy and physiology of the esophagus]. , 1962, Ceskoslovenska otolaryngologie.

[7]  A. Paintal Vagal afferent fibres , 1962, Ergebnisse der Physiologie, biologischen Chemie und experimentellen Pharmakologie.

[8]  B. Fleshler,et al.  Physiology of the Gastrointestinal Tract , 1969 .

[9]  Letter: Comparative anatomy of the esophagus. , 1974, Gastroenterology.

[10]  Comparative Anatomy of the Esophagus , 1974 .

[11]  R. Norgren Projections from the nucleus of the solitary tract in the rat , 1978, Neuroscience.

[12]  A I Basbaum,et al.  Differential origins of spinothalamic tract projections to medial and lateral thalamus in the rat , 1979, The Journal of comparative neurology.

[13]  P. Sawchenko Central connections of the sensory and motor nuclei of the vagus nerve. , 1983, Journal of the autonomic nervous system.

[14]  J. Christensen Origin of sensation in the esophagus. , 1984, The American journal of physiology.

[15]  R. Blair,et al.  Viscerosomatic convergence onto T2–T4 spinoreticular, spinoreticular-spinothalamic, and spinothalamic tract neurons in the cat , 1984, Experimental Neurology.

[16]  F. Cerveró,et al.  Somatic and visceral primary afferents in the lower thoracic dorsal root ganglia of the cat , 1984, The Journal of comparative neurology.

[17]  W. Ammons,et al.  T2-T5 spinothalamic neurons projecting to medial thalamus with viscerosomatic input. , 1985, Journal of neurophysiology.

[18]  F. Cerveró Visceral nociception: peripheral and central aspects of visceral nociceptive systems. , 1985, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[19]  W. C. Groat Spinal cord projections and neuropeptides in visceral afferent neurons. , 1986 .

[20]  J. Morrison,et al.  Functional properties of spinal visceral afferents supplying abdominal and pelvic organs, with special emphasis on visceral nociception. , 1986, Progress in brain research.

[21]  P. Andrews Vagal afferent innervation of the gastrointestinal tract. , 1986, Progress in brain research.

[22]  Andrew C. N. Chen,et al.  Human pain responsivity in a tonic pain model: Psychological determinants , 1989, Pain.

[23]  D. Hopkins,et al.  Viscerotopic representation of the upper alimentary tract in the rat: Sensory ganglia and nuclei of the solitary and spinal trigeminal tracts , 1989, The Journal of comparative neurology.

[24]  W. Whitehead Effects of Psychological Factors on Gastrointestinal Function , 1989 .

[25]  T. Ness,et al.  Visceral pain: a review of experimental studies , 1990, Pain.

[26]  R. Goyal,et al.  Stimulus-response function studies of esophageal mechanosensitive nociceptors in sympathetic afferents of opossum. , 1990, Journal of neurophysiology.

[27]  E. Mayer,et al.  Role of visceral afferent mechanisms in functional bowel disorders. , 1990, Gastroenterology.

[28]  Agonist-specific modulation of intracellular calcium in colonic myocytes by neurokinins and carbachol , 1990 .

[29]  C. Dalton,et al.  Cerebral potentials evoked by oesophageal distension in patients with non-cardiac chest pain. , 1992, Gut.

[30]  A. Apkarian,et al.  Squirrel monkey lateral thalamus. II. Viscerosomatic convergent representation of urinary bladder, colon, and esophagus , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[32]  C. Woolf An overview of the mechanisms of hyperalgesia. , 1995, Pulmonary pharmacology.

[33]  P. Furlong,et al.  Topographic mapping of cortical potentials evoked by distension of the human proximal and distal oesophagus. , 1995, Electroencephalography and clinical neurophysiology.

[34]  J. R. Augustine Circuitry and functional aspects of the insular lobe in primates including humans , 1996, Brain Research Reviews.

[35]  W. Willis,et al.  Visceral nociceptive input into the ventral posterolateral nucleus of the thalamus: a new function for the dorsal column pathway. , 1996, Journal of neurophysiology.

[36]  R. Dolan,et al.  The role of the prefrontal cortex in higher cognitive functions. , 1996, Brain research. Cognitive brain research.

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

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

[39]  N. Talley Scope of the problem of functional digestive disorders. , 2003, The European journal of surgery. Supplement. : = Acta chirurgica. Supplement.

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

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

[42]  K. D. Singh,et al.  Cortical localisation of magnetic fields evoked by oesophageal distension. , 1998, Electroencephalography and clinical neurophysiology.

[43]  D. Thompson,et al.  Brain-gut axis in health and disease. , 1998, Gastroenterology.

[44]  M. Weisenberg,et al.  The influence of film-induced mood on pain perception , 1998, Pain.

[45]  Shine,et al.  Cognitive evoked potentials to anticipated oesophageal stimulus in humans: quantitative assessment of the cognitive aspects of visceral perception , 1999, Neurogastroenterology and motility : the official journal of the European Gastrointestinal Motility Society.

[46]  A Schnitzler,et al.  Different cortical organization of visceral and somatic sensation in humans , 1999, The European journal of neuroscience.

[47]  N. Costes,et al.  Haemodynamic brain responses to acute pain in humans: sensory and attentional networks. , 1999, Brain : a journal of neurology.

[48]  Frieling,et al.  Cortical activation during oesophageal stimulation: a neuromagnetic study , 1999, Neurogastroenterology and motility : the official journal of the European Gastrointestinal Motility Society.

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

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

[51]  A. Hobson,et al.  Contribution of central sensitisation to the development of noncardiac chest pain , 2000, The Lancet.

[52]  Modulation of the brain processing of human oesophageal sensation by emotions: A functional magnetic resonance imaging study , 2000 .