Evidence for alterations in central noradrenergic signaling in irritable bowel syndrome

NeuroImage

Volumn 63, Issue 4, 2012, Pages 1854-1863

  Berman, Steven ^a   Suyenobu, Brandall ^a   Naliboff, Bruce D ^a   Bueller, Joshua ^a   Stains, Jean ^a   Wong, Heng ^b   Mandelkern, Mark ^c,d   Fitzgerald, Leah ^e   Ohning, Gordon ^d   Gupta, Arpana ^a   Labus, Jennifer S ^a   Tillisch, Kirsten ^a   Mayer, Emeran A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d VAGLA Health Care Center   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

2 Adrenergic receptors; Corticolimbic inhibition; Early life trauma; Yohimbine

Indexed keywords

ALPHA ADRENERGIC RECEPTOR; CLONIDINE; FLUORODEOXYGLUCOSE F 18; NORADRENALIN; PLACEBO; YOHIMBINE;

ADULT; AMYGDALOID NUCLEUS; ANTERIOR CINGULATE; ARTICLE; BRAIN FUNCTION; BRAIN MAPPING; BRAIN STEM; CINGULATE GYRUS; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GLUCOSE METABOLISM; HUMAN; IRRITABLE COLON; LIMBIC SYSTEM; MALE; NORADRENALIN BLOOD LEVEL; NORADRENERGIC SYSTEM; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; SIGNAL TRANSDUCTION;

ADULT; ANXIETY; AROUSAL; BRAIN; CENTRAL NERVOUS SYSTEM; FATIGUE; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; IRRITABLE BOWEL SYNDROME; MALE; MIDDLE AGED; NERVE NET; NOREPINEPHRINE; POSITRON-EMISSION TOMOGRAPHY; PSYCHOMOTOR PERFORMANCE; QUESTIONNAIRES; RECEPTORS, ADRENERGIC, ALPHA-2; SYMPATHETIC NERVOUS SYSTEM; SYMPATHOLYTICS; WOUNDS AND INJURIES; YOHIMBINE; YOUNG ADULT;

EID: 84866891750     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2012.08.028     Document Type: Article

References (65)

1. Adeyemi E.O., Desai K.D., Towsey M., Ghista D. Characterization of autonomic dysfunction in patients with irritable bowel syndrome by means of heart rate variability studies. Am. J. Gastroenterol. 1999, 94:816-823.
2. Aggarwal A., Cutts T.F., Abell T.L., Cardoso S., Familoni B., Bremer J., Karas J. Predominant symptoms in irritable bowel syndrome correlate with specific autonomic nervous system abnormalities. Gastroenterology 1994, 106:945-950.
3. Al-Chaer E.D., Weaver S.A. Early life trauma and chronic pain. Functional Pain Syndromes: Presentation and Pathophysiology 2009, 423-452. IASP Press, Seattle. E.A. Mayer, M.C. Bushnell (Eds.).
4. Arnsten A.F.T., Goldmanrakic P.S. Selective prefrontal cortical projections to the region of the locus coeruleus and raphe nuclei in the rhesus-monkey. Brain Res. 1984, 106:9-18.
5. Berman S.M., Chang L., Suyenobu B., Derbyshire S.W., Stains J., FitzGerald L., Mandelkern M., Hamm L., Vogt B., Naliboff B.D., Mayer E.A. Condition-specific deactivation of brain regions by 5-HT3 receptor antagonist alosetron. Gastroenterology 2002, 123:969-977.
6. Berman S.M., Naliboff B.D., Chang L., FitzGerald L., Antolin T., Camplone A., Mayer E.A. Enhanced preattentive central nervous system reactivity in irritable bowel syndrome. Am. J. Gastroenterol. 2002, 97:2791-2797.
7. Berman S., Suyenobu B., Naliboff B.D., Bueller J., Stains J., Wong H., Mandelkern M., Mayer E.A. Differential noradrenergic (NE) modulation of brain metabolic and electrical activity in IBS patients and healthy controls. Gastroenterology 2007, 132(A-726).
8. Berman S.M., Naliboff B.D., Suyenobu B., Labus J.S., Stains J., Ohning G., Kilpatrick L., Bueller J.A., Ruby K., Jarcho J., Mayer E.A. 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.
9. Bijlsma E.Y., de Jongh R., Olivier B., Groenink L. Fear-potentiated startle, but not light-enhanced startle, is enhanced by anxiogenic drugs. Pharmacol. Biochem. Behav. 2010, 96:24-31.
10. Bremner J.D., Krystal J.H., Southwick S.M., Charney D.S. Noradrenergic mechanisms in stress and anxiety: I. Preclinical studies. Synapse 1996, 23:28-38.
11. Bremner J.D., Krystal J.H., Southwick S.M., Charney D.S. Noradrenergic mechanisms in stress and anxiety: II. Clinical studies. Synapse 1996, 23:39-51.
12. Bremner J.D., Innis R.B., Ng C.K., Staib L.H., Salomon R.M., Bronen R.A., Duncan J., Southwick S.M., Krystal J.H., Rich D., Zubal G., Dey H., Soufer R., Charney S.D. Positron emission tomography measurement of cerebral metabolic correlates of yohimbine administration in combat related posttraumatic stress disorder. Arch. Gen. Psychiatry 1997, 54:246-254.
13. Bremner J.D., Bolus R., Mayer E.A. Psychometric properties of the Early Trauma Inventory-Self Report. J. Nerv. Ment. Dis. 2007, 195:211-218.
14. Caldji C., Diorio J., Meaney M.J. Variations in maternal care in infancy regulate the development of stress reactivity. Biol. Psychiatry 2000, 48:1164-1174.
15. Camilleri M., Kim D.Y., McKinzie S., Kim H.J., Thomforde G.M., Burton D.D., Low P.A., Zinsmeister A.R. A randomized, controlled exploratory study of clonidine in diarrhea-predominant irritable bowel syndrome. Clin. Gastroenterol. Hepatol. 2003, 1:111-121.
16. Chang L., Mayer E.A., Johnson T., FitzGerald L., Naliboff B. Differences in somatic perception in female patients with irritable bowel syndrome with and without fibromyalgia. Pain 2000, 84:297-307.
17. Chang L., Munakata J., Mayer E.A., Schmulson M.J., Johnson T.D., Bernstein C.N., Saba L., Naliboff B., Anton P.A., Matin K. Perceptual responses in patients with inflammatory and functional bowel disease. Gut 2000, 47:497-505.
18. Coan J.A., Allen J.J. Frontal EEG asymmetry as a moderator and mediator of emotion. Biol. Psychol. 2004, 67:7-49.
19. Coull J.T., Buchel C., Friston K.J., Frith C.D. Noradrenergically mediated plasticity in a human attentional neuronal network. NeuroImage 2000, 11. (822-822).
20. Cullen T.J., Walker M.A., Eastwood S.L., Esiri M.M., Harrison P.J., Crow T.J. Anomalies of asymmetry of pyramidal cell density and structure in dorsolateral prefrontal cortex in schizophrenia. Br. J. Psychiatry 2006, 188:26-31.
21. Czeh B., Perez-Cruz C., Fuchs E., Flugge G. Chronic stress-induced cellular changes in the medial prefrontal cortex and their potential clinical implications: does hemisphere location matter?. Behav. Brain Res. 2008, 190:1-13.
22. Davidson R.J. Anxiety and affective style: role of prefrontal cortex and amygdala. Biol. Psychiatry 2002, 51:68-80.
23. Dickhaus B., Mayer E.A., Firooz N., Stains J., Conde F., Olivas T.I., Fass R., Chang L., Mayer M., Naliboff B.D. Irritable bowel syndrome patients show enhanced modulation of visceral perception by auditory stress. Am. J. Gastroenterol. 2003, 98:135-143.
24. Dinan T.G., Barry S., Ahkion S., Chua A., Keeling P.W. Assessment of central noradrenergic functioning in irritable bowel syndrome using a neuroendocrine challenge test. J. Psychosom. Res. 1990, 34:575-580.
25. Eysenck H.J., Eysenck S.B.G. Manual of the Eysenck Personality Questionnaire: (EPQ-R Adult) Comprising the EPQ-Revised (EPQ-R) and EPQ-R Short Scale 1994, Educational and Industrial Testing Service, San Diego.
26. Farhadi A., Bruninga K., Fields J., Keshavarzian A. Irritable bowel syndrome: an update on therapeutic modalities. Expert Opin. Invest. Drugs 2001, 10:1211-1222.
27. Fluegge G., van Kampen M., Mijnster M.J. Perturbations in brain monomamine systems during stress. Cell Tissue Res. 2003, 315:1-14.
28. Flugge G., van Kampen M., Meyer H., Fuchs E. Alpha2A and alpha2C-adrenoceptor regulation in the brain: alpha2A changes persist after chronic stress. Eur. J. Neurosci. 2003, 17:917-928.
29. Heitkemper M., Jarrett M., Cain K., Shaver J., Bond E., Woods N.F., Walker E. Increased urine catecholamines and cortisol in women with irritable bowel syndrome. Am. J. Gastroenterol. 1996, 91:906-913.
30. Hubbard C.S., Labus J.S., Bueller J., Stains J., Suyenobu B., Dukes G.E., Kelleher D.L., Tillisch K., Naliboff B.D., Mayer E.A. Corticotropin-releasing factor receptor 1 antagonist alters regional activation and effective connectivity in an -emotional-arousal circuit during expectation of abdominal pain. J. Neurosci. 2011, 31:12491-12500.
31. Johnstone T., van Reekum C.M., Urry H.L., Kalin N.H., Davidson R.J. Failure to regulate: counterproductive recruitment of top-down prefrontal-subcortical circuitry in major depression. J. Neurosci. 2007, 27:8877-8884.
32. Kennedy P.J., Clarke G., Quigley E.M.M., Groeger J.A., Dinan T.G., Cryan J.F. Gut memories: towards a cognitive neurobiology of irritable bowel syndrome. Neurosci. Biobehav. Rev. 2012, 36:310-340.
33. Kilpatrick L.A., Labus J.S., Coveleskie K., Hammer C., Rappold G., Tillisch K., Bueller J.A., Suyenobu B., Jarcho J.M., McRoberts J.A., Niesler B., Mayer E.A. The HTR3A polymorphism c. -42C>T is associated with amygdala responsiveness in patients with irritable bowel syndrome. Gastroenterology 2011, 140:1943-1951.
34. Koob G.F. Corticotropin-releasing factor, norepinephrine, and stress. Biol. Psychiatry 1999, 46:1167-1180.
35. Labus J., Bolus R., Chang L., Wiklund I., Naesdal J., Mayer E., Naliboff B. The visceral sensitivity index: development and validation of a gastrointestinal symptom-specific anxiety scale. Aliment. Pharmacol. Ther. 2004, 20:89-97.
36. Labus J.S., Mayer E.A., Chang L., Bolus R., Naliboff B.D. The central role of gastrointestinal-specific anxiety in irritable bowel syndrome: further validation of the Visceral Sensitivity Index. Psychosom. Med. 2007, 69:89-98.
37. Labus J.S., Mayer E.A., Hamaguchi T., Mizuno T., Kano M., Fukudo S. 5-Httlpr gene polymorphism modulates activity and connectivity within an emotional arousal network of healthy control subjects during visceral pain. Gastroenterology 2008, 134(A-121).
38. Labus J.S., Naliboff B.N., Fallon J., Berman S.M., Suyenobu B., Bueller J.A., Mandelkern M., Mayer E.A. 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.
39. Labus J.S., Mayer E.A., Jarcho J., Kilpatrick L.A., Kilkens T.O., Evers E.A., Backes W.H., Brummer R.J., van Nieuwenhoven M.A. Acute tryptophan depletion alters the effective connectivity of emotional arousal circuitry during visceral stimuli in healthy women. Gut 2011, 60:1196-1203.
40. Ladd C.O., Huot R.L., Thrivikraman K.V., Nemeroff C.B., Meaney M.J., Plotsky P., Mayer E.A., Saper C.B. Long-term Behavioral and Neuroendocrine Adaptations to Adverse Early Experience. The Biological Basis for Mind Body Interactions 2000, 81-103. Elsevier, Amsterdam.
41. Lim E.P., Tan C.H., Jay T.M., Dawe G.S. Locus coeruleus stimulation and noradrenergic modulation of hippocampo-prefrontal cortex long-term potentiation. Int. J. Neuropsychopharmacol. 2010, 13:1219-1231.
42. Longstreth G.F., Thompson W.G., Chey W.D., Houghton L.A., Mearin F., Spiller R.C. Functional bowel disorders. Gastroenterology 2006, 130:1480-1491.
43. Martinez V., Taché Y. CRF1 receptors as a therapeutic target for irritable bowel syndrome. Curr. Pharm. Des. 2006, 12:4071-4088.
44. Mayer E.A., Bushnell M.C. Functional pain disorders: time for a paradigm shift?. Functional Pain Syndromes: Presentation and Pathophysiology 2009, 531-565. IASP Press, Seattle. E.A. Mayer, M.C. Bushnell (Eds.).
45. McNaughton N., Corr P.J. A two-dimensional neuropsychology of defense: fear/anxiety and defensive distance. Neurosci. Biobehav. Rev. 2004, 28:285-305.
46. Meaney M.J. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu. Rev. Neurosci. 2001, 24:1161-1192.
47. Meyerbroeker K., Powers M.B., van Stegeren A., Emmelkamp P.M.G. Does yohimbine hydrochloride facilitate fear extinction in virtual reality treatment of fear of flying? A randomized placebo-controlled trial. Psychother. Psychosom. 2012, 81:29-37.
48. Munakata J., Naliboff B., Harraf F., Kodner A., Lembo T., Chang L., Silverman D.H., Mayer E.A. Repetitive sigmoid stimulation induces rectal hyperalgesia in patients with irritable bowel syndrome. Gastroenterology 1997, 112:55-63.
49. Naliboff B.N.R.J.L. Anxiety in functional pain disorders. Functional Pain Syndromes: Presentation and Pathophysiology 2009, 185-214. IASP Press, Seattle. E.A. Mayer, D.M. Bushnell (Eds.).
50. Naliboff B.D., Benton D., Solomon G.F., Morley J.E., Fahey J.L., Bloom E.T., Makinodan T., Gilmore S.L. Immunological changes in young and old adults during brief laboratory stress. Psychosom. Med. 1991, 53:121-132.
51. Naliboff B.D., Munakata J., Fullerton S., Gracely R.H., Kodner A., Harraf F., Mayer E.A. Evidence for two distinct perceptual alterations in irritable bowel syndrome. Gut 1997, 41:505-512.
52. Park M.I., Camilleri M. Genetics and genotypes in irritable bowel syndrome: implications for diagnosis and treatment. Gastroenterol. Clin. N. Am. 2005, 34:305-317.
53. Pezawas L., Meyer-Lindenberg A., Drabant E.M., Verchinski B.A., Munoz K.E., Kolachana B.S., Egan M.F., Mattay V.S., Hariri A.R., Weinberger D.R. 5-HTTLPR polymorphism impacts human cingulate-amygdala interactions: a genetic susceptibility mechanism for depression. Nat. Neurosci. 2005, 8:828-834.
54. Ramos B.P., Arnsten A.F.T. Adrenergic pharmacology and cognition: focus on the prefrontal cortex. Pharmacol. Ther. 2007, 113:523-536.
55. Soeter M., Kindt M. Noradrenergic enhancement of associative fear memory in humans. Neurobiol. Learn. Mem. 2011, 96:263-271.
56. Soeter M., Kindt M. Stimulation of the noradrenergic system during memory formation impairs extinction learning but not the disruption of reconsolidation. Neuropsychopharmacology 2012, 37:1204-1215.
57. Tillisch K., Labus J., Nam B., Bueller J., Smith S., Suyenobu B., Siffert J., McKelvy J., Naliboff B., Mayer E.A. Neurokinin-1-receptor antagonism decreases anxiety and emotional arousal circuit response to noxious visceral distension in women with irritable bowel syndrome: a pilot study. Aliment. Pharmacol. Ther. 2012, 35:36-367.
58. Truong T.T., Naliboff B.D., Chang L. Novel techniques to study visceral hypersensitivity in irritable bowel syndrome. Curr. Gastroenterol. Rep. 2008, 10:369-378.
59. Valentino R.J., Miselis R.R., Pavcovich L.A. Pontine regulation of pelvic viscera: pharmacological target for pelvic visceral dysfunction. Trends Pharmacol. Sci. 1999, 20:253-260.
60. Verdu B., Decosterd I., Buclin T., Stiefel F., Berney A. Antidepressants for the treatment of chronic pain. Drugs 2008, 68:2611-2632.
61. Vianna E., Labus J.S., Berman S.M., Suyenobu B.Y., Jarcho J., Tillisch K., Naliboff B.D., Mayer E.A. Increased allocation of cognitive resources for selective attention in IBS patients. Gastroenterology 2009, 136. (A17-A17).
62. Vogt B.A., Aston-Jones G., Vogt L.J. Shared norepinephrinergic and cingulate circuits, nociceptive and allostatic interactions, and models of functional pain and stress disorders. Cingulate Neurobiology and Disease 2009, 467-498. Oxford University Press, New York. B.A. Vogt (Ed.).
63. Welch B.L. The generalization of students' problem when several different population variances are involved. Biometrika 1947, 34(1-2):28-35.
64. Wong M.L., Kling M.A., Munson P.J., Listwak S., Licinio J., Prolo P., Karp B., McCutcheon I.E., Geracioti T.D., DeBellis M.D., Rice K.C., Goldstein D.S., Veldhuis J.D., Chrousos G.P., Oldfield E.H., McCann S.M., Gold P.W. Pronounced and sustained central hypernoradrenergic function in major depression with melancholic features: relation to hypercortisolism and corticotropin-releasing hormone. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:325-330.
65. Wong H.Y., Mayer E.A., Naliboff B.D., Dickhaus B., Olivas T.I., Ameen V.Z., Reinholdt J., Chang L. Evidence for alterations in central autonomic activity during sleep in women with diarrhea-predominant irritable bowel syndrome (IBS-D). Gastroenterology 2006, 130(A-292).