Cognitive performance in irritable bowel syndrome: Evidence of a stress-related impairment in visuospatial memory

Psychological Medicine

Volumn 44, Issue 7, 2014, Pages 1553-1566

  Kennedy, P J ^a,b   Clarke, G ^a,b   O'neill, A ^a   Groeger, J A ^c   Quigley, E M M ^a,d   Shanahan, F ^a,d   Cryan, J F ^a,d   Dinan, T G ^a,b  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b University College Cork and INFANT Centre   (Ireland)

^c UNIVERSITY OF HULL   (United Kingdom)

^d UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

CANTAB; cognition; cortisol; irritable bowel syndrome (IBS); stress

Indexed keywords

ADULT; COGNITION DISORDERS; COMPLICATION; CROHN DISEASE; FEMALE; HUMAN; IRRITABLE COLON; MALE; MEMORY DISORDERS; MENTAL STRESS; PHYSIOLOGY; PSYCHOLOGY; SPATIAL MEMORY;

ADULT; COGNITION DISORDERS; CROHN DISEASE; FEMALE; HUMANS; IRRITABLE BOWEL SYNDROME; MALE; MEMORY DISORDERS; SPATIAL MEMORY; STRESS, PSYCHOLOGICAL;

EID: 84897385384     PISSN: 00332917     EISSN: 14698978     Source Type: Journal    
DOI: 10.1017/S0033291713002171     Document Type: Article

References (103)

1. Afzal M, Potokar JP, Probert CS, Munafo MR (2006). Selective processing of gastrointestinal symptom-related stimuli in irritable bowel syndrome. Psychosomatic Medicine 68, 758-761
2. Agostini A, Benuzzi F, Filippini N, Bertani A, Scarcelli A, Farinelli V, Marchetta C, Calabrese C, Rizzello F, Gionchetti P, Ercolani M, Campieri M, Nichelli P (2013). New insights into the brain involvement in patients with Crohn's disease: A voxel-based morphometry study. Neurogastroenterology and Motility 25, 147-e82
3. Aizawa E, Sato Y, Kochiyama T, Saito N, Izumiyama M, Morishita J, Kanazawa M, Shima K, Mushiake H, Hongo M, Fukudo S (2012). Altered cognitive function of prefrontal cortex during error feedback in patients with irritable bowel syndrome, based on FMRI and dynamic causal modeling. Gastroenterology 143, 1188-1198
4. Alvarez JA, Emory E (2006). Executive function and the frontal lobes: A meta-Analytic review. Neuropsychology Review 16, 17-42
5. Assef EC, Capovilla AG, Capovilla FC (2007). Computerized Stroop test to assess selective attention in children with attention deficit hyperactivity disorder. Spanish Journal of Psychcology 10, 33-40
6. Austin MP, Mitchell P, Goodwin GM (2001). Cognitive deficits in depression: Possible implications for functional neuropathology. British Journal of Psychiatry 178, 200-206
7. Barbara G, Stanghellini V, De Giorgio R, Cremon C, Cottrell GS, Santini D, Pasquinelli G, Morselli-Labate AM, Grady EF, Bunnett NW, Collins SM, Corinaldesi R (2004). Activated mast cells in proximity to colonic nerves correlate with abdominal pain in irritable bowel syndrome. Gastroenterology 126, 693-702
8. Bender R, Lange S (2001). Adjusting for multiple testing-when and how? Journal of Clinical Epidemiology 54, 343-349
9. Bennett EJ, Tennant CC, Piesse C, Badcock CA, Kellow JE (1998). Level of chronic life stress predicts clinical outcome in irritable bowel syndrome. Gut 43, 256-261
10. Berman S, Munakata J, Naliboff BD, Chang L, Mandelkern M, Silverman D, Kovalik E, Mayer EA (2000). Gender differences in regional brain response to visceral pressure in IBS patients. European Journal of Pain 4, 157-172
11. Blackwell AD, Sahakian BJ, Vesey R, Semple JM, Robbins TW, Hodges Jr. (2004). Detecting dementia: Novel neuropsychological markers of preclinical Alzheimer's disease. Dementia and Geriatric Cognitive Disorders 17, 42-48
12. Bohmelt AH, Nater UM, Franke S, Hellhammer DH, Ehlert U (2005). Basal and stimulated hypothalamic-pituitary-Adrenal axis activity in patients with functional gastrointestinal disorders and healthy controls. Psychosomatic Medicine 67, 288-294
13. Botvinick MM, Cohen JD, Carter CS (2004). Conflict monitoring and anterior cingulate cortex: An update. Trends in Cognitive Sciences 8, 539-546
14. Chang L, Sundaresh S, Elliott J, Anton PA, Baldi P, Licudine A, Mayer M, Vuong T, Hirano M, Naliboff BD, Ameen VZ, Mayer EA (2009). Dysregulation of the hypothalamic-pituitary-Adrenal (HPA) axis in irritable bowel syndrome. Neurogastroenterology and Motility 21, 149-159
15. Chapman S, Martin M (2011). Attention to pain words in irritable bowel syndrome: Increased orienting and speeded engagement. British Journal of Health Psychology 16, 47-60
16. Clarke G, Fitzgerald P, Cryan JF, Cassidy EM, Quigley EM, Dinan TG (2009a). Tryptophan degradation in irritable bowel syndrome: Evidence of indoleamine 2,3-Dioxygenase activation in a male cohort. BioMed Central Gastroenterology 9, 6
17. Clarke G, McKernan DP, Gaszner G, Quigley EM, Cryan JF, Dinan TG (2012). A distinct profile of tryptophan metabolism along the kynurenine pathway downstream of toll-like receptor activation in irritable bowel syndrome. Frontiers in Pharmacology 3, 90
18. Clarke G, Quigley EMM, Cryan JF, Dinan TG (2009b). Irritable bowel syndrome: Towards biomarker identification. Trends in Molecular Medicine 15, 478-489
19. Collins SM (2005). Dysregulation of peripheral cytokine production in irritable bowel syndrome. American Journal of Gastroenterology 100, 2517-2518
20. Collins SM, Surette M, Bercik P (2012). The interplay between the intestinal microbiota and the brain. Nature Reviews Microbiology 10, 735-742
21. Coyne JC, van Sonderen E (2012a). The Hospital Anxiety and Depression Scale (HADS) is dead, but like Elvis, there will still be citings. Journal of Psychosomatic Research 73, 77-78
22. Coyne JC, van Sonderen E (2012b). No further research needed: Abandoning the Hospital and Anxiety Depression Scale (HADS). Journal of Psychosomatic Research 72, 173-174
23. Creed F (2007). Cognitive behavioural model of irritable bowel syndrome. Gut 56, 1039-1041
24. Creed F, Fernandes L, Guthrie E, Palmer S, Ratcliffe J, Read N, Rigby C, Thompson D, Tomenson B (2003). The cost-effectiveness of psychotherapy and paroxetine for severe irritable bowel syndrome. Gastroenterology 124, 303-317
25. Creed F, Guthrie E, Ratcliffe J, Fernandes L, Rigby C, Tomenson B, Read N, Thompson DG (2005). Does psychological treatment help only those patients with severe irritable bowel syndrome who also have a concurrent psychiatric disorder? Australian and New Zealand Journal of Psychiatry 39, 807-815
26. Creed F, Tomenson B, Guthrie E, Ratcliffe J, Fernandes L, Read N, Palmer S, Thompson DG (2008). The relationship between somatisation and outcome in patients with severe irritable bowel syndrome. Journal of Psychosomatic Research 64, 613-620
27. Cryan JF, O'Mahony SM (2011). The microbiome-gut-brain axis: From bowel to behavior. Neurogastroenterology and Motility 23, 187-192
28. de Kloet ER, Oitzl MS, Joels M (1999). Stress and cognition: Are corticosteroids good or bad guys? Trends in Neurosciences 22, 422-426
29. de Rover M, Pironti VA, McCabe JA, Acosta-Cabronero J, Arana FS, Morein-Zamir S, Hodges JR, Robbins TW, Fletcher PC, Nestor PJ, Sahakian BJ (2011). Hippocampal dysfunction in patients with mild cognitive impairment: A functional neuroimaging study of a visuospatial paired associates learning task. Neuropsychologia 49, 2060-2070
30. Dinan TG, Clarke G, Quigley EM, Scott LV, Shanahan F, Cryan J, Cooney J, Keeling PW (2008). Enhanced cholinergic-mediated increase in the pro-inflammatory cytokine IL-6 in irritable bowel syndrome: Role of muscarinic receptors. American Journal of Gastroenterology 103, 2570-2576
31. Dinan TG, Quigley EM, Ahmed SM, Scully P, O'Brien S, O'Mahony L, O'Mahony S, Shanahan F, Keeling PW (2006). Hypothalamic-pituitary-gut axis dysregulation in irritable bowel syndrome: Plasma cytokines as a potential biomarker? Gastroenterology 130, 304-311
32. Downes JJ, Roberts AC, Sahakian BJ, Evenden JL, Morris RG, Robbins TW (1989). Impaired extra-Dimensional shift performance in medicated and unmedicated Parkinson's disease: Evidence for a specific attentional dysfunction. Neuropsychologia 27, 1329-1243
33. Feise RJ (2002). Do multiple outcome measures require p-Value adjustment? BMC Medical Research Methodology 2, 8
34. Fitzgerald P, Cassidy EugeneM, Clarke G, Scully P, Barry S, Quigley Eamonn MM, Shanahan F, Cryan J, Dinan Timothy G (2008). Tryptophan catabolism in females with irritable bowel syndrome: Relationship to interferon-gamma, severity of symptoms and psychiatric co-morbidity. Neurogastroenterology and Motility 20, 1291-1297
35. Ford AC, Forman D, Bailey AG, Axon AT, Moayyedi P (2008). Fluctuation of gastrointestinal symptoms in the community: A 10-year longitudinal follow-up study. Alimentary Pharmacology and Therapeutics 28, 1013-1020
36. Fray PJ, Robbins TW (1996). CANTAB battery: Proposed utility in neurotoxicology. Neurotoxicology and Teratology 18, 499-504
37. Fries E, Dettenborn L, Kirschbaum C (2009). The cortisol awakening response (CAR): Facts and future directions. International Journal of Psychophysiology 72, 67-73
38. Gibbs-Gallagher N, Palsson OS, Levy RL, Meyer K, Drossman DA, Whitehead WE (2001). Selective recall of gastrointestinal-sensation words: Evidence for a cognitive-behavioral contribution to irritable bowel syndrome. American Journal of Gastroenterology 96, 1133-1138
39. Glass JM (2006). Cognitive dysfunction in fibromyalgia and chronic fatigue syndrome: New trends and future directions. Current Rheumatology Reports 8, 425-429
40. Gomborone JE, Dewsnap PA, Libby GW, Farthing MJ (1993). Selective affective biasing in recognition memory in the irritable bowel syndrome. Gut 34, 1230-1233
41. Goodhand JR, Wahed M, Mawdsley JE, Farmer AD, Aziz Q, Rampton DS (2012). Mood disorders in inflammatory bowel disease: Relation to diagnosis, disease activity, perceived stress, and other factors. Inflammatory Bowel Diseases 18, 2301-2309
42. Grenham S, Clarke G, Cryan JF, Dinan TG (2011). Brain-gut-microbe communication in health and disease. Frontiers in Physiology 2, 94
43. Guilarte M, Santos J, de Torres I, Alonso C, Vicario M, Ramos L, Martinez C, Casellas F, Saperas E, Malagelada Jr. (2007). Diarrhoea-predominant IBS patients show mast cell activation and hyperplasia in the jejunum. Gut 56, 203-209
44. Hazlett-Stevens H, Craske MG, Mayer EA, Chang L, Naliboff BD (2003). Prevalence of irritable bowel syndrome among university students: The roles of worry, neuroticism, anxiety sensitivity and visceral anxiety. Journal of Psychosomatic Research 55, 501-505
45. Hinkelmann K, Muhtz C, Dettenborn L, Agorastos A, Moritz S, Wingenfeld K, Spitzer C, Gold SM, Wiedemann K, Otte C (2013). Association between cortisol awakening response and memory function in major depression. Psychological Medicine. Published online: 27 February 2013. doi:10.1017/S0033291713000287
46. Kennedy PJ, Clarke G, Quigley EM, Groeger JA, Dinan TG, Cryan JF (2012). Gut memories: Towards a cognitive neurobiology of irritable bowel syndrome. Neuroscience and Biobehavioral Reviews 36, 310-340
47. Kroenke K, Spitzer RL, Williams JB (2001). The PHQ-9: Validity of a brief depression severity measure. Journal of General Internal Medicine 16, 606-613
48. Lackner JM, Lou Coad M, Mertz HR, Wack DS, Katz LA, Krasner SS, Firth R, Mahl TC, Lockwood AH (2006). Cognitive therapy for irritable bowel syndrome is associated with reduced limbic activity, GI symptoms, and anxiety. Behaviour Research and Therapy 44, 621-638
49. Law R, Hucklebridge F, Thorn L, Evans P, Clow A (2013). State variation in the cortisol awakening response. Stress. Published online: 29 July 2013. doi:10.3109/ 10253890.2013.817552
50. Lembo AJ, Zaman M, Krueger RF, Tomenson BM, Creed FH (2009). Psychiatric disorder, irritable bowel syndrome, and extra-intestinal symptoms in a population-based sample of twins. American Journal of Gastroenterology 104, 686-694
51. Levy RL, Cain KC, Jarrett M, Heitkemper MM (1997). The relationship between daily life stress and gastrointestinal symptoms in women with irritable bowel syndrome. Journal of Behavioral Medicine 20, 177-193
52. Liebregts T, Adam B, Bredack C, Roth A, Heinzel S, Lester S, Downie-Doyle S, Smith E, Drew P, Talley NJ, Holtmann G (2007). Immune activation in patients with irritable bowel syndrome. Gastroenterology 132, 913-920
53. Longstreth GF, Thompson WG, Chey WD, Houghton LA, Mearin F, Spiller RC (2006). Functional bowel disorders. Gastroenterology 130, 1480-1491
54. Longstreth GF, Wilson A, Knight K, Wong J, Chiou CF, Barghout V, Frech F, Ofman JJ (2003). Irritable bowel syndrome, health care use, and costs: A U.S. managed care perspective. American Journal of Gastroenterology 98, 600-607
55. Lupien SJ, Maheu F, Tu M, Fiocco A, Schramek TE (2007). The effects of stress and stress hormones on human cognition: Implications for the field of brain and cognition. Brain and Cognition 65, 209-237
56. Lupien SJ, McEwen BS, Gunnar MR, Heim C (2009). Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nature Reviews Neuroscience 10, 434-445
57. Martin M, Chapman SC (2010). Cognitive processing in putative functional gastrointestinal disorder: Rumination yields orientation to social threat not pain. European Journal of Pain 14, 207-213
58. Mayer EA (2000). The neurobiology of stress and gastrointestinal disease. Gut 47, 861-869
59. Mayer EA, Aziz Q, Coen S, Kern M, Labus JS, Lane R, Kuo B, Naliboff B, Tracey I (2009). Brain imaging approaches to the study of functional GI disorders: A Rome working team report. Neurogastroenterology and Motility 21, 579-596
60. Mayer EA, Naliboff BD, Chang L, Coutinho SV (2001). V. Stress and irritable bowel syndrome. American Journal of Physiology Gastrointestinal and Liver Physiology 280, G519-G524
61. Mayer EA, Tillisch K (2011). The brain-gut axis in abdominal pain syndromes. Annual Review of Medicine 62, 381-396
62. McEwen BS (1999). Stress and the aging hippocampus. Frontiers in Neuroendocrinology 20, 49-70
63. McKernan DP, Gaszner G, Quigley EM, Cryan JF, Dinan TG (2011). Altered peripheral toll-like receptor responses in the irritable bowel syndrome. Alimentary Pharmacology and Therapeutics 33, 1045-1052
64. Mehta MA, Sahakian BJ, McKenna PJ, Robbins TW (1999). Systemic sulpiride in young adult volunteers simulates the profile of cognitive deficits in Parkinson's disease. Psychopharmacology 146, 162-174
65. Moriarty O, McGuire BE, Finn DP (2011). The effect of pain on cognitive function: A review of clinical and preclinical research. Progress in Neurobiology 93, 385-404
66. Mykletun A, Jacka F, Williams L, Pasco J, Henry M, Nicholson GC, Kotowicz MA, Berk M (2010). Prevalence of mood and anxiety disorder in self reported irritable bowel syndrome (IBS). An epidemiological population based study of women. BioMed Central Gastroenterology 10, 88
67. Nagahama Y, Okada T, Katsumi Y, Hayashi T, Yamauchi H, Oyanagi C, Konishi J, Fukuyama H, Shibasaki H (2001). Dissociable mechanisms of attentional control within the human prefrontal cortex. Cerebral Cortex 11, 85-92
68. Naliboff BD, Berman S, Chang L, Derbyshire SW, Suyenobu B, Vogt BA, Mandelkern M, Mayer EA (2003). Sex-related differences in IBS patients: Central processing of visceral stimuli. Gastroenterology 124, 1738-1747
69. Nelson H, Willison J (1991). National Adult Reading Test (NART): Test Manual. NFER Nelson: Windsor
70. Norton S, Sacker A, Done J (2012). Further research needed: A comment on Coyne and van Sonderen's call to abandon the Hospital Anxiety and Depression Scale. Journal of Psychosomatic Research 73, 75-76; author reply 77-78
71. Ohman L, Simren M (2007). New insights into the pathogenesis and pathophysiology of irritable bowel syndrome. Digestive and Liver Disease 39, 201-215
72. Ohman L, Simren M (2010). Pathogenesis of IBS: Role of inflammation, immunity and neuroimmune interactions. Nature Reviews Gastroenterology and Hepatology 7, 163-173
73. Owen AM, Morris RG, Sahakian BJ, Polkey CE, Robbins TW (1996). Double dissociations of memory and executive functions in working memory tasks following frontal lobe excisions, temporal lobe excisions or amygdalo-hippocampectomy in man. Brain 119, 1597-1615
74. Owen AM, Sahakian BJ, Semple J, Polkey CE, Robbins TW (1995). Visuo-spatial short-Term recognition memory and learning after temporal lobe excisions, frontal lobe excisions or amygdalo-hippocampectomy in man. Neuropsychologia 33, 1-24
75. Posserud I, Svedlund J, Wallin J, Simren M (2009). Hypervigilance in irritable bowel syndrome compared with organic gastrointestinal disease. Journal of Psychosomatic Research 66, 399-405
76. Pruessner JC, Kirschbaum C, Meinlschmid G, Hellhammer DH (2003). Two formulas for computation of the area under the curve represent measures of total hormone concentration versus time-Dependent change. Psychoneuroendocrinology 28, 916-931
77. Quigley EM (2006). Changing face of irritable bowel syndrome. World Journal of Gastroenterology 12, 1-5
78. Rahman S, Sahakian BJ, Hodges JR, Rogers RD, Robbins TW (1999). Specific cognitive deficits in mild frontal variant frontotemporal dementia. Brain 122, 1469-1493
79. Raison CL, Capuron L, Miller AH (2006). Cytokines sing the blues: Inflammation and the pathogenesis of depression. Trends in Immunology 27, 24-31
80. Robbins TW, James M, Owen AM, Sahakian BJ, Lawrence AD, McInnes L, Rabbitt PM (1998). A study of performance on tests from the CANTAB battery sensitive to frontal lobe dysfunction in a large sample of normal volunteers: Implications for theories of executive functioning and cognitive aging. Cambridge Neuropsychological Test Automated Battery. Journal of the International Neuropsychological Society 4, 474-490
81. Robbins TW, Sahakian BJ (1994). Computer methods of assessment of cognitive function. In Principles and Practice of Geriatric Psychiatry, pp. 205-209. John Wiley & Sons Ltd: Chichester
82. Sahakian BJ, Owen AM (1992). Computerized assessment in neuropsychiatry using CANTAB: Discussion paper. Journal of the Royal Society of Medicine 85, 399-402
83. Scully P, McKernan DP, Keohane J, Groeger D, Shanahan F, Dinan TG, Quigley EM (2010). Plasma cytokine profiles in females with irritable bowel syndrome and extra-intestinal co-morbidity. American Journal of Gastroenterology 10, 2235-2243
84. Sharpe M, Peveler R, Mayou R (1992). The psychological treatment of patients with functional somatic symptoms: A practical guide. Journal of Psychosomatic Research 36, 515-529
85. Snaith RP (2003). The Hospital Anxiety and Depression Scale. Health and Quality of Life Outcomes 1, 29
86. Song L, Che W, Min-Wei W, Murakami Y, Matsumoto K (2006). Impairment of the spatial learning and memory induced by learned helplessness and chronic mild stress. Pharmacology, Biochemistry and Behavior 83, 186-193
87. Spence MJ, Moss-Morris R (2007). The cognitive behavioural model of irritable bowel syndrome: A prospective investigation of patients with gastroenteritis. Gut 56, 1066-1071
88. Spiegel BM (2009). The burden of IBS: Looking at metrics. Current Gastroenterology Reports 11, 265-269
89. Sterlemann V, Rammes G, Wolf M, Liebl C, Ganea K, Muller MB, Schmidt MV (2010). Chronic social stress during adolescence induces cognitive impairment in aged mice. Hippocampus 20, 540-549
90. Strauss E, Sherman EMS, Spreen O (2006). Compendium of Neuropsychological Tests: Administration, Norms, and Commentary. Oxford University Press: New York
91. Suarez-Hitz KA, Otto B, Bidlingmaier M, Schwizer W, Fried M, Ehlert U (2012). Altered psychobiological responsiveness in women with irritable bowel syndrome. Psychosomatic Medicine 74, 221-231
92. Swainson R, Hodges JR, Galton CJ, Semple J, Michael A, Dunn BD, Iddon JL, Robbins TW, Sahakian BJ (2001). Early detection and differential diagnosis of Alzheimer's disease and depression with neuropsychological tasks. Dementia and Geriatric Cognitive Disorders 12, 265-280
93. Sweeney JA, Kmiec JA, Kupfer DJ (2000). Neuropsychologic impairments in bipolar and unipolar mood disorders on the CANTAB neurocognitive battery. Biological Psychiatry 48, 674-684
94. Tillisch K, Labus JS, Naliboff BD, Bolus R, Shetzline M, Mayer EA, Chang L (2005). Characterization of the alternating bowel habit subtype in patients with irritable bowel syndrome. American Journal of Gastroenterology 100, 896-904
95. Tillisch K, Mayer EA, Labus JS (2011). Quantitative meta-Analysis identifies brain regions activated during rectal distension in irritable bowel syndrome. Gastroenterology 140, 91-100
96. Vogt BA (2013). Inflammatory bowel disease: Perspectives from cingulate cortex in the first brain. Neurogastroenterology and Motility 25, 93-98
97. Weiss EM, Kemmler G, Deisenhammer EA, Fleischhacker WW, Delazer M (2003). Sex differences in cognitive functions. Personality and Individual Differences 35, 863-875
98. Wells CW, Lewis S, Barton JR, Corbett S (2006). Effects of changes in hemoglobin level on quality of life and cognitive function in inflammatory bowel disease patients. Inflammatory Bowel Diseases 12, 123-130
99. Whorwell PJ, Prior A, Colgan SM (1987). Hypnotherapy in severe irritable bowel syndrome: Further experience. Gut 28, 423-425
100. Whorwell PJ, Prior A, Faragher EB (1984). Controlled trial of hypnotherapy in the treatment of severe refractory irritable-bowel syndrome. Lancet 2, 1232-1234
101. Wilson S, Roberts L, Roalfe A, Bridge P, Singh S (2004). Prevalence of irritable bowel syndrome: A community survey. British Journal of Gerneral Practice 54, 495-502
102. Wolf OT (2003). HPA axis and memory. Best Practice and Research: Clinical Endocrinology and Metabolism 17, 287-299
103. Zigmond AS, Snaith RP (1983). The hospital anxiety and depression scale. Acta Psychiatrica Scandinavica 67, 361-370