Acute tryptophan depletion reduces kynurenine levels: Implications for treatment of impaired visuospatial memory performance in irritable bowel syndrome

Psychopharmacology

Volumn 232, Issue 8, 2015, Pages 1357-1371

  Kennedy, Paul J ^a,b   Allen, Andrew P ^a,b   O'Neill, Ann ^a   Quigley, Eamonn M M ^a,b,c   Cryan, John F ^a,b   Dinan, Timothy G ^a,b   Clarke, Gerard ^a,b  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b UNIVERSITY COLLEGE CORK   (Ireland)

^c HOUSTON METHODIST HOSPITAL   (United States)

Author keywords

Acute tryptophan depletion; Brain gut axis; CANTAB ; Cognition; Cognitive impairment; Irritable bowel syndrome (IBS); Kynurenine; Paired Associates Learning; Visuospatial memory

Indexed keywords

KYNURENINE; TRYPTOPHAN;

ADOLESCENT; ADULT; BLOOD; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; CROSSOVER PROCEDURE; DEFICIENCY; DOUBLE BLIND PROCEDURE; FEMALE; HIPPOCAMPUS; HUMAN; IRRITABLE BOWEL SYNDROME; MEMORY DISORDERS; METABOLISM; PHOTOSTIMULATION; PHYSIOLOGY; PROCEDURES; PSYCHOLOGY; PSYCHOMOTOR PERFORMANCE; TREATMENT OUTCOME; YOUNG ADULT;

ADOLESCENT; ADULT; CROSS-OVER STUDIES; DOUBLE-BLIND METHOD; FEMALE; HIPPOCAMPUS; HUMANS; IRRITABLE BOWEL SYNDROME; KYNURENINE; MEMORY DISORDERS; PHOTIC STIMULATION; PSYCHOMOTOR PERFORMANCE; TREATMENT OUTCOME; TRYPTOPHAN; YOUNG ADULT;

EID: 84939941566     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-014-3767-z     Document Type: Article

References (84)

1. 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
2. Alexander KS, Wu H-Q, Schwarcz R, Bruno JP (2012) Acute elevations of brain kynurenic acid impair cognitive flexibility: normalization by the alpha7 positive modulator galantamine. Psychopharmacology 220:627-637
3. Aron AR, Fletcher PC, Bullmore T, Sahakian BJ, Robbins TW (2003) Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans. Nat Neurosci 6:115-116
4. Badawy A (2013) Novel nutritional treatment for manic and psychotic disorders: a review of tryptophan and tyrosine depletion studies and the potential of protein-based formulations using glycomacropeptide. Psychopharmacology 228:347-358
5. Beck AT, Steer RA, Brown GK (1996) Manual for the Beck Depression Inventory-II. Psychological Corporation, San Antonio
6. Berman S, Suyenobu B, Naliboff BD, Bueller J, Stains J, Wong H, Mandelkern M, Fitzgerald L, Ohning G, Gupta A (2012) Evidence for alterations in central noradrenergic signaling in irritable bowel syndrome. NeuroImage 63:1854-1863
7. Blackwell AD, Sahakian BJ, Vesey R, Semple JM, Robbins TW, Hodges JR (2004) Detecting dementia: novel neuropsychological markers of preclinical Alzheimer's disease. Dement Feriatric Cogn 17:42-48
8. Blankstein U, Chen J, Diamant NE, Davis KD (2010) Altered brain structure in irritable bowel syndrome: potential contributions of pre-existing and disease-driven factors. Gastroenterology 138:1783-1789
9. Bond A, Lader M (1974) The use of analogue scales in rating subjective feelings. Br J Med Psychol 47:211-218
10. Buysse DJ, Reynolds CF 3rd, Monk TH, Berman SR, Kupfer DJ (1989) The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiatry Res 28:193-213
11. Capuron L, Miller AH (2011) Immune system to brain signaling: neuropsychopharmacological implications. Pharmacol Ther 130:226-238
12. Capuron L, Neurauter G, Musselman DL, Lawson DH, Nemeroff CB, Fuchs D, Miller AH (2003) Interferon-alpha-induced changes in tryptophan metabolism. Relationship to depression and paroxetine treatment. Biol Psychiatry 54:906-914
13. Chase HW, Crockett MJ, Msetfi RM, Murphy RA, Clark L, Sahakian BJ, Robbins TW (2011) 5-HT modulation by acute tryptophan depletion of human instrumental contingency judgements. Psychopharmacology 213:615-623
14. Chess AC, Simoni MK, Alling TE, Bucci DJ (2007) Elevations of endogenous kynurenic acid produce spatial working memory deficits. Schizophr Bull 33:797-804
15. Chess AC, Landers AM, Bucci DJ (2009) L-kynurenine treatment alters contextual fear conditioning and context discrimination but not cue-specific fear conditioning. Behav Brain Res 201:325-331
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. BMC Gastroenterol 9:6
17. Clarke G, Quigley EMM, Cryan JF, Dinan TG (2009b) Irritable bowel syndrome: towards biomarker identification. Trends Mol Med 15:478-489
18. 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. Front Pharmacol 3:90
19. Cohen S, Kamarck T, Mermelstein R (1983) A global measure of perceived stress. J Health Soc Behav 24(4):385-396
20. Cools R, Robinson OJ, Sahakian B (2007) Acute tryptophan depletion in healthy volunteers enhances punishment prediction but does not affect reward prediction. Neuropsychopharmacology 33:2291-2299
21. Corte Z, Venta R (2010) Biological variation of free plasma amino acids in healthy individuals. Clin Chem Lab Med CCLM FESCC 48:99-104
22. Coull JT, Frith CD, Frackowiak RSJ, Grasby PM (1996) A fronto-parietal network for rapid visual information processing: a PET study of sustained attention and working memory. Neuropsychologia 34:1085-1095
23. Crockett MJ, Clark L, Roiser JP, Robinson OJ, Cools R, Chase HW, Ouden H, Apergis-Schoute A, Campbell-Meiklejohn D, Seymour B, Sahakian BJ, Rogers RD, Robbins TW (2012) Converging evidence for central 5-HT effects in acute tryptophan depletion. Mol Psychiatry 17:121-123
24. Cryan JF, O'Mahony SM (2011) The microbiome-gut-brain axis: from bowel to behavior. Neurogastroenterol Motil 23:187-192
25. 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
26. Drossman DA, Camilleri M, Mayer EA, Whitehead WE (2002) AGA technical review on irritable bowel syndrome. Gastroenterology 123:2108-2131
27. Ellenbogen MA, Young SN, Dean P, Palmour RM, Benkelfat C (1996) Mood response to acute tryptophan depletion in healthy volunteers: sex differences and temporal stability. Neuropsychopharmacology 15:465-474
28. Ellingson BM, Mayer E, Harris RJ, Ashe-McNally C, Naliboff BD, Labus JS, Tillisch K (2013) Diffusion tensor imaging detects microstructural reorganization in the brain associated with chronic irritable bowel syndrome. Pain 154:1528-1541
29. Elliott R, Dolan RJ (1999) Differential neural responses during performance of matching and nonmatching to sample tasks at two delay intervals. J Neurosci 19:5066-5073
30. Elliott R, Baker SC, Rogers RD, O'Leary DA, Paykel ES, Frith CD, Dolan RJ, Sahakian BJ (1997) Prefrontal dysfunction in depressed patients performing a complex planning task: a study using positron emission tomography. Psychol Med 27:937-942
31. Elliott R, Rubinsztein JS, Sahakian BJ, Dolan RJ (2000) Selective attention to emotional stimuli in a verbal go/no-go task: an fMRI study. Neuroreport 11:1739-1744
32. Fitzgerald P, Cassidy Eugene M, 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. Neurogastroenterol Motil 20:1291-1297
33. Floden D, Stuss DT (2006) Inhibitory control is slowed in patients with right superior medial frontal damage. J Cogn Neurosci 18:1843-1849
34. Francis CY, Morris J, Whorwell PJ (1997) The irritable bowel severity scoring system: a simple method of monitoring irritable bowel syndrome and its progress. Aliment Pharmacol Ther 11:395-402
35. Fray PJ, Robbins TW (1996) CANTAB battery: proposed utility in neurotoxicology. Neurotoxicol Teratol 18:499-504
36. Goldstein M, Brendel G, Tuescher O, Pan H, Epstein J, Beutel M, Yang Y, Thomas K, Levy K, Silverman M (2007) Neural substrates of the interaction of emotional stimulus processing and motor inhibitory control: an emotional linguistic go/no-go fMRI study. Neuroimage 36:1026-1040
37. Grenham S, Clarke G, Cryan JF, Dinan TG (2011) Brain-gut-microbe communication in health and disease. Front Physiol 2:94
38. Groeger JA, Field D, Hammond SM (1999) Measuring memory span. Int J Psychol 34:359-363
39. Holzer P (2001) Gastrointestinal afferents as targets of novel drugs for the treatment of functional bowel disorders and visceral pain. Eur J Pharmacol 429:177-193
40. Holzer P (2004) Gastrointestinal pain in functional bowel disorders: sensory neurons as novel drug targets. Expert Opin Ther Targets 8:107-123
41. Hong J-Y, Kilpatrick LA, Labus J, Gupta A, Jiang Z, Ashe-McNalley C, Stains J, Heendeniya N, Ebrat B, Smith S (2013) Patients with chronic visceral pain show sex-related alterations in intrinsic oscillations of the resting brain. J Neurosci 33:11994-12002
42. Jiang Z, Dinov ID, Labus J, Shi Y, Zamanyan A, Gupta A, Ashe-McNalley C, Hong J-Y, Tillisch K, Toga AW (2013) Sex-related differences of cortical thickness in patients with chronic abdominal pain. PLoS One 8:e73932
43. Kennedy PJ, Clarke G, Quigley EMM, Groeger JA, Dinan TG, Cryan JF (2012) Gut memories: towards a cognitive neurobiology of irritable bowel syndrome. Neurosci Biobehav Rev 36:310-340
44. Kennedy PJ, Clarke G, O'Neill A, Groeger JA, Quigley EMM, Shanahan F, Cryan JF, Dinan TG (2014a) Cognitive performance in irritable bowel syndrome: evidence of a stress-related impairment in visuospatial memory. Psychol Med 44:1553-1566
45. Kennedy PJ, Cryan JF, Quigley EMM, Dinan TG, Clarke G (2014b) A sustained hypothalamic-pituitary-adrenal axis response to acute psychosocial stress in irritable bowel syndrome. Psychol Med FirstView 1-12
46. Klaassen T, Riedel WJ, van Someren A, Deutz NE, Honig A, van Praag HM (1999) Mood effects of 24-hour tryptophan depletion in healthy first-degree relatives of patients with affective disorders. Biol Psychiatry 46:489-497
47. Labus JS, Dinov ID, Jiang Z, Ashe-McNalley C, Zamanyan A, Shi Y, Hong J-Y, Gupta A, Tillisch K, Ebrat B (2014) Irritable bowel syndrome in female patients is associated with alterations in structural brain networks. Pain 155:137-149
48. Longstreth GF, Thompson WG, Chey WD, Houghton LA, Mearin F, Spiller RC (2006) Functional bowel disorders. Gastroenterology 130:1480-1491
49. Mayer EA, Tillisch K (2011) The brain-gut axis in abdominal pain syndromes. Annu Rev Med 62:381-396
50. Mayer EA, Naliboff BD, Chang L, Coutinho SV (2001) V. Stress and irritable bowel syndrome. Am J Physiol Gastrointest Liver Physiol 280:G519-G524
51. 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. Neurogastroenterol Motil Off J Eur Gastrointest Motil Soc 21:579-596
52. Mendelsohn D, Riedel WJ, Sambeth A (2009) Effects of acute tryptophan depletion on memory, attention and executive functions: a systematic review. Neurosci Biobehav Rev 33:926-952
53. Möller M, Du Preez JL, Viljoen FP, Berk M, Emsley R, Harvey BH (2013) Social isolation rearing induces mitochondrial, immunological, neurochemical and behavioural deficits in rats, and is reversed by clozapine or N-acetyl cysteine. Brain Behav Immun 30:156-167
54. Murphy FC, Smith KA, Cowen PJ, Robbins TW, Sahakian BJ (2002) The effects of tryptophan depletion on cognitive and affective processing in healthy volunteers. Psychopharmacology 163:42-53
55. Nachev P, Wydell H, O'Neill K, Husain M, Kennard C (2007) The role of the pre-supplementary motor area in the control of action. Neuroimage 36:T155-T163
56. Nelson H, Willison J (1991) National adult reading test (NART): test manual, 2nd edn. NFER Nelson, Windsor
57. Neumeister A, Nugent AC, Waldeck T, Geraci M, Schwarz M, Bonne O, Bain EE, Luckenbaugh DA, Herscovitch P, Charney DS (2004) Neural and behavioral responses to tryptophan depletion in unmedicated patients with remitted major depressive disorder and controls. Arch Gen Psychiatry 61:765
58. Nishizawa S, Benkelfat C, Young SN, Leyton M, Mzengeza S, de Montigny C, Blier P, Diksic M (1997) Differences between males and females in rates of serotonin synthesis in human brain. Proc Natl Acad Sci U S A 94:5308-5313
59. 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
60. 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 J Neurol 119(Pt 5):1597-1615
61. Riedel WJ, Klaassen T, Deutz NE, van Someren A, van Praag HM (1999) Tryptophan depletion in normal volunteers produces selective impairment in memory consolidation. Psychopharmacology 141:362-369
62. Robbins TW, Sahakian BJ (1994) Computer methods of assessment of cognitive function. Principles and Practice of Geriatric Psychiatry. John Wiley & Sons Ltd, Chichester, pp 205-209
63. Rowe JB, Owen AM, Johnsrude IS, Passingham RE (2001) Imaging the mental components of a planning task. Neuropsychologia 39:315-327
64. Ruddick JP, Evans AK, Nutt DJ, Lightman SL, Rook GA, Lowry CA (2006) Tryptophan metabolism in the central nervous system: medical implications. Expert Rev Mol Med 8:1-27
65. Sahakian BJ, Owen AM (1992) Computerized assessment in neuropsychiatry using CANTAB: discussion paper. J R Soc Med 85:399-402
66. Schmitt JA, Jorissen BL, Sobczak S, van Boxtel MP, Hogervorst E, Deutz NE, Riedel WJ (2000) Tryptophan depletion impairs memory consolidation but improves focussed attention in healthy young volunteers. J Psychopharmacol (Oxford, England) 14:21-29
67. Seminowicz DA, Labus JS, Bueller JA, Tillisch K, Naliboff BD, Bushnell MC, Mayer EA (2010) Regional gray matter density changes in brains of patients with irritable bowel syndrome. Gastroenterology 139(48-57):e2
68. Sheehan DV, Lecrubier Y, Sheehan KH, Amorim P, Janavs J, Weiller E, Hergueta T, Baker R, Dunbar GC (1998) The Mini-International Neuropsychiatric Interview (MINI): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J Clin Psychiatry 59:22-33
69. Spielberger CD, Gorsuch RL, Lushene R, Vagg PR, Jacobs GA (1983) Manual for the state-trait anxiety inventory. Consulting Psychologists Press, Palo Alto
70. Stone TW, Darlington LG (2002) Endogenous kynurenines as targets for drug discovery and development. Nat Rev Drug Discov 1:609-620
71. Stone TW, Darlington LG (2013) The kynurenine pathway as a therapeutic target in cognitive and neurodegenerative disorders. Br J Pharmacol 169:1211-1227
72. Strauss E, Sherman EMS, Spreen O (2006) Compendium of neuropsychological tests: administration, norms, and commentary, 3rd edn. Oxford University Press, NY
73. Sun X, Zhang X, Chen X, Zhang P, Bao M, Zhang D, Chen J, He S, Hu X (2005) Age-dependent brain activation during forward and backward digit recall revealed by fMRI. Neuroimage 26:36-47
74. 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. Dement Geriatr Cogn Disord 12:265-280
75. Sweeney JA, Kmiec JA, Kupfer DJ (2000) Neuropsychologic impairments in bipolar and unipolar mood disorders on the CANTAB neurocognitive battery. Biol Psychiatry 48:674-684
76. 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
77. van den Wildenberg WP, van Boxtel GJ, van der Molen MW, Bosch DA, Speelman JD, Brunia CH (2006) Stimulation of the subthalamic region facilitates the selection and inhibition of motor responses in Parkinson's disease. J Cogn Neurosci 18:626-636
78. van der Plasse G (2012) Converging evidence for central 5-HT effects in acute tryptophan depletion? Mol Psychiatry 18:271-272
79. van Donkelaar EL, Blokland A, Ferrington L, Kelly PA, Steinbusch HW, Prickaerts J (2011) Mechanism of acute tryptophan depletion: is it only serotonin? Mol Psychiatry 16:695-713
80. Vaynman S, Ying Z, Gomez-Pinilla F (2004) Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. Eur J Neurosci 20:2580-2590
81. Vecsei L, Szalardy L, Fulop F, Toldi J (2013) Kynurenines in the CNS: recent advances and new questions. Nat Rev Drug Discov 12:64-82
82. Watson D, Clark LA, Tellegen A (1988) Development and validation of brief measures of positive and negative affect: the PANAS scales. J Pers Soc Psychol 54:1063-1070
83. Woods DL, Kishiyama MM, Yund EW, Herron TJ, Edwards B, Poliva O, Hink RF, Reed B (2010) Improving digit span assessment of short-term verbal memory. J Clin Exp Neuropsychol 4:1-11
84. Young SN, Tourjman SV, Teff KL, Pihl RO, Anderson GH (1988) The effect of lowering plasma tryptophan on food selection in normal males. Pharmacol Biochem Behav 31:149-152