Skip to main content

Advertisement

Log in

Changes in Tryptophan Catabolite (TRYCAT) Pathway Patterning Are Associated with Mild Impairments in Declarative Memory in Schizophrenia and Deficits in Semantic and Episodic Memory Coupled with Increased False-Memory Creation in Deficit Schizophrenia

  • Published:
Molecular Neurobiology Aims and scope Submit manuscript

Abstract

Evidence indicates that schizophrenia and in particular negative symptoms and deficit schizophrenia are accompanied by neurocognitive impairments and changes in the patterning of the tryptophan catabolite (TRYCAT) pathway. This cross-sectional study was carried out to examine the associations between cognitive functions (as measured with Consortium to Establish a Registry for Alzheimer’s disease (CERAD)) and TRYCAT pathway patterning in patients with (n = 40) and without (n = 40) deficit schizophrenia and normal controls (n = 40). Cognitive measures were assessed with the Verbal Fluency Test (VFT), Boston Naming Test (BNT), Mini-Mental State Examination (MMSE), Word List Memory (WLM), Constructional Praxis, Word List Recall (WLRecall), and Word List Recognition (WLRecognition), while TRYCAT measurements assessed the IgA/IgM responses to noxious TRYCATs, namely quinolinic acid (QA), 3-OH-kynurenine (3HK), picolinic acid (PA), and xanthurenic (XA) acid, and more protective (PRO) TRYCATs, including kynurenic acid (KA) and anthranilic acid (AA). IgA NOX/PRO, IgM KA/3HK, and IgA/IgM NOX/PRO ratios were computed. Schizophrenia was accompanied by lower VFT and WLM, while BNT (dysnomia) and MMSE are significantly lower in multiple- than first-episode schizophrenia. Deficit schizophrenia is strongly associated with worse outcomes on VFT, MMSE, WLM, WLRecall, WLRecognition, and delayed recall savings and increased false memories. Around 40–50% of the variance in negative symptoms’ scores was explained by VFT, WLM, WLRecall, and MMSE. Increases in IgA NOX/PRO, IgM KA/3HK, and/or IgA/IgM NOX/PRO ratios were associated with impairments in VFT, BNT, MMSE, WLM, WLRecall, WLRecognition, and false-memory creation. In conclusion, nondeficit schizophrenia is accompanied by mild memory impairments, while disease progression is accompanied by broader cognitive impairments. Deficit schizophrenia and negative symptoms are strongly associated with deficits in working memory, delayed recall and recognition, and increased false-memory creation. These cognitive impairments and memory deficits are in part explained by increased production and/or attenuated regulation of TRYCATs with neurotoxic, excitotoxic, immune-inflammatory, oxidative, and nitrosative potential, which may contribute to neuroprogression.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Andreasen NC, Olsen S (1982) Negative v positive schizophrenia. Definition and validation. Arch Gen Psychiatry 39(7):789–794

    Article  CAS  PubMed  Google Scholar 

  2. Emsley RA, Oosthuizen PP, Joubert AF, Roberts MC, Stein DJ (1999) Depressive and anxiety symptoms in patients with schizophrenia and schizophreniform disorder. J Clin Psychiatry 60(11):747–751

    Article  CAS  PubMed  Google Scholar 

  3. Mellor CS (1991) Methodological problems in identifying and measuring first-rank symptoms of schizophrenia. In: Marneros A, Andreasen N, Tsuang MT (eds) Negative versus positive schizophrenia. Springer-Verlag, Berlin, pp. 71–78. https://doi.org/10.1007/978-3-642-76841-5_8

    Chapter  Google Scholar 

  4. Marneros A, Deister A, Rohde A (1991) Long-term monomorphism of negative and positive schizophrenic episodes. In: Marneros A, Andreasen N, Tsuang MT (eds) Negative versus positive schizophrenia. Springer-Verlag, Berlin, pp. 183–196. https://doi.org/10.1007/978-3-642-76841-5_8

    Chapter  Google Scholar 

  5. Cuesta MJ, Peralta V (1995) Cognitive disorders in the positive, negative, and disorganization syndromes of schizophrenia. Psychiatry Res 58(3):227–235

    Article  CAS  PubMed  Google Scholar 

  6. Schaefer J, Giangrande E, Weinberger DR, Dickinson D (2013) The global cognitive impairment in schizophrenia: consistent over decades and around the world. Schizophr Res 150(1):42–50

    Article  PubMed  PubMed Central  Google Scholar 

  7. Kanchanatawan B, Sirivichayakul S, Ruxrungtham K, Carvalho AF, Geffard M, Ormstad H, Anderson G, Maes M (2017) Deficit, but not nondeficit, schizophrenia is characterized by mucosa-associated activation of the tryptophan catabolite (TRYCAT) pathway with highly specific increases in IgA responses directed to picolinic, xanthurenic, and quinolinic acid. Mol Neurobiol (in press). https://doi.org/10.1007/s12035-017-0417-6

  8. Kanchanatawan B, Sirivichayakul S, Thika S, Ruxrungtham K, Carvalho AF, Geffard M, Anderson G, Noto C et al (2017) Physio-somatic symptoms in schizophrenia: association with depression, anxiety, neurocognitive deficits and the tryptophan catabolite pathway. Metab Brain Dis (in press). https://doi.org/10.1007/s11011-017-9982-7

  9. Reichenberg A (2010) The assessment of neuropsychological functioning in schizophrenia. Dialogues Clin Neurosci 12(3):383–392

    PubMed  Google Scholar 

  10. Yu M, Tang X, Wang X, Zhang X, Zhang X, Sha W, Yao S, Shu N et al (2015) Neurocognitive impairments in deficit and non-deficit schizophrenia and their relationships with symptom dimensions and other clinical variables. PLoS One 10:e0138357

    Article  PubMed  PubMed Central  Google Scholar 

  11. Keefe RS, Harvey PD (2012) Cognitive impairment in schizophrenia. Handb Exp Pharmacol 213:11–37

    Article  CAS  Google Scholar 

  12. Seidman LJ, Lanca M, Kremen WS, Faraone SV, Tsuang MT (2003) Organizational and visual memory deficits in schizophrenia and bipolar psychoses using the Rey-Osterrieth complex figure: effects of duration of illness. J Clin Exp Neuropsychol 25:949–964

    Article  PubMed  Google Scholar 

  13. Grillon ML, Krebs MO, Gourevitch R, Giersch A, Huron C (2010) Episodic memory and impairment of an early encoding process in schizophrenia. Neuropsychology 24(1):101–108

    Article  PubMed  Google Scholar 

  14. Christensen BK, Patrick RE, Stuss DT, Gillingham S, Zipursky RB (2013) CE verbal episodic memory impairment in schizophrenia: a comparison with frontal lobe lesion patients. Clin Neuropsychol 27(4):647–666

    Article  PubMed  Google Scholar 

  15. Davidson M, Harvey P, Welsh KA, Powchik P, Putnam KM, Mohs RC (1996) Cognitive functioning in late-life schizophrenia: a comparison of elderly schizophrenic patients and patients with Alzheimer’s disease. Am J Psychiatry 153(10):1274–1279

    Article  CAS  PubMed  Google Scholar 

  16. Barch DM, Ceaser A (2012) Cognition in schizophrenia: core psychological and neural mechanisms. Trends Cogn Sci 16(1):27–34

    Article  PubMed  Google Scholar 

  17. Berna F, Potheegadoo J, Aouadi I, Ricarte JJ, Allé MC, Coutelle R, Boyer L, Cuervo-Lombard CV et al (2016) A meta-analysis of autobiographical memory studies in schizophrenia spectrum disorder. Schizophr Bull 42(1):56–66

    PubMed  Google Scholar 

  18. Chan RC, Xu T, Heinrichs RW, Yu Y, Wang Y (2010) Neurological soft signs in schizophrenia: a meta-analysis. Schizophr Bull 36(6):1089–1104

    Article  PubMed  Google Scholar 

  19. Kirkpatrick B, Galderisi S (2008) Deficit schizophrenia: an update. World Psychiatry 7:143–147

    Article  PubMed  PubMed Central  Google Scholar 

  20. Cohen AS, Docherty NM (2004) Deficit versus negative syndrome in schizophrenia: prediction of attentional impairment. Schizophr Bull 30(4):827–835

    Article  PubMed  Google Scholar 

  21. Fervaha G, Takeuchi H, Foussias G, Agid O, Remington G (2016) Using poverty of speech as a case study to explore the overlap between negative symptoms and cognitive dysfunction. Schizophr Res 176(2–3):411–416

    Article  PubMed  Google Scholar 

  22. Kanchanatawan B, Sirivichayakul S, Ruxrungtham K, Carvalho AF, Geffard M, Anderson G, Maes M (2017) Deficit schizophrenia is characterized by defects in IgM-mediated responses to tryptophan catabolites (TRYCATs): a paradigm shift towards defects in natural self-regulatory immune responses coupled with mucosa-derived TRYCAT pathway activation. Mol Neurobiol (in press). https://doi.org/10.1007/s12035-017-0465-y

  23. Polgár P (2011) Differentiation of deficit and non-deficit schizophrenia based on cognitive functions. Ideggyogy Sz 64(3–4):128–132

    PubMed  Google Scholar 

  24. Harvey PD, Koren D, Reihenberg A, Bowie CR (2006) Negative symptoms and cognitive deficits: what is the nature of their relationship? Schizophr Bull 32:250–258

    Article  PubMed  Google Scholar 

  25. American Psychiatric Association (2000) Diagnostic and statistical manual of mental disorders: DSM-IV-TR. American Psychiatric Association, Washington, DC

    Google Scholar 

  26. American Psychiatric Association (2013) Diagnostic and statistical manual of mental disorders, 5th edn. Arlington, VA

    Book  Google Scholar 

  27. Kirkpatrick B, Buchanan RW, McKenney PD, Alphs LD, Carpenter WT Jr (1989) The schedule for the deficit syndrome: an instrument for research in schizophrenia. Psychiatry Res 30:119–123

    Article  CAS  PubMed  Google Scholar 

  28. Kittirathanapaiboon P, Khamwongpin M (2005) The validity of the Mini International Neuropsychiatric Interview (M.I.N.I.) Thai version: Suanprung Hospital, Department of Mental Health

  29. Kay SR, Fiszbein A, Opler LA (1986) Negative symptom rating scale: limitations in psychometric and research methodology. Psychiatry Res 19:169–173

    Article  CAS  PubMed  Google Scholar 

  30. Andreasen NC (1989) The Scale for the Assessment of Negative Symptoms (SANS): conceptual and theoretical foundations. Br J Psychiatry Suppl 7:49–58

    Google Scholar 

  31. Overall JE, Gorham DR (1962) The brief psychiatric rating scale. Psychol Reports 10:799–812

    Article  Google Scholar 

  32. Heatherton TF, Kozlowski LT, Frecker RC, Fagerström KO (1991) The Fagerström test for nicotine dependence: a revision of the Fagerström tolerance questionnaire. Br J Addict 86:1119–1127

    Article  CAS  PubMed  Google Scholar 

  33. CERAD (1986) CERAD—an overview: the Consortium to Establish a Registry for Alzheimer’s Disease. http://cerad.mc.duke.edu/

  34. Beeri MS, Schmeidler J, Sano M, Wang J, Lally R, Grossman H, Silverman JM (2006) Age, gender, and education norms on the CERAD neuropsychological battery in the oldest old. Neurology 67(6):1006–1010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Welsh KA, Butters N, Mohs RC, Beekly D, Edland S, Fillenbaum G, Heyman A (1994) The consortium to establish a registry for Alzheimer’s disease (CERAD). Part V: a normative study of the neuropsychological battery. Neurology 44(4):609–614

    Article  CAS  PubMed  Google Scholar 

  36. Kaplan EF, Goodglass H, Weintraub S (1978) The Boston naming test. Veterans Administration Medical Center, Boston

    Google Scholar 

  37. Duleu S, Mangas A, Sevin F, Veyret B, Bessede A, Geffard M (2010) Circulating antibodies to IDO/THO pathway metabolites in Alzheimer’s disease. Int J Alzheimers Dis. https://doi.org/10.4061/2010/501541

  38. Roomruangwong C, Kanchanatawan B, Sirivichayakul S, Anderson G, Carvalho AF, Duleu S, Geffard M, Maes M (2017) IgA/IgM responses to gram-negative bacteria are not associated with prenatal depression, but with physio-somatic symptoms and activation of the tryptophan catabolite pathway at the end of term and postnatal anxiety. CNS Neurol Disord Drug Targets (in press). https://doi.org/10.2174/1871527316666170407145533

  39. Trojano L, Gainotti G (2016) Drawing disorders in Alzheimer’s disease and other forms of dementia. J Alzheimers Dis 53(1):31–52

    Article  PubMed  Google Scholar 

  40. Golimbet V, Gritsenko I, Alfimova M, Lebedeva I, Lezheiko T, Abramova L, Kaleda V, Ebstein R (2006) Association study of COMT gene Val158Met polymorphism with auditory P300 and performance on neurocognitive tests in patients with schizophrenia and their relatives. World J Biol Psychiatry 7(4):238–245

    Article  PubMed  Google Scholar 

  41. Holthausen EA, Wiersma D, Sitskoorn MM, Dingemans PM, Schene AH, van den Bosch RJ (2003) Long-term memory deficits in schizophrenia: primary or secondary dysfunction? Neuropsychology 17(4):539–547

    Article  PubMed  Google Scholar 

  42. Ragland JD, Laird AR, Ranganath C, Blumenfeld RS, Gonzales SM, Glahn DC (2009) Prefrontal activation deficits during episodic memory in schizophrenia. Am J Psychiatry 166(8):863–874

    Article  PubMed  PubMed Central  Google Scholar 

  43. Ragland JD, Ranganath C, Harms MP, Barch DM, Gold JM, Layher E, Lesh TA, MacDonald AW 3rd et al (2015) Functional and neuroanatomic specificity of episodic memory dysfunction in schizophrenia: a functional magnetic resonance imaging study of the relational and item-specific encoding task. JAMA Psychiatry 72(9):909–916

    Article  PubMed  PubMed Central  Google Scholar 

  44. Bonner-Jackson A, Haut K, Csernansky JG, Barch DM (2005) The influence of encoding strategy on episodic memory and cortical activity in schizophrenia. Biol Psychiatry 58(1):47–55

    Article  PubMed  PubMed Central  Google Scholar 

  45. Rushe TM, Woodruff PW, Murray RM, Morris RG (1999) Episodic memory and learning in patients with chronic schizophrenia. Schizophr Res 35(1):85–96

    Article  CAS  PubMed  Google Scholar 

  46. Leavitt VM, Goldberg TE (2009) Episodic memory in schizophrenia. Neuropsychol Rev 19(3):312–323

    Article  PubMed  Google Scholar 

  47. Czepielewski LS, Massuda R, Goi P, Sulzbach-Vianna M, Reckziegel R, Costanzi M, Kapczinski F, Rosa AR et al (2015) Verbal episodic memory along the course of schizophrenia and bipolar disorder: a new perspective. Eur Neuropsychopharmacol 25(2):169–175

    Article  CAS  PubMed  Google Scholar 

  48. Brazo P, Ilongo M, Dollfus S (2013) Distinct episodic verbal memory profiles in schizophrenia. Behav Sci (Basel) 3(2):192–205

    Article  Google Scholar 

  49. Picchioni MM, Murray RM (2007) Schizophrenia. BMJ 335(7610):91–95

    Article  PubMed  PubMed Central  Google Scholar 

  50. Leung A, Chue P (2000) Sex differences in schizophrenia, a review of the literature. Acta Psychiatr Scand Suppl 401:3–38

    Article  CAS  PubMed  Google Scholar 

  51. Häfner H (2003) Gender differences in schizophrenia. Psychoneuroendocrinology Suppl 2:17–54

    Article  Google Scholar 

  52. Hara Y, Waters EM, McEwen BS, Morrison JH (2015) Estrogen effects on cognitive and synaptic health over the Lifecourse. Physiol Rev 95(3):785–807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Davis J, Moylan S, Harvey BH, Maes M, Berk M (2014) Neuroprogression in schizophrenia: pathways underpinning clinical staging and therapeutic corollaries. Aust N Z J Psychiatry 48(6):512–529

    Article  PubMed  Google Scholar 

  54. Davis J, Eyre H, Jacka FN, Dodd S, Dean O, McEwen S, Debnath M, McGrath J et al (2016) A review of vulnerability and risks for schizophrenia: beyond the two hit hypothesis. Neurosci Biobehav Rev 65:185–194

    Article  PubMed  PubMed Central  Google Scholar 

  55. Smith RS, Maes M (1995) The macrophage-T-lymphocyte theory of schizophrenia: additional evidence. Med Hypotheses 45(2):135–141

    Article  CAS  PubMed  Google Scholar 

  56. Anderson G, Maes M (2013) Schizophrenia: linking prenatal infection to cytokines, the tryptophan catabolite (TRYCAT) pathway, NMDA receptor hypofunction, neurodevelopment and neuroprogression. Prog Neuro-Psychopharmacol Biol Psychiatry 42:5–19

    Article  CAS  Google Scholar 

  57. Zhao Q, Lv Y, Zhou Y, Hong Z, Guo Q (2012) Short-term delayed recall of auditory verbal learning test is equivalent to long-term delayed recall for identifying amnestic mild cognitive impairment. PLoS One 7(12):e51157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Bora E, Binnur Akdede B, Alptekin K (2017) Neurocognitive impairment in deficit and non-deficit schizophrenia: a meta-analysis. Psychol Med 4:1–14

    Google Scholar 

  59. Anderson G, Berk M, Dodd S, Bechter K, Altamura AC, Dell’osso B, Kanba S, Monji A et al (2013) Immuno-inflammatory, oxidative and nitrosative stress, and neuroprogressive pathways in the etiology, course and treatment of schizophrenia. Prog Neuro-Psychopharmacol Biol Psychiatry 42:1–4

    Article  CAS  Google Scholar 

  60. Dantas CR, Barros BR, Fernandes PT, Li LM, Banzato CE (2011) Insight controlled for cognition in deficit and nondeficit schizophrenia. Schizophr Res 128(1–3):124–126

    Article  PubMed  Google Scholar 

  61. Moritz S, Woodward TS, Rodriguez-Raecke R (2006) Patients with schizophrenia do not produce more false memories than controls but are more confident in them. Psychol Med 36:659–667

    Article  PubMed  Google Scholar 

  62. Bombin I, Mayoral M, Castro-Fornieles J, Gonzalez-Pinto A, de la Serna E, Rapado-Castro M, Barbeito S, Parellada M et al (2013) Neuropsychological evidence for abnormal neurodevelopment associated with early-onset psychoses. Psychol Med 43(4):757–768

    Article  CAS  PubMed  Google Scholar 

  63. Sewell RA, Perry EB Jr, Karper LP, Bell MD, Lysaker P, Goulet JL, Brenner L, Erdos J et al (2010) Clinical significance of neurological soft signs in schizophrenia: factor analysis of the neurological evaluation scale. Schizophr Res 124(1–3):1–12

    Article  PubMed  Google Scholar 

  64. Saleem MM, Harte MK, Marshall KM, Scally A, Brewin A, Neill JC (2013) First episode psychosis patients show impaired cognitive function—a study of a South Asian population in the UK. J Psychopharmacol 27(4):366–373

    Article  PubMed  Google Scholar 

  65. Eack SM, Mesholam-Gately RI, Greenwald DP, Hogarty SS, Keshavan MS (2013) Negative symptom improvement during cognitive rehabilitation: results from a 2-year trial of cognitive enhancement therapy. Psychiatry Res 209(1):21–26

    Article  PubMed  PubMed Central  Google Scholar 

  66. Sanchez AH, Lavaysse LM, Starr JN, Gard DE (2014) Daily life evidence of environment-incongruent emotion in schizophrenia. Psychiatry Res 220(1–2):89–95

    Article  PubMed  PubMed Central  Google Scholar 

  67. O’Leary DS, Flaum M, Kesler ML, Flashman LA, Arndt S, Andreasen NC (2000) Cognitive correlates of the negative, disorganized, and psychotic symptom dimensions of schizophrenia. J Neuropsychiatry Clin Neurosci 12(1):4–15

    Article  PubMed  Google Scholar 

  68. Iaccarino HF, Suckow RF, Xie S, Bucci DJ (2013) The effect of transient increases in kynurenic acid and quinolinic acid levels early in life on behavior in adulthood: implications for schizophrenia. Schizophr Res 150(2–3):392–397

    Article  PubMed  Google Scholar 

  69. Maes M, Mihaylova I, Ruyter MD, Kubera M, Bosmans E (2007) The immune effects of TRYCATs (tryptophan catabolites along the IDO pathway): relevance for depression—and other conditions characterized by tryptophan depletion induced by inflammation. Neuro Endocrinol Lett 28(6):826–831

    CAS  PubMed  Google Scholar 

  70. Lugo-Huitrón R, Blanco-Ayala T, Ugalde-Muñiz P, Carrillo-Mora P, Pedraza-Chaverrí J, Silva-Adaya D, Maldonado PD, Torres I et al (2011) On the antioxidant properties of kynurenic acid: free radical scavenging activity and inhibition of oxidative stress. Neurotoxicol Teratol 33:538–547

    Article  PubMed  Google Scholar 

  71. Koola MM (2016) Kynurenine pathway and cognitive impairments in schizophrenia: pharmacogenetics of galantamine and memantine. Schizophr Res Cogn 4:4–9

    Article  PubMed  PubMed Central  Google Scholar 

  72. Anderson G, Maes M (2017) The interactions of tryptophan and its catabolites with melatonin and the alpha 7 nicotinic receptor in CNS and psychiatric disorders: role for the aryl hydrocarbon receptor and direct mitochondria regulation. Int J Tryptophan Res 2017:1–8

    Google Scholar 

  73. Okusaga O, Fuchs D, Reeves G, Giegling I, Hartmann AM, Konte B, Friedl M, Groer M et al (2017) Kynurenine and tryptophan levels in patients with schizophrenia with elevated antigliadin immunoglobulin G antibodies. Psychosom Med 78(8):931–939

  74. Kita T, Morrison PF, Heyes MP, Markey SP (2002) Effects of systemic and central nervous system localized inflammation on the contributions of metabolic precursors to the l-kynurenine and quinolinic acid pools in brain. J Neurochem 82:258–268

    Article  CAS  PubMed  Google Scholar 

  75. Anderson G, Maes M (2015) The gut-brain axis: the role of melatonin in linking psychiatric, inflammatory and neurodegenerative conditions. Adv Integrative Med 2(1):31–37

    Article  Google Scholar 

  76. Stone TW, Darlington LG (2013) The kynurenine pathway as a therapeutic target in cognitive and neurodegenerative disorders. Br J Pharmacol 169(6):1211–1227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Pocivavsek A, Thomas MA, Elmer GI, Bruno JP, Schwarcz R (2014) Continuous kynurenine administration during the prenatal period, but not during adolescence, causes learning and memory deficits in adult rats. Psychopharmacology 231(14):2799–2809

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Baran H, Jellinger K, Deecke L (1999) Kynurenine metabolism in Alzheimer’s disease. J Neural Transm (Vienna) 106(2):165–181

    Article  CAS  Google Scholar 

  79. Hlinák Z, Krejci I (1995) Kynurenic acid and 5,7-dichlorokynurenic acids improve social and object recognition in male rats. Psychopharmacology 120(4):463–469

    Article  PubMed  Google Scholar 

  80. Savvateeva E, Popov A, Kamyshev N, Bragina J, Heisenberg M, Senitz D, Kornhuber J, Riederer P (2000) Age-dependent memory loss, synaptic pathology and altered brain plasticity in the Drosophila mutant cardinal accumulating 3-hydroxykynurenine. J Neural Transm (Vienna) 107(5):581–601

    Article  CAS  Google Scholar 

  81. Forrest CM, Mackay GM, Oxford L, Millar K, Darlington LG, Higgins MJ, Stone TW (2011) Kynurenine metabolism predicts cognitive function in patients following cardiac bypass and thoracic surgery. J Neurochem 119(1):136–152

    Article  CAS  PubMed  Google Scholar 

  82. Fazio F, Lionetto L, Curto M, Iacovelli L, Cavallari M, Zappulla C, Ulivieri M, Napoletano F et al (2015) Xanthurenic acid activates mGlu2/3 metabotropic glutamate receptors and is a potential trait marker for schizophrenia. Sci Rep 5:17799

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Marek GJ, Wright RA, Schoepp DD, Monn JA, Aghajanian GK (2000) Physiological antagonism between 5-hydroxytryptamine(2A) and group II metabotropic glutamate receptors in prefrontal cortex. J Pharmacol Exp Ther 292:76–87

    CAS  PubMed  Google Scholar 

  84. Latif-Hernandez A, Shah D, Ahmed T, Lo AC, Callaerts-Vegh Z, Van der Linden A, Balschun D, D’Hooge R (2016) Quinolinic acid injection in mouse medial prefrontal cortex affects reversal learning abilities, cortical connectivity and hippocampal synaptic plasticity. Sci Rep 6:36489

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Zhou L, Chen P, Peng Y, Ouyang R (2016) Role of oxidative stress in the neurocognitive dysfunction of obstructive sleep apnea syndrome. Oxidative Med Cell Longev 2016:9626831

    Google Scholar 

  86. Simen AA, Bordner KA, Martin MP, Moy LA, Barry LC (2011) Cognitive dysfunction with aging and the role of inflammation. Ther Adv Chronic Dis 2(3):175–195

    Article  PubMed  PubMed Central  Google Scholar 

  87. Choi DY, Lee JW, Lin G, Lee YK, Lee YH, Choi IS, Han SB, Jung JK et al (2012) Obovatol attenuates LPS-induced memory impairments in mice via inhibition of NF-κB signaling pathway. Neurochem Int 60(1):68–77

    Article  CAS  PubMed  Google Scholar 

  88. Raffard S, Gutierrez LA, Yazbek H, Larue A, Boulenger JP, Lançon C, Benoit M, Faget C et al (2016) Working memory deficit as a risk factor for severe apathy in schizophrenia: a 1-year longitudinal study. Schizophr Bull 42(3):642–651

    Article  PubMed  PubMed Central  Google Scholar 

  89. Kurtz MM, Moberg PJ, Mozley LH, Hickey T, Arnold SE, Bilker WB, Gur RE (2001) Cognitive impairment and functional status in elderly institutionalized patients with schizophrenia. Int J Geriatr Psychiatry 16(6):631–638

    Article  CAS  PubMed  Google Scholar 

  90. Lin CH, Huang CL, Chang YC, Chen PW, Lin CY, Tsai GE, Lane HY (2013) Clinical symptoms, mainly negative symptoms, mediate the influence of neurocognition and social cognition on functional outcome of schizophrenia. Schizophr Res 146(1–3):231–237

    Article  PubMed  Google Scholar 

  91. McGurk SR, Moriarty PJ, Harvey PD, Parrella M, White L, Friedman J, Davis KL (2000) Relationship of cognitive functioning, adaptive life skills, and negative symptom severity in poor-outcome geriatric schizophrenia patients. J Neuropsychiatry Clin Neurosci 12(2):257–264

    Article  CAS  PubMed  Google Scholar 

  92. Nuechterlein KH, Green MF, Kern RS, Baade LE, Barch DM, Cohen JD, Essock S et al (2008) The MATRICS consensus cognitive battery, part 1: test selection, reliability, and validity. Am J Psychiatry 165(2):203–213

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This research has been supported by the Asahi Glass Foundation, Chulalongkorn University Centenary Academic Development Project, and IDRPHT and GEMAC, France.

Author information

Authors and Affiliations

Authors

Contributions

All the contributing authors have participated in the manuscript. MM and BK designed the study. BK recruited patients and completed rating scales and diagnostic interviews. ST performed the CERAD measurements. SS performed the TRYCAT assays. MM carried out the statistical analyses. All authors contributed to interpretation of the data and writing of the manuscript.

Corresponding author

Correspondence to Michael Maes.

Ethics declarations

Conflict of Interest

The authors have no conflict of interest with any commercial or other association in connection with the submitted article.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kanchanatawan, B., Hemrungrojn, S., Thika, S. et al. Changes in Tryptophan Catabolite (TRYCAT) Pathway Patterning Are Associated with Mild Impairments in Declarative Memory in Schizophrenia and Deficits in Semantic and Episodic Memory Coupled with Increased False-Memory Creation in Deficit Schizophrenia. Mol Neurobiol 55, 5184–5201 (2018). https://doi.org/10.1007/s12035-017-0751-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12035-017-0751-8

Keywords

Navigation