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Original Investigations

Basal glutamate in the hippocampus and the dorsolateral prefrontal cortex in schizophrenia: Relationships to cognitive proficiency investigated with structural equation modelling

ORCID Icon, , , , , , , , & show all
Pages 730-740 | Received 17 Oct 2022, Accepted 28 Mar 2023, Published online: 24 Apr 2023

References

  • [APA] American Psychiatric Association. 2013. Diagnostic and statistical manual of mental disorders. 5th ed. Washington, DC: APA.
  • [WHO] World Health Organization. 2002. Global burden of disease. Geneva: World Health Organization.
  • Abbott C, Bustillo J. 2006. What have we learned from proton magnetic resonance spectroscopy about schizophrenia? A critical update. Curr Opin Psychiatry. 19(2):135–139.
  • Aleman A, Hijman R, de Haan EH, Kahn RS. 1999. Memory impairment in schizophrenia: a meta-analysis. Am J Psychiatry. 156(9):1358–1366. eng.le
  • Bartha R, Williamson PC, Drost DJ, Malla AK, Neufeld RW. 1999. Medial prefrontal glutamine and dreaming. Br J Psychiatry. 175:288–289. English.
  • Benes FM. 2000. Emerging principles of altered neural circuitry in schizophrenia. Brain Res Brain Res Rev. 31(2–3):251–269.
  • Brambilla P, Riva MA, Melcangi R, Diwadkar VA. 2007. The role of glutamatergic pathways in schizophrenia: from animal models to human imaging studies. Clinical Neuropsychiatry. 4:199–207.
  • Carlsson A. 2006. The neurochemical circuitry of schizophrenia. Pharmacopsychiatry. 39 Suppl 1:S10–S14. eng.
  • Carter CS, MacDonald AW, Ross LL, Stenger VA. 2001. Anterior cingulate cortex activity and impaired self-monitoring of performance in patients with schizophrenia: an event-related fMRI study. Am J Psychiatry. 158(9):1423–1428.
  • Castner SA, Williams GV. 2007. Tuning the engine of cognition: a focus on NMDA/D1 receptor interactions in prefrontal cortex. Brain Cogn. 63(2):94–122. eng.
  • Coupland NJ, Ogilvie CJ, Hegadoren KM, Seres P, Hanstock CC, Allen PS. 2005. Decreased prefrontal myo-inositol in major depressive disorder. Biol Psychiatry. 57(12):1526–1534. eng.
  • Das TK, Dey A, Sabesan P, Javadzadeh A, Theberge J, Radua J, Palaniyappan L. 2018. Putative astroglial dysfunction in schizophrenia: a meta-analysis of (1)H-MRS studies of medial prefrontal myo-inositol. Front Psychiatry. 9:438. eng.
  • Diwadkar VA. 2012. Adolescent risk pathways toward schizophrenia: sustained attention and the brain. Curr Top Med Chem. 12(21):2339–2347.
  • Diwadkar VA, Bakshi N, Gupta G, Pruitt P, White R, Eickhoff SB. 2014. Dysfunction and dysconnection in cortical-striatal networks during sustained attention: genetic risk for schizophrenia or bipolar disorder and its impact on brain network function. Front Psychiatry. 5:50.
  • Diwadkar VA, Bustamante A, Rai H, Uddin M. 2014. Epigenetics, stress, and their potential impact on brain network function: a focus on the schizophrenia diatheses. Front Psychiatry. 5:71.
  • Eichenbaum H. 2017. Prefrontal–hippocampal interactions in episodic memory. Nat Rev Neurosci. 18(9):547–558.
  • Gasparovic C, Song T, Devier D, Bockholt HJ, Caprihan A, Mullins PG, Posse S, Jung RE, Morrison LA. 2006. Use of tissue water as a concentration reference for proton spectroscopic imaging. Magn Reson Med. 55(6):1219–1226.
  • Godlewska BR, Minichino A, Emir U, Angelescu I, Lennox B, Micunovic M, Howes O, Cowen PJ. 2021. Brain glutamate concentration in men with early psychosis: a magnetic resonance spectroscopy case-control study at 7 T. Transl Psychiatry. 11(1):367. eng.
  • Gold JM, Harvey PD. 1993. Cognitive deficits in schizophrenia. Psychiatr Clin North Am. 16(2):295–312. eng.
  • Hayes AF, Scharkow M. 2013. The relative trustworthiness of inferential tests of the indirect effect in statistical mediation analysis: does method really matter? Psychol Sci. 24(10):1918–1927.
  • Heinrichs RW, Zakzanis KK. 1998. Neurocognitive deficit in schizophrenia: a quantitative review of the evidence. Neuropsychology. 12(3):426–445. eng.
  • Insel TR. 2010. Rethinking schizophrenia. Nature. 468(7321):187–193.
  • Isaacson JS, Scanziani M. 2011. How inhibition shapes cortical activity. Neuron. 72(2):231–243. English.
  • Jansma JM, Ramsey NF, van der Wee NJ, Kahn RS. 2004. Working memory capacity in schizophrenia: a parametric fMRI study. Schizophr Res. 68(2–3):159–171.
  • Jeon P, Mackinley M, Theberge J, Palaniyappan L. 2021. The trajectory of putative astroglial dysfunction in first episode schizophrenia: a longitudinal 7-Tesla MRS study. Sci Rep. 11(1):22333. eng.
  • Kay SR, Fiszbein A, Opler LA. 1987. The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr Bull. 13(2):261–276.
  • Keshavan MS, Stanley JA, Pettegrew JW. 2000. Magnetic resonance spectroscopy in schizophrenia: methodogical issues and findings-Part II. Biol Psychiatry. 48(5):369–380.
  • Kessler RC, Chiu WT, Demler O, Merikangas KR, Walters EE. 2005. Prevalence, severity, and comorbidity of 12-month DSM-IV disorders in the National Comorbidity Survey Replication. Arch Gen Psychiatry. 62(6):617–627.
  • Kim H, McGrath BM, Silverstone PH. 2005. A review of the possible relevance of inositol and the phosphatidylinositol second messenger system (PI-cycle) to psychiatric disorders–focus on magnetic resonance spectroscopy (MRS) studies. Hum Psychopharmacol. 20(5):309–326. eng.
  • Lauritzen M, Mathiesen C, Schaefer K, Thomsen KJ. 2012. Neuronal inhibition and excitation, and the dichotomic control of brain hemodynamic and oxygen responses. NeuroImage. 62(2):1040–1050. English.
  • Little TD, Jorgensen TD, Lang KM, Moore EW. 2014. On the joys of missing data. J Pediatr Psychol. 39(2):151–162.
  • Logothetis NK. 2008. What we can do and what we cannot do with fMRI. Nature. 453(7197):869–878. eng.
  • Lynn J, Woodcock EA, Anand C, Khatib D, Stanley JA. 2018. Differences in steady-state glutamate levels and variability between ‘non-task-active’ control conditions: evidence from 1H fMRS of the prefrontal cortex. Neuroimage. 172:554–561.
  • Maddock RJ, Buonocore MH. 2012. MR spectroscopic studies of the brain in psychiatric disorders. Curr Top Behav Neurosci. 11:199–251. eng.
  • Marsman A, van den Heuvel MP, Klomp D, Kahn RS, Luijten PR, Hulshoff Pol HE. 2013. Glutamate in schizophrenia: a focused review and meta-analysis of 1H-MRS studies. Schizophr Bull. 39:120–129.
  • Merritt K, Egerton A, Kempton MJ, Taylor MJ, McGuire PK. 2016. Nature of glutamate alterations in schizophrenia: a meta-analysis of proton magnetic resonance spectroscopy studies. JAMA Psychiatry. 73(7):665–674. eng.
  • Merritt K, McGuire PK, Egerton A, Aleman A, Block W, Bloemen OJN, Borgan F, Bustillo JR, Capizzano AA, Coughlin JM, et al. 2021. Association of age, antipsychotic medication, and symptom severity in schizophrenia with proton magnetic resonance spectroscopy brain glutamate level. JAMA Psychiatry. 78(6):667.
  • Olbrich HM, Valerius G, Rüsch N, Büchert M, Thiel T, Hennig J, Ebert D, Van Elst LT. 2008. Frontolimbic glutamate alterations in first episode schizophrenia: evidence from a magnetic resonance spectroscopy study. World J Biol Psychiatry. 9(1):59–63. English.
  • Posse S, Otazo R, Caprihan A, Bustillo J, Chen H, Henry P-G, Marjanska M, Gasparovic C, Zuo C, Magnotta V, et al. 2007. Proton echo-planar spectroscopic imaging of J-coupled resonances in human brain at 3 and 4 tesla. Magn Reson Med. 58(2):236–244. English.
  • Pouwels PJ, Frahm J. 1998. Regional metabolite concentrations in human brain as determined by quantitative localized proton MRS. Magn Reson Med. 39(1):53–60.
  • Provencher SW. 1993. Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn Reson Med. 30(6):672–679.
  • Psychological Corporation. 1999. Wechsler abbreviated Scale of Intelligence (WASI) manual. San Antonio (TX): Author.
  • Reddy-Thootkur M, Kraguljac NV, Lahti AC. 2020. The role of glutamate and GABA in cognitive dysfunction in schizophrenia and mood disorders - a systematic review of magnetic resonance spectroscopy studies. Schizophr Res. 249:74–84. eng.
  • Rosoklija G, Toomayan G, Ellis SP, Keilp J, Mann JJ, Latov N, Hays AP, Dwork AJ. 2000. Structural abnormalities of subicular dendrites in subjects with schizophrenia and mood disorders: preliminary findings. Arch Gen Psychiatry. 57(4):349–356. eng.
  • Ross B, Bluml S. 2001. Magnetic resonance spectroscopy of the human brain. Anat Rec. 265(2):54–84.
  • Rusch N, Tebartz van Elst L, Valerius G, Buchert M, Thiel T, Ebert D, Hennig J, Olbrich HM. 2008. Neurochemical and structural correlates of executive dysfunction in schizophrenia. Schizophr Res. 99(1–3):155–163. eng.
  • Salthouse TA, Mitchell DR, Skovronek E, Babcock RL. 1989. Effects of adult age and working memory on reasoning and spatial abilities. J Exp Psychol Learn Mem Cogn. 15(3):507–516. English.
  • Schmiedek F, Lövdén M, Lindenberger U. 2010. Hundred days of cognitive training enhance broad cognitive abilities in adulthood: findings from the COGITO study. Fronti Aging Neurosci. 2:27. English.
  • Singh S, Khushu S, Kumar P, Goyal S, Bhatia T, Deshpande SN. 2018. Evidence for regional hippocampal damage in patients with schizophrenia. Neuroradiology. 60(2):199–205. eng.
  • Smucny J, Carter CS, Maddock RJ. 2021. Medial prefrontal cortex glutamate is reduced in schizophrenia and moderated by measurement quality: a meta-analysis of 1H-MRS studies. Biol Psychiatry. 90(9):643–651.
  • Stan AD, Ghose S, Zhao C, Hulsey K, Mihalakos P, Yanagi M, Morris SU, Bartko JJ, Choi C, Tamminga CA. 2015. Magnetic resonance spectroscopy and tissue protein concentrations together suggest lower glutamate signaling in dentate gyrus in schizophrenia. Mol Psychiatry. 20(4):433–439. eng.
  • Stanley JA, Burgess A, Khatib D, Ramaseshan K, Arshad M, Wu H, Diwadkar V. 2017. Functional dynamics of hippocampal glutamate during associative learning assessed with in vivo 1H functional magnetic resonance spectroscopy. Neuroimage. 153:189–197.
  • Stanley JA, Raz N. 2018. Functional magnetic resonance spectroscopy: the “new” MRS for cognitive neuroscience and psychiatry research. Front Psychiatry. 9:76.
  • Steen RG, Hamer RM, Lieberman JA. 2005. Measurement of brain metabolites by 1H magnetic resonance spectroscopy in patients with schizophrenia: a systematic review and meta-analysis. Neuropsychopharmacology. 30(11):1949–1962.
  • Stephan KE, Baldeweg T, Friston KJ. 2006. Synaptic plasticity and dysconnection in schizophrenia. Biol Psychiatry. 59(10):929–939. eng.
  • Sullivan EV, Shear PK, Zipursky RB, Sagar HJ, Pfefferbaum A. 1994. A deficit profile of executive, memory, and motor functions in schizophrenia. Biol Psychiatry. 36(10):641–653.
  • Tan HY, Choo WC, Fones CS, Chee MW. 2005. fMRI study of maintenance and manipulation processes within working memory in first-episode schizophrenia. Am J Psychiatry. 162(10):1849–1858.
  • Tatti R, Haley MS, Swanson OK, Tselha T, Maffei A. 2017. Neurophysiology and regulation of the balance between excitation and inhibition in neocortical circuits. [review. Biol Psychiatry. 81(10):821–831. English.
  • The MRS package was developed by Edward J. Auerbach and Małgorzata Marjańska and provided by the University of Minnesota under a C2P agreement. https://www.cmrr.umn.edu/spectro/
  • Tkác I, Gruetter R. 2005. Methodology of 1H NMR spectroscopy of the human brain at very high magnetic fields. Appl Magn Reson. 29(1):139–157. English.
  • Toulopoulou T, Rabe-Hesketh S, King H, Murray RM, Morris RG. 2003. Episodic memory in schizophrenic patients and their relatives. Schizophr Res. 63(3):261–271.
  • van Elst LT, Valerius G, Büchert M, Thiel T, Rüsch N, Bubl E, Hennig J, Ebert D, Olbrich HM. 2005. Increased prefrontal and hippocampal glutamate concentration in schizophrenia: evidence from a magnetic resonance spectroscopy study. Biol Psychiatry. 58(9):724–730.
  • Wang AM, Pradhan S, Coughlin JM, Trivedi A, DuBois SL, Crawford JL, Sedlak TW, Nucifora FC Jr, Nestadt G, Nucifora LG, et al. 2019. Assessing brain metabolism with 7-T proton magnetic resonance spectroscopy in patients with first-episode psychosis. JAMA Psychiatry. 76(3):314–323. eng.
  • Wechsler D. 2009. WMS-IV: Wechsler memory scale-fourth edition. San Antonio (TX): Pearson.
  • Wijtenburg SA, Wang M, Korenic SA, Chen S, Barker PB, Rowland LM. 2021. Metabolite alterations in adults with schizophrenia, first degree relatives, and healthy controls: a multi-region 7T MRS study. Front Psychiatry. 12:656459. eng.
  • Woodcock EA, Arshad M, Khatib D, Stanley JA. 2018. Automated voxel placement: a linux-based suite of tools for accurate and reliable single voxel coregistration. J Neuroimaging Psychiatry Neurol. 3(1):1–8.
  • Woodcock RW, Johnson MB. 1989. Tests of psychoeducational achievement-revised. Allen (TX): DLM Teaching Resources.
  • Zhu G, Gheorghiu D, Allen PS. 1992. Motional degradation of metabolite signal strengths when using STEAM: a correction method. NMR Biomed. 5(4):209–211.

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