Glutamatergic hypo-function in the left superior and middle temporal gyri in early schizophrenia: a data-driven three-dimensional proton spectroscopic imaging study.


Journal

Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology
ISSN: 1740-634X
Titre abrégé: Neuropsychopharmacology
Pays: England
ID NLM: 8904907

Informations de publication

Date de publication:
10 2020
Historique:
received: 06 03 2020
accepted: 06 05 2020
revised: 23 04 2020
pubmed: 14 5 2020
medline: 24 6 2021
entrez: 14 5 2020
Statut: ppublish

Résumé

Proton magnetic resonance spectroscopy (

Identifiants

pubmed: 32403117
doi: 10.1038/s41386-020-0707-y
pii: 10.1038/s41386-020-0707-y
pmc: PMC7608301
doi:

Substances chimiques

Protons 0
Glutamine 0RH81L854J
Aspartic Acid 30KYC7MIAI
Glutamic Acid 3KX376GY7L
Creatine MU72812GK0

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

1851-1859

Subventions

Organisme : U.S. Department of Health & Human Services | NIH | National Center for Research Resources (NCRR)
ID : P20 RR021938-01A1
Pays : International
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Mental Health (NIMH)
ID : R01MH084898
Pays : International
Organisme : U.S. Department of Health & Human Services | NIH | National Center for Research Resources (NCRR)
ID : R01 EB01606
Pays : International
Organisme : U.S. Department of Health & Human Services | NIH | National Center for Research Resources (NCRR)
ID : 3 UL1 RR031977-02S2
Pays : International
Organisme : NIMH NIH HHS
ID : R01 MH084898
Pays : United States

Références

Moghaddam B, Javitt D. From revolution to evolution: the glutamate hypothesis of schizophrenia and its implication for treatment. Neuropsychopharmacology. 2012;37:4–15.
pubmed: 21956446 doi: 10.1038/npp.2011.181
Olabi B, Ellison-Wright I, McIntosh AM, Wood SJ, Bullmore E, Lawrie SM. Are there progressive brain changes in schizophrenia? A meta-analysis of structural magnetic resonance imaging studies. Biol Psychiatry. 2011;70:88–96.
pubmed: 21457946 doi: 10.1016/j.biopsych.2011.01.032
Marsman A, van den Heuvel MP, Klomp DW, Kahn RS, Luijten PR, Hulshoff Pol HE. Glutamate in schizophrenia: a focused review and meta-analysis of (1)H-MRS studies. Schizophr Bull. 2013;39:120–9.
pubmed: 21746807 doi: 10.1093/schbul/sbr069
Merritt K, Egerton A, Kempton MJ, Taylor MJ, McGuire PK. Nature of glutamate alterations in schizophrenia: a meta-analysis of proton magnetic resonance spectroscopy Studies. JAMA Psychiatry. 2016;73:665–74.
pubmed: 27304221 doi: 10.1001/jamapsychiatry.2016.0442
Iwata Y, Nakajima S, Plitman E, Mihashi Y, Caravaggio F, Chung JK, et al. Neurometabolite levels in antipsychotic-naive/free patients with schizophrenia: a systematic review and meta-analysis of (1)H-MRS studies. Prog Neuropsychopharmacol Biol Psychiatry. 2018;86:340–52.
pubmed: 29580804 doi: 10.1016/j.pnpbp.2018.03.016
Bustillo JR, Jones T, Chen H, Lemke N, Abbott C, Qualls C, et al. Glutamatergic and neuronal dysfunction in gray and white matter: a spectroscopic imaging study in a large schizophrenia sample. Schizophr Bull. 2016;43:611–19.
pmcid: 5473520
de la Fuente-Sandoval C, Leon-Ortiz P, Azcarraga M, Stephano S, Favila R, Diaz-Galvis L, et al. Glutamate levels in the associative striatum before and after 4 weeks of antipsychotic treatment in first-episode psychosis: a longitudinal proton magnetic resonance spectroscopy study. JAMA Psychiatry. 2013;70:1057–66.
pubmed: 23966023 pmcid: 3790718 doi: 10.1001/jamapsychiatry.2013.289
Buchanan RW, Davis M, Goff D, Green MF, Keefe RS, Leon AC, et al. A summary of the FDA-NIMH-MATRICS workshop on clinical trial design for neurocognitive drugs for schizophrenia. Schizophr Bull. 2005;31:5–19.
pubmed: 15888422 doi: 10.1093/schbul/sbi020
Kay SR, Fiszbein A, Opler LA. The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr Bull. 1987;13:261–76.
pubmed: 3616518 doi: 10.1093/schbul/13.2.261
Goryawala MZ, Sheriff S, Maudsley AA. Regional distributions of brain glutamate and glutamine in normal subjects. NMR Biomed. 2016;29:1108–16.
pubmed: 27351339 pmcid: 4962701 doi: 10.1002/nbm.3575
Maudsley AA, Domenig C, Govind V, Darkazanli A, Studholme C, Arheart K, et al. Mapping of brain metabolite distributions by volumetric proton MR spectroscopic imaging (MRSI). Magn Reson Med. 2009;61:548–59.
pubmed: 19111009 pmcid: 2724718 doi: 10.1002/mrm.21875
Cox RW. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res. 1996;29:162–73.
pubmed: 8812068 doi: 10.1006/cbmr.1996.0014
Vaden KI Jr., Gebregziabher M, Kuchinsky SE, Eckert MA. Multiple imputation of missing fMRI data in whole brain analysis. Neuroimage. 2012;60:1843–55.
pubmed: 22500925 doi: 10.1016/j.neuroimage.2012.01.123
Maudsley AA, Darkazanli A, Alger JR, Hall LO, Schuff N, Studholme C, et al. Comprehensive processing, display and analysis for in vivo MR spectroscopic imaging. NMR Biomed. 2006;19:492–503.
pubmed: 16763967 pmcid: 2673915 doi: 10.1002/nbm.1025
Ebel A, Maudsley AA. Improved spectral quality for 3D MR spectroscopic imaging using a high spatial resolution acquisition strategy. Magn Reson imaging. 2003;21:113–20.
pubmed: 12670597 doi: 10.1016/S0730-725X(02)00645-8
Goryawala M SM, Maudsley AA. Effects of Apodization smoothing and denoising on spectral fitting. Magn Reson Med. 2020;20:108–14.
Soher BJ, Young K, Govindaraju V, Maudsley AA. Automated spectral analysis III: application to in vivo proton MR spectroscopy and spectroscopic imaging. Magn Reson Med. 1998;40:822–31.
pubmed: 9840826 doi: 10.1002/mrm.1910400607
Zhang Y, Taub E, Salibi N, Uswatte G, Maudsley AA, Sheriff S, et al. Comparison of reproducibility of single voxel spectroscopy and whole-brain magnetic resonance spectroscopy imaging at 3T. NMR Biomed. 2018;31:e3898.
pubmed: 29436038 pmcid: 6291009 doi: 10.1002/nbm.3898
Rubin LH, Witkiewitz K, Andre JS, Reilly S. Methods for handling missing data in the behavioral neurosciences: don’t throw the baby rat out with the bath water. J Undergrad Neurosci Educ. 2007;5:A71–7.
pubmed: 23493038 pmcid: 3592650
Cox RW, Chen G, Glen DR, Reynolds RC, Taylor PA. FMRI clustering in AFNI: false-positive rates redux. Brain Connect. 2017;7:152–71.
pubmed: 28398812 pmcid: 5399747 doi: 10.1089/brain.2016.0475
Atagun MI, Sikoglu EM, Can SS, Karakas-Ugurlu G, Ulusoy-Kaymak S, Caykoylu A, et al. Investigation of Heschl’s gyrus and planum temporale in patients with schizophrenia and bipolar disorder: a proton magnetic resonance spectroscopy study. Schizophr Res. 2015;161:202–9.
pubmed: 25480359 doi: 10.1016/j.schres.2014.11.012
Seese RR, O’Neill J, Hudkins M, Siddarth P, Levitt J, Tseng B, et al. Proton magnetic resonance spectroscopy and thought disorder in childhood schizophrenia. Schizophr Res. 2011;133:82–90.
pubmed: 21872444 pmcid: 3229835 doi: 10.1016/j.schres.2011.07.011
Takahashi T, Wood SJ, Yung AR, Soulsby B, McGorry PD, Suzuki M, et al. Progressive gray matter reduction of the superior temporal gyrus during transition to psychosis. Arch Gen Psychiatry. 2009;66:366–76.
pubmed: 19349306 doi: 10.1001/archgenpsychiatry.2009.12
Javitt DC, Steinschneider M, Schroeder CE, Arezzo JC. Role of cortical N-methyl-D-aspartate receptors in auditory sensory memory and mismatch negativity generation: implications for schizophrenia. Proc Natl Acad Sci USA. 1996;93:11962–7.
pubmed: 8876245 doi: 10.1073/pnas.93.21.11962 pmcid: 38166
Javitt DC, Sweet RA. Auditory dysfunction in schizophrenia: integrating clinical and basic features. Nat Rev Neurosci. 2015;16:535–50.
pubmed: 26289573 pmcid: 4692466 doi: 10.1038/nrn4002
Stone JM, Dietrich C, Edden R, Mehta MA, De Simoni S, Reed LJ, et al. Ketamine effects on brain GABA and glutamate levels with 1H-MRS: relationship to ketamine-induced psychopathology. Mol Psychiatry. 2012;17:664–5.
pubmed: 22212598 doi: 10.1038/mp.2011.171
Bustillo J, Galloway MP, Ghoddoussi F, Bolognani F, Perrone-Bizzozero N. Medial-frontal cortex hypometabolism in chronic phencyclidine exposed rats assessed by high resolution magic angle spin 11.7T proton magnetic resonance spectroscopy. Neurochemistry Int. 2012;61:128–31.
doi: 10.1016/j.neuint.2012.04.003
Wada A, Kunii Y, Matsumoto J, Hino M, Yang Q, Niwa SI, et al. Prominent increased calcineurin immunoreactivity in the superior temporal gyrus in schizophrenia: A postmortem study. Psychiatry Res. 2017;247:79–83.
pubmed: 27871031 doi: 10.1016/j.psychres.2016.11.018
Nucifora LG, MacDonald ML, Lee BJ, Peters ME, Norris AL, Orsburn BC, et al. Increased protein insolubility in brains from a subset of patients with schizophrenia. Am J Psychiatry. 2019;176:730–43.
pubmed: 31055969 doi: 10.1176/appi.ajp.2019.18070864
MacDonald ML, Garver M, Newman J, Sun Z, Kannarkat J, Salisbury R, et al. Synaptic proteome alterations in the primary auditory cortex of individuals with schizophrenia. JAMA Psychiatry. 2019:77;1–10.
Glantz LA, Lewis DA. Decreased dendritic spine density on prefrontal cortical pyramidal neurons in schizophrenia. Arch Gen Psychiatry. 2000;57:65–73.
doi: 10.1001/archpsyc.57.1.65 pubmed: 10632234
Ongur D, Prescot AP, Jensen JE, Cohen BM, Renshaw PF. Creatine abnormalities in schizophrenia and bipolar disorder. Psychiatry Res. 2009;172:44–8.
pubmed: 19239984 pmcid: 2729651 doi: 10.1016/j.pscychresns.2008.06.002
Tibbo PG, Bernier D, Hanstock CC, Seres P, Lakusta B, Purdon SE. 3-T proton magnetic spectroscopy in unmedicated first episode psychosis: a focus on creatine. Magn Reson Med. 2013;69:613–20.
pubmed: 22511463 doi: 10.1002/mrm.24291
Kraguljac NV, Reid M, White D, Jones R, den Hollander J, Lowman D, et al. Neurometabolites in schizophrenia and bipolar disorder - a systematic review and meta-analysis. Psychiatry Res. 2012;203:111–25.
pubmed: 22981426 pmcid: 3466386 doi: 10.1016/j.pscychresns.2012.02.003
Meyer EJ, Kirov II, Tal A, Davitz MS, Babb JS, Lazar M, et al. Metabolic abnormalities in the hippocampus of patients with schizophrenia: A 3D multivoxel MR spectroscopic imaging study at 3T. AJNR Am J Neuroradiol. 2016;37:2273–9.
pubmed: 27444940 pmcid: 5161606 doi: 10.3174/ajnr.A4886
Lahti AC, Holcomb HH, Weiler MA, Medoff DR, Tamminga CA. Functional effects of antipsychotic drugs: comparing clozapine with haloperidol. Biol Psychiatry. 2003;53:601–8.
pubmed: 12679238 doi: 10.1016/S0006-3223(02)01602-5
Lahti AC, Weiler MA, Medoff DR, Tamminga CA, Holcomb HH. Functional effects of single dose first- and second-generation antipsychotic administration in subjects with schizophrenia. Psychiatry Res 2005;139:19–30.
pubmed: 15950442 doi: 10.1016/j.pscychresns.2005.02.006
Du F, Cooper AJ, Thida T, Sehovic S, Lukas SE, Cohen BM, et al. In vivo evidence for cerebral bioenergetic abnormalities in schizophrenia measured using 31P magnetization transfer spectroscopy. JAMA Psychiatry. 2014;71:19–27.
pubmed: 24196348 pmcid: 7461723 doi: 10.1001/jamapsychiatry.2013.2287
Das TK, Dey A, Sabesan P, Javadzadeh A, Theberge J, Radua J, et al. Putative astroglial dysfunction in schizophrenia: a meta-analysis of (1)H-MRS studies of medial prefrontal myo-inositol. Front Psychiatry. 2018;9:438.
pubmed: 30298023 pmcid: 6160540 doi: 10.3389/fpsyt.2018.00438
Wang AM, Pradhan S, Coughlin JM, Trivedi A, DuBois SL, Crawford JL, et al. Assessing brain metabolism with 7-T proton magnetic resonance spectroscopy in patients with first-episode psychosis. JAMA Psychiatry. 2019;76:314–23.
pubmed: 30624573 pmcid: 6439827 doi: 10.1001/jamapsychiatry.2018.3637
Reid MA, Salibi N, White DM, Gawne TJ, Denney TS, Lahti AC. 7T Proton magnetic resonance spectroscopy of the anterior cingulate cortex in first-episode schizophrenia. Schizophr Bull. 2019;45:180–9.
pubmed: 29385594 doi: 10.1093/schbul/sbx190
Lim KO, Adalsteinsson E, Spielman D, Sullivan EV, Rosenbloom MJ, Pfefferbaum A. Proton magnetic resonance spectroscopic imaging of cortical gray and white matter in schizophrenia. Arch Gen Psychiatry. 1998;55:346–52.
pubmed: 9554430 doi: 10.1001/archpsyc.55.4.346
Bertolino A, Nawroz S, Mattay VS, Barnett AS, Duyn JH, Moonen CT, et al. Regionally specific pattern of neurochemical pathology in schizophrenia as assessed by multislice proton magnetic resonance spectroscopic imaging. Am J Psychiatry. 1996;153:1554–63.
pubmed: 8942451 doi: 10.1176/ajp.153.12.1554
Haijma SV, Van Haren N, Cahn W, Koolschijn PC, Hulshoff Pol HE, Kahn RS. Brain volumes in schizophrenia: a meta-analysis in over 18 000 subjects. Schizophr Bull. 2013;39:1129–38.
pubmed: 23042112 doi: 10.1093/schbul/sbs118
Glasser MF, Coalson TS, Robinson EC, Hacker CD, Harwell J, Yacoub E, et al. A multi-modal parcellation of human cerebral cortex. Nature. 2016;536:171–8.
pubmed: 27437579 pmcid: 4990127 doi: 10.1038/nature18933
Kegeles LS, Mao X, Stanford AD, Girgis R, Ojeil N, Xu X, et al. Elevated prefrontal cortex gamma-aminobutyric acid and glutamate-glutamine levels in schizophrenia measured in vivo with proton magnetic resonance spectroscopy. Arch Gen Psychiatry. 2012;69:449–59.
pubmed: 22213769 doi: 10.1001/archgenpsychiatry.2011.1519
Gardner DM, Murphy AL, O’Donnell H, Centorrino F, Baldessarini RJ. International consensus study of antipsychotic dosing. Am J Psychiatry. 2010;167:686–93.
pubmed: 20360319 doi: 10.1176/appi.ajp.2009.09060802

Auteurs

Juan R Bustillo (JR)

Departments of Psychiatry, University of New Mexico, Albuquerque, NM, 87131-0001, USA. jbustillo@salud.unm.edu.
Department of Neurosciences, University of New Mexico, Albuquerque, NM, USA. jbustillo@salud.unm.edu.

Joel Upston (J)

Departments of Psychiatry, University of New Mexico, Albuquerque, NM, 87131-0001, USA.
Department Mathematics & Statistics, University of New Mexico, Albuquerque, NM, USA.

Elizabeth Grace Mayer (EG)

Departments of Psychiatry, University of New Mexico, Albuquerque, NM, 87131-0001, USA.
Department Mathematics & Statistics, University of New Mexico, Albuquerque, NM, USA.

Thomas Jones (T)

Departments of Psychiatry, University of New Mexico, Albuquerque, NM, 87131-0001, USA.

Andrew A Maudsley (AA)

Department of Radiology, University of Miami, FL, NM, USA.

Charles Gasparovic (C)

Mind Research Network, Albuquerque, NM, USA.

Mauricio Tohen (M)

Departments of Psychiatry, University of New Mexico, Albuquerque, NM, 87131-0001, USA.

Rhoshel Lenroot (R)

Departments of Psychiatry, University of New Mexico, Albuquerque, NM, 87131-0001, USA.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH