Abnormal Glutamatergic Neurotransmission and Neuronal-Glial Interactions in Acute Mania

Biological Psychiatry

Volumn 64, Issue 8, 2008, Pages 718-726

  Öngür, Dost ^a,b   Jensen, J Eric ^a,b   Prescot, Andrew P ^a,b   Stork, Caitlin ^c   Lundy, Miriam ^d   Cohen, Bruce M ^a,b   Renshaw, Perry F ^a,b  

^a MCLEAN HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^d YALE UNIVERSITY SCHOOL OF NURSING   (United States)

Author keywords

Bipolar disorder; glia; glutamate; glutamine; MRS; schizophrenia

Indexed keywords

ANTICONVULSIVE AGENT; ATYPICAL ANTIPSYCHOTIC AGENT; BENZODIAZEPINE DERIVATIVE; CHOLINE; CREATINE; GLUTAMIC ACID; GLUTAMINE; INOSITOL; LITHIUM; N ACETYLASPARTIC ACID; NEUROLEPTIC AGENT;

ACUTE PSYCHOSIS; ADULT; ARTICLE; BIPOLAR MANIA; BRAIN NERVE CELL; CELL INTERACTION; CINGULATE GYRUS; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GLIA CELL; GLUTAMATERGIC TRANSMISSION; HOSPITAL PATIENT; HUMAN; IMAGING SYSTEM; MALE; MENTAL PATIENT; NEUROIMAGING; NEUROTRANSMISSION; OCCIPITAL CORTEX; PARIETAL LOBE; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; SCHIZOPHRENIA;

ACUTE DISEASE; ADOLESCENT; ADULT; ASPARTIC ACID; BIPOLAR DISORDER; CASE-CONTROL STUDIES; CEREBRAL CORTEX; FEMALE; GLUTAMIC ACID; GLUTAMINE; GYRUS CINGULI; HUMANS; MAGNETIC RESONANCE IMAGING; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MATCHED-PAIR ANALYSIS; NEUROGLIA; NEURONS; NEUROTRANSMITTER AGENTS; OCCIPITAL LOBE; PARIETAL LOBE; PILOT PROJECTS; REFERENCE VALUES; SCHIZOPHRENIA; SYNAPTIC TRANSMISSION; YOUNG ADULT;

EID: 52949123611     PISSN: 00063223     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biopsych.2008.05.014     Document Type: Article

References (73)

1. Kessler R.C., Rubinow D.R., Holmes C., Abelson J.M., and Zhao S. The epidemiology of DSM-III-R bipolar I disorder in a general population survey. Psychol Med 27 (1997) 1079-1089
2. World Health Organization. Global Burden of Disease (2002), World Health Organization, Geneva
3. Öngür D., Drevets W.C., and Price J.L. Glial reduction in the subgenual prefrontal cortex in mood disorders. Proc Natl Acad Sci U S A 95 (1998) 13290-13295
4. Rajkowska G. Postmortem studies in mood disorders indicate altered numbers of neurons and glial cells. Biol Psychiatry 48 (2000) 766-777
5. Blumberg H.P., Krystal J.H., Bansal R., Martin A., Dziura J., Durkin K., et al. Age, rapid-cycling, and pharmacotherapy effects on ventral prefrontal cortex in bipolar disorder: A cross-sectional study. Biol Psychiatry 59 (2006) 611-618
6. Drevets W.C., Price J.L., Simpson J.R., Todd R.D., Reich T., Vannier M., et al. Subgenual prefrontal cortex abnormalities in mood disorders. Nature 386 (1997) 824-827
7. Drevets W.C. Neuroimaging studies of mood disorders. Biol Psychiatry 48 (2000) 813-829
8. Blumberg H.P., Leung H.C., Skudlarski P., Lacadie C.M., Fredericks C.A., Harris B.C., et al. A functional magnetic resonance imaging study of bipolar disorder: State- and trait-related dysfunction in ventral prefrontal cortices. Arch Gen Psychiatry 60 (2003) 601-609
9. Hattori E., Liu C., Badner J.A., Bonner T.I., Christian S.L., Maheshwari M., et al. Polymorphisms at the G72/G30 gene locus, on 13q33, are associated with bipolar disorder in two independent pedigree series. Am J Hum Genet 72 (2003) 1131-1140
10. Craddock N., O'Donovan M.C., and Owen M.J. The genetics of schizophrenia and bipolar disorder: Dissecting psychosis. J Med Genet 42 (2005) 193-204
11. Zarate Jr. C.A., Singh J., and Manji H.K. Cellular plasticity cascades: Targets for the development of novel therapeutics for bipolar disorder. Biol Psychiatry 59 (2006) 1006-1020
12. Rothman D.L., Behar K.L., Hyder F., and Shulman R.G. In vivo NMR studies of the glutamate neurotransmitter flux and neuroenergetics: Implications for brain function. Annu Rev Physiol 65 (2003) 401-427
13. Pellerin L., and Magistretti P.J. Neuroscience. Let there be (NADH) light. Science 305 (2004) 50-52
14. Igarashi H., Kwee I.L., Nakada T., Katayama Y., and Terashi A. 1H magnetic resonance spectroscopic imaging of permanent focal cerebral ischemia in rat: Longitudinal metabolic changes in ischemic core and rim. Brain Res 907 (2001) 208-221
15. Mlynarik V., Kohler I., Gambarota G., Vaslin A., Clarke P.G., and Gruetter R. Quantitative proton spectroscopic imaging of the neurochemical profile in rat brain with microliter resolution at ultra-short echo times. Magn Reson Med 59 (2008) 52-58
16. Sanacora G., Rothman D.L., Mason G., and Krystal J.H. Clinical studies implementing glutamate neurotransmission in mood disorders. Ann N Y Acad Sci 1003 (2003) 292-308
17. Kugaya A., and Sanacora G. Beyond monoamines: Glutamatergic function in mood disorders. CNS Spectr 10 (2005) 808-819
18. Berton O., and Nestler E.J. New approaches to antidepressant drug discovery: Beyond monoamines. Nat Rev Neurosci 7 (2006) 137-151
19. Lan M.J., McLoughlin G.A., Griffin J.L., Tsang T.M., Huang J.T., Yuan P., et al. Metabonomic analysis identifies molecular changes associated with the pathophysiology and drug treatment of bipolar disorder. Mol Psychiatry (2008) [published online ahead of print February 5]
20. Govindaraju V., Young K., and Maudsley A.A. Proton NMR chemical shifts and coupling constants for brain metabolites. NMR Biomed 13 (2000) 129-153
21. Auer D.P., Putz B., Kraft E., Lipinski B., Schill J., and Holsboer F. Reduced glutamate in the anterior cingulate cortex in depression: An in vivo proton magnetic resonance spectroscopy study. Biol Psychiatry 47 (2000) 305-313
22. Hasler G., van der Veen J.W., Tumonis T., Meyers N., Shen J., and Drevets W.C. Reduced prefrontal glutamate/glutamine and gamma-aminobutyric acid levels in major depression determined using proton magnetic resonance spectroscopy. Arch Gen Psychiatry 64 (2007) 193-200
23. Mirza Y., Tang J., Russell A., Banerjee S.P., Bhandari R., Ivey J., et al. Reduced anterior cingulate cortex glutamatergic concentrations in childhood major depression. J Am Acad Child Adolesc Psychiatry 43 (2004) 341-348
24. Michael N., Erfurth A., Ohrmann P., Gossling M., Arolt V., Heindel W., et al. Acute mania is accompanied by elevated glutamate/glutamine levels within the left dorsolateral prefrontal cortex. Psychopharmacology (Berl) 168 (2003) 344-346
25. Cecil K.M., DelBello M.P., Morey R., and Strakowski S.M. Frontal lobe differences in bipolar disorder as determined by proton MR spectroscopy. Bipolar Disord 4 (2002) 357-365
26. Frye M.A., Watzl J., Banakar S., O'Neill J., Mintz J., Davanzo P., et al. Increased anterior cingulate/medial prefrontal cortical glutamate and creatine in bipolar depression. Neuropsychopharmacology 32 (2007) 2490-2499
27. Dager S.R., Friedman S.D., Parow A., Demopulos C., Stoll A.L., Lyoo I.K., et al. Brain metabolic alterations in medication-free patients with bipolar disorder. Arch Gen Psychiatry 61 (2004) 450-458
28. Bhagwagar Z., Wylezinska M., Jezzard P., Evans J., Ashworth F., Sule A., et al. Reduction in occipital cortex gamma-aminobutyric acid concentrations in medication-free recovered unipolar depressed and bipolar subjects. Biol Psychiatry 61 (2007) 806-812
29. Moore C.M., Frazier J.A., Glod C.A., Breeze J.L., Dieterich M., Finn C.T., et al. Glutamine and glutamate levels in children and adolescents with bipolar disorder: A 4.0-T proton magnetic resonance spectroscopy study of the anterior cingulate cortex. J Am Acad Child Adolesc Psychiatry 46 (2007) 524-534
30. Sanacora G., Gueorguieva R., Epperson C.N., Wu Y.T., Appel M., Rothman D.L., et al. Subtype-specific alterations of gamma-aminobutyric acid and glutamate in patients with major depression. Arch Gen Psychiatry 61 (2004) 705-713
31. Goff D.C., and Coyle J.T. The emerging role of glutamate in the pathophysiology and treatment of schizophrenia. Am J Psychiatry 158 (2001) 1367-1377
32. Theberge J., Bartha R., Drost D.J., Menon R.S., Malla A., Takhar J., et al. Glutamate and glutamine measured with 4.0 T proton MRS in never-treated patients with schizophrenia and healthy volunteers. Am J Psychiatry 159 (2002) 1944-1946
33. Theberge J., Al-Semaan Y., Williamson P.C., Menon R.S., Neufeld R.W., Rajakumar N., et al. Glutamate and glutamine in the anterior cingulate and thalamus of medicated patients with chronic schizophrenia and healthy comparison subjects measured with 4.0-T proton MRS. Am J Psychiatry 160 (2003) 2231-2233
34. Ryner L.N., Sorenson J.A., and Thomas M.A. Localized 2D J-resolved 1H MR spectroscopy: Strong coupling effects in vitro and in vivo. Magn Reson Imaging 13 (1995) 853-869
35. Ke Y., Cohen B.M., Bang J.Y., Yang M., and Renshaw P.F. Assessment of GABA concentration in human brain using two-dimensional proton magnetic resonance spectroscopy. Psychiatry Res 100 (2000) 169-178
36. Schulte R.F., and Boesiger P. ProFit: Two-dimensional prior-knowledge fitting of J-resolved spectra. NMR Biomed 19 (2006) 255-263
37. Phillips M.L., Drevets W.C., Rauch S.L., and Lane R. Neurobiology of emotion perception II: Implications for major psychiatric disorders. Biol Psychiatry 54 (2003) 515-528
38. Strakowski S.M., Delbello M.P., and Adler C.M. The functional neuroanatomy of bipolar disorder: A review of neuroimaging findings. Mol Psychiatry 10 (2005) 105-116
39. Jensen J.E., Frederick B.D., Wang L., Brown J., and Renshaw P.F. Two-dimensional, J-resolved spectroscopic imaging of GABA at 4 Tesla in the human brain. Magn Reson Med 54 (2005) 783-788
40. First M.B., Spitzer R.L., Gibbon M., and Williams J.B.W. Structured Clinical Interview for DSM-IV Axis I Disorders (1995), New York State Psychiatric Institute, Biometrics Research, New York
41. Woods S.W. Chlorpromazine equivalent doses for the newer atypical antipsychotics. J Clin Psychiatry 64 (2003) 663-667
42. Ogg R.J., Kingsley P.B., and Taylor J.S. WET, a T1- and B1-insensitive water-suppression method for in vivo localized 1H NMR spectroscopy. J Magn Reson B 104 (1994) 1-10
43. Provencher S.W. Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn Reson Med 30 (1993) 672-679
44. Smith S.A., Levante T.O., Meier B.H., and Ernst R.R. Computer simulations in magnetic resonance. An object-oriented programming approach. J Magn Reson A 106 (1994) 75-105
45. Provencher S.W. Automatic quantitation of localized in vivo 1H spectra with LCModel. NMR Biomed 14 (2001) 260-264
46. Posse S., Otazo R., Caprihan A., Bustillo J., Chen H., Henry P.G., et al. Proton echo-planar spectroscopic imaging of J-coupled resonances in human brain at 3 and 4 Tesla. Magn Reson Med 58 (2007) 236-244
47. Hetherington H.P., Mason G.F., Pan J.W., Ponder S.L., Vaughan J.T., Twieg D.B., et al. Evaluation of cerebral gray and white matter metabolite differences by spectroscopic imaging at 4.1T. Magn Reson Med 32 (1994) 565-571
48. Wang Y., and Li S.J. Differentiation of metabolic concentrations between gray matter and white matter of human brain by in vivo 1H magnetic resonance spectroscopy. Magn Reson Med 39 (1998) 28-33
49. Kishimoto H., Takazu O., Ohno S., Yamaguchi T., Fujita H., Kuwahara H., et al. 11C-glucose metabolism in manic and depressed patients. Psychiatry Res 22 (1987) 81-88
50. Cotter D.R., Pariante C.M., and Everall I.P. Glial cell abnormalities in major psychiatric disorders: The evidence and implications. Brain Res Bull 55 (2001) 585-595
51. Hertz L., and Zielke H.R. Astrocytic control of glutamatergic activity: Astrocytes as stars of the show. Trends Neurosci 27 (2004) 735-743
52. Varoqui H., Zhu H., Yao D., Ming H., and Erickson J.D. Cloning and functional identification of a neuronal glutamine transporter. J Biol Chem 275 (2000) 4049-4054
53. Schoepp D. New directions in the treatment of schizophrenia: Modulators of mGlu2 and/or mGlu3 receptors. Neuropsychopharmacology 31 (2006) S25
54. Bertolino A., Callicott J.H., Elman I., Mattay V.S., Tedeschi G., Frank J.A., et al. Regionally specific neuronal pathology in untreated patients with schizophrenia: A proton magnetic resonance spectroscopic imaging study. Biol Psychiatry 43 (1998) 641-648
55. Bertolino A., Frye M., Callicott J.H., Mattay V.S., Rakow R., Shelton-Repella J., et al. Neuronal pathology in the hippocampal area of patients with bipolar disorder: A study with proton magnetic resonance spectroscopic imaging. Biol Psychiatry 53 (2003) 906-913
56. Lyoo I.K., and Renshaw P.F. Magnetic resonance spectroscopy: Current and future applications in psychiatric research. Biol Psychiatry 51 (2002) 195-207
57. Yildiz-Yesiloglu A., and Ankerst D.P. Neurochemical alterations of the brain in bipolar disorder and their implications for pathophysiology: A systematic review of the in vivo proton magnetic resonance spectroscopy findings. Prog Neuropsychopharmacol Biol Psychiatry 30 (2006) 969-995
58. Stork C., and Renshaw P.F. Mitochondrial dysfunction in bipolar disorder: Evidence from magnetic resonance spectroscopy research. Mol Psychiatry 10 (2005) 900-919
59. Schirmer T., and Auer D.P. On the reliability of quantitative clinical magnetic resonance spectroscopy of the human brain. NMR Biomed 13 (2000) 28-36
60. Geurts J.J., Barkhof F., Castelijns J.A., Uitdehaag B.M., Polman C.H., and Pouwels P.J. Quantitative 1H-MRS of healthy human cortex, hippocampus, and thalamus: Metabolite concentrations, quantification precision, and reproducibility. J Magn Reson Imaging 20 (2004) 366-371
61. Bartha R., Drost D.J., Menon R.S., and Williamson P.C. Comparison of the quantification precision of human short echo time (1)H spectroscopy at 1.5 and 4.0 Tesla. Magn Reson Med 44 (2000) 185-192
62. Provencher S.W. LCModel & LCMgui User's Manual (2005), Stephen Provencher, Oakville, Ontario, Canada
63. Schubert F., Gallinat J., Seifert F., and Rinneberg H. Glutamate concentrations in human brain using single voxel proton magnetic resonance spectroscopy at 3 Tesla. Neuroimage 21 (2004) 1762-1771
64. Du J., Suzuki K., Wei Y., Wang Y., Blumenthal R., Chen Z., et al. The anticonvulsants lamotrigine, riluzole, and valproate differentially regulate AMPA receptor membrane localization: Relationship to clinical effects in mood disorders. Neuropsychopharmacology 32 (2007) 793-802
65. Friedman S.D., Dager S.R., Parow A., Hirashima F., Demopulos C., Stoll A.L., et al. Lithium and valproic acid treatment effects on brain chemistry in bipolar disorder. Biol Psychiatry 56 (2004) 340-348
66. Dixon J.F., and Hokin L.E. The antibipolar drug valproate mimics lithium in stimulating glutamate release and inositol 1,4,5-trisphosphate accumulation in brain cortex slices but not accumulation of inositol monophosphates and bisphosphates. Proc Natl Acad Sci U S A 94 (1997) 4757-4760
67. Dixon J.F., and Hokin L.E. Lithium acutely inhibits and chronically up-regulates and stabilizes glutamate uptake by presynaptic nerve endings in mouse cerebral cortex. Proc Natl Acad Sci U S A 95 (1998) 8363-8368
68. Zarate Jr. C.A., Du J., Quiroz J., Gray N.A., Denicoff K.D., Singh J., et al. Regulation of cellular plasticity cascades in the pathophysiology and treatment of mood disorders: Role of the glutamatergic system. Ann N Y Acad Sci 1003 (2003) 273-291
69. Frey B.N., Stanley J.A., Nery F.G., Monkul E.S., Nicoletti M.A., Chen H.H., et al. Abnormal cellular energy and phospholipid metabolism in the left dorsolateral prefrontal cortex of medication-free individuals with bipolar disorder: An in vivo 1H MRS study. Bipolar Disord 9 suppl 1 (2007) 119-127
70. Theberge J., Williamson K.E., Aoyama N., Drost D.J., Manchanda R., Malla A.K., et al. Longitudinal grey-matter and glutamatergic losses in first-episode schizophrenia. Br J Psychiatry 191 (2007) 325-334
71. Barker P.B., Soher B.J., Blackband S.J., Chatham J.C., Mathews V.P., and Bryan R.N. Quantitation of proton NMR spectra of the human brain using tissue water as an internal concentration reference. NMR Biomed 6 (1993) 89-94
72. Benes F.M., and Berretta S. GABAergic interneurons: Implications for understanding schizophrenia and bipolar disorder. Neuropsychopharmacology 25 (2001) 1-27
73. Heckers S., Stone D.J., Walsh J., Shick J.F., Koul P., and Benes F.M. Hippocampal GAD65 and GAD67 mRNA expression in schizophrenia and bipolar disorder. Schizophr Res 49 (2001) 61