From pathophysiology to novel antidepressant drugs: Glial contributions to the pathology and treatment of mood disorders

Biological Psychiatry

Volumn 73, Issue 12, 2013, Pages 1172-1179

  Sanacora, Gerard ^a   Banasr, Mounira ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Antidepressant astrocytes depression; EAAT glia prefrontal cortex stress

Indexed keywords

CLOMIPRAMINE; DESIPRAMINE; EXCITATORY AMINO ACID TRANSPORTER 1; EXCITATORY AMINO ACID TRANSPORTER 2; FLUOXETINE; GLUTAMIC ACID; GLUTAMINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PAROXETINE; RILUZOLE;

AMINO ACID TRANSPORT; AMYGDALOID NUCLEUS; ANTIDEPRESSANT ACTIVITY; ANXIETY DISORDER; CHRONIC STRESS; CINGULATE GYRUS; COMPETITIVE INHIBITION; DEPRESSION; DOWN REGULATION; GLIA CELL; GLUCOSE METABOLISM; GRAY MATTER; HIPPOCAMPUS; HUMAN; LONG TERM POTENTIATION; MACROGLIA; MAJOR DEPRESSION; MATERNAL DEPRIVATION; MONOTHERAPY; MOOD DISORDER; NERVE CELL PLASTICITY; NEUROPROTECTION; NONHUMAN; OLIGODENDROGLIA; PATHOPHYSIOLOGY; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSYCHOPHARMACOTHERAPY; REVIEW; STRUCTURE ACTIVITY RELATION; UPREGULATION;

ANIMALS; ANTIDEPRESSIVE AGENTS; CELL COMMUNICATION; HUMANS; MOOD DISORDERS; NEUROGLIA; NEURONS;

EID: 84878379500     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2013.03.032     Document Type: Review

References (96)

1. J.L. Price, and W.C. Drevets Neural circuits underlying the pathophysiology of mood disorders Trends Cogn Sci 16 2012 61 71
2. J.J. Miguel-Hidalgo, and G. Rajkowska Morphological brain changes in depression: Can antidepressants reverse them? CNS Drugs 16 2002 361 372
3. R.L.K. Virchow Die Cellularpathologie in ihrer Begründung auf physiologische und pathologische Gewebelehre 1858 A. Hirschwald Berlin
4. C. Eroglu, and B.A. Barres Regulation of synaptic connectivity by glia Nature 468 2010 223 231
5. K.A. Nave Myelination and the trophic support of long axons Nat Rev Neurosci 11 2010 275 283
6. S. David, and A. Kroner Repertoire of microglial and macrophage responses after spinal cord injury Nat Rev Neurosci 12 2011 388 399
7. D.P. Schafer, E.K. Lehrman, A.G. Kautzman, R. Koyama, A.R. Mardinly, and R. Yamasaki Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner Neuron 74 2012 691 705
8. T. Blank, and M. Prinz Microglia as modulators of cognition and neuropsychiatric disorders Glia 61 2013 62 70
9. N.A. Oberheim, S.A. Goldman, and M. Nedergaard Heterogeneity of astrocytic form and function Methods Mol Biol 814 2012 23 45
10. B.R. Ransom, and C.B. Ransom Astrocytes: Multitalented stars of the central nervous system Methods Mol Biol 814 2012 3 7
11. H.H. Tsai, H. Li, L.C. Fuentealba, A.V. Molofsky, R. Taveira-Marques, and H. Zhuang Regional astrocyte allocation regulates CNS synaptogenesis and repair Science 337 2012 358 362
12. N.A. Oberheim, T. Takano, X. Han, W. He, J.H. Lin, and F. Wang Uniquely hominid features of adult human astrocytes J Neurosci 29 2009 3276 3287
13. A.V. Molofsky, R. Krencik, E.M. Ullian, H.H. Tsai, B. Deneen, and W.D. Richardson Astrocytes and disease: A neurodevelopmental perspective Genes Dev 26 2012 891 907
14. D. Ongur, W.C. Drevets, and J.L. Price Glial reduction in the subgenual prefrontal cortex in mood disorders Proc Natl Acad Sci U S A 95 1998 13290 13295
15. D. Cotter, D. Mackay, S. Landau, R. Kerwin, and I. Everall Reduced glial cell density and neuronal size in the anterior cingulate cortex in major depressive disorder Arch Gen Psychiatry 58 2001 545 553
16. R.A. Gittins, and P.J. Harrison A morphometric study of glia and neurons in the anterior cingulate cortex in mood disorder J Affect Disord 133 2011 328 332
17. G. Rajkowska, J.J. Miguel-Hidalgo, J. Wei, G. Dilley, S.D. Pittman, and H.Y. Meltzer Morphometric evidence for neuronal and glial prefrontal cell pathology in major depression Biol Psychiatry 45 1999 1085 1098
18. G. Rajkowska, A. Halaris, and L.D. Selemon Reductions in neuronal and glial density characterize the dorsolateral prefrontal cortex in bipolar disorder Biol Psychiatry 49 2001 741 752
19. N.A. Uranova, V.M. Vostrikov, D.D. Orlovskaya, and V.I. Rachmanova Oligodendroglial density in the prefrontal cortex in schizophrenia and mood disorders: A study from the Stanley Neuropathology Consortium Schizophr Res 67 2004 269 275
20. D. Cotter, D. Mackay, G. Chana, C. Beasley, S. Landau, and I.P. Everall Reduced neuronal size and glial cell density in area 9 of the dorsolateral prefrontal cortex in subjects with major depressive disorder Cerebral Cortex 12 2002 386 394
21. M.R. Williams, T. Hampton, R.K. Pearce, S.R. Hirsch, O. Ansorge, and M. Thom Astrocyte decrease in the subgenual cingulate and callosal genu in schizophrenia Eur Arch Psychiatry Clin Neurosci 263 2013 41 52
22. M. Hamidi, W.C. Drevets, and J.L. Price Glial reduction in amygdala in major depressive disorder is due to oligodendrocytes Biol Psychiatry 55 2004 563 569
23. M.P. Bowley, W.C. Drevets, D. Ongur, and J.L. Price Low glial numbers in the amygdala in major depressive disorder Biol Psychiatry 52 2002 404 412
24. N. Edgar, and E. Sibille A putative functional role for oligodendrocytes in mood regulation Trans Psychiatry 2 2012 e109
25. J. Steiner, H. Bielau, R. Brisch, P. Danos, O. Ullrich, and C. Mawrin Immunological aspects in the neurobiology of suicide: elevated microglial density in schizophrenia and depression is associated with suicide J Psychiatr Res 42 2008 151 157
26. W. Beumer, S.M. Gibney, R.C. Drexhage, L. Pont-Lezica, J. Doorduin, and H.C. Klein The immune theory of psychiatric diseases: A key role for activated microglia and circulating monocytes J Leukoc Biol 92 2012 959 975
27. M.B. Muller, P.J. Lucassen, A. Yassouridis, W.J. Hoogendijk, F. Holsboer, and D.F. Swaab Neither major depression nor glucocorticoid treatment affects the cellular integrity of the human hippocampus Eur J Neurosci 14 2001 1603 1612
28. M.J. Webster, M.B. Knable, N. Johnston-Wilson, K. Nagata, M. Inagaki, and R.H. Yolken Immunohistochemical localization of phosphorylated glial fibrillary acidic protein in the prefrontal cortex and hippocampus from patients with schizophrenia, bipolar disorder, and depression Brain Behav Immun 15 2001 388 400
29. N.L. Johnston-Wilson, C.D. Sims, J.P. Hofmann, L. Anderson, A.D. Shore, and E.F. Torrey Disease-specific alterations in frontal cortex brain proteins in schizophrenia, bipolar disorder, and major depressive disorder. The Stanley Neuropathology Consortium Mol Psychiatry 5 2000 142 149
30. X. Si, J.J. Miguel-Hidalgo, G. O'Dwyer, C.A. Stockmeier, and G. Rajkowska Age-dependent reductions in the level of glial fibrillary acidic protein in the prefrontal cortex in major depression Neuropsychopharmacology 29 2004 2088 2096
31. L.L. Altshuler, O.A. Abulseoud, L. Foland-Ross, G. Bartzokis, S. Chang, and J. Mintz Amygdala astrocyte reduction in subjects with major depressive disorder but not bipolar disorder Bipolar Disord 12 2010 541 549
32. S.H. Fatemi, J.A. Laurence, M. Araghi-Niknam, J.M. Stary, S.C. Schulz, and S. Lee Glial fibrillary acidic protein is reduced in cerebellum of subjects with major depression, but not schizophrenia Schizophr Res 69 2004 317 323
33. J.J. Miguel-Hidalgo, C. Baucom, G. Dilley, J.C. Overholser, H.Y. Meltzer, and C.A. Stockmeier Glial fibrillary acidic protein immunoreactivity in the prefrontal cortex distinguishes younger from older adults in major depressive disorder Biol Psychiatry 48 2000 861 873
34. P.V. Choudary, M. Molnar, S.J. Evans, H. Tomita, J.Z. Li, and M.P. Vawter Altered cortical glutamatergic and GABAergic signal transmission with glial involvement in depression Proc Natl Acad Sci U S A 102 2005 15653 15658
35. R. Bernard, I.A. Kerman, R.C. Thompson, E.G. Jones, W.E. Bunney, and J.D. Barchas Altered expression of glutamate signaling, growth factor, and glia genes in the locus coeruleus of patients with major depression Mol Psychiatry 16 2011 634 646
36. C. Ernst, E.S. Chen, and G. Turecki Histone methylation and decreased expression of TrkB.T1 in orbital frontal cortex of suicide completers Mol Psychiatry 14 2009 830 832
37. C. Ernst, C. Nagy, S. Kim, J.P. Yang, X. Deng, and I.C. Hellstrom Dysfunction of astrocyte connexins 30 and 43 in dorsal lateral prefrontal cortex of suicide completers Biol Psychiatry 70 2011 312 319
38. B. Czeh, M. Simon, B. Schmelting, C. Hiemke, and E. Fuchs Astroglial plasticity in the hippocampus is affected by chronic psychosocial stress and concomitant fluoxetine treatment Neuropsychopharmacology 31 2006 1616 1626
39. Y. Gong, X.L. Sun, F.F. Wu, C.J. Su, J.H. Ding, and G. Hu Female early adult depression results in detrimental impacts on the behavioral performance and brain development in offspring CNS Neurosci Ther 18 2012 461 470
40. C. Araya-Callis, C. Hiemke, N. Abumaria, and G. Flugge Chronic psychosocial stress and citalopram modulate the expression of the glial proteins GFAP and NDRG2 in the hippocampus Psychopharmacology (Berl) 224 2012 209 222
41. Y. Ye, G. Wang, H. Wang, and X. Wang Brain-derived neurotrophic factor (BDNF) infusion restored astrocytic plasticity in the hippocampus of a rat model of depression Neurosci Lett 503 2011 15 19
42. M. Leventopoulos, D. Rüedi-Bettschen, I. Knuesel, J. Feldon, C.R. Pryce, and J. Opacka-Juffry Long-term effects of early life deprivation on brain glia in Fischer rats Brain Res 1142 2007 119 126
43. M. Banasr, and R.S. Duman Glial loss in the prefrontal cortex is sufficient to induce depressive-like behaviors Biol Psychiatry 64 2008 863 870
44. M. Banasr, G.M. Chowdhury, R. Terwilliger, S.S. Newton, R.S. Duman, and K.L. Behar Glial pathology in an animal model of depression: Reversal of stress-induced cellular, metabolic and behavioral deficits by the glutamate-modulating drug riluzole Mol Psychiatry 15 2010 501 511
45. R.D. Gosselin, S. Gibney, D. O'Malley, T.G. Dinan, and J.F. Cryan Region specific decrease in glial fibrillary acidic protein immunoreactivity in the brain of a rat model of depression Neuroscience 159 2009 915 925
46. J.D. Sun, Y. Liu, Y.H. Yuan, J. Li, and N.H. Chen Gap junction dysfunction in the prefrontal cortex induces depressive-like behaviors in rats Neuropsychopharmacology 37 2012 1305 1320
47. H. Imbe, A. Kimura, T. Donishi, and Y. Kaneoke Chronic restraint stress decreases glial fibrillary acidic protein and glutamate transporter in the periaqueductal gray matter Neuroscience 223 2012 209 218
48. G. Sanacora, D.L. Rothman, G.F. Mason, and J.H. Krystal Clinical studies implementing glutamate neurotransmission in mood disorders B. Moghaddam, M.E. Wolf, Glutamate and Disorders of Cognition and Motivation 2003 New York Academy of Sciences New York 292 308
49. J.J. Miguel-Hidalgo, R. Waltzer, A.A. Whittom, M.C. Austin, G. Rajkowska, and C.A. Stockmeier Glial and glutamatergic markers in depression, alcoholism, and their comorbidity J Affect Disord 127 2010 230 240
50. S.L. Gourley, J.W. Espitia, G. Sanacora, and J.R. Taylor Antidepressant-like properties of oral riluzole and utility of incentive disengagement models of depression in mice Psychopharmacology (Berl) 219 2012 805 814
51. M. Zink, B. Vollmayr, P.J. Gebicke-Haerter, and F.A. Henn Reduced expression of glutamate transporters vGluT1, EAAT2 and EAAT4 in learned helpless rats, an animal model of depression Neuropharmacology 58 2010 465 473
52. R.D. Gosselin, R.M. O'Connor, M. Tramullas, M. Julio-Pieper, T.G. Dinan, and J.F. Cryan Riluzole normalizes early-life stress-induced visceral hypersensitivity in rats: Role of spinal glutamate reuptake mechanisms Gastroenterology 138 2010 2418 2425
53. S. Bradesi, V. Golovatscka, H.S. Ennes, J.A. McRoberts, I. Karagiannides, and K. Bakirtzi Role of astrocytes and altered regulation of spinal glutamatergic neurotransmission in stress-induced visceral hyperalgesia in rats Am J Physiol Gastrointest Liver Physiol 301 2011 G580 G589
54. A.J. Bechtholt-Gompf, H.V. Walther, M.A. Adams, W.A. Carlezon Jr, D. Ongur, and B.M. Cohen Blockade of astrocytic glutamate uptake in rats induces signs of anhedonia and impaired spatial memory Neuropsychopharmacology 35 2010 2049 2059
55. C.S. John, K.L. Smith, A. Van't Veer, H.S. Gompf, W.A. Carlezon Jr, and B.M. Cohen Blockade of astrocytic glutamate uptake in the prefrontal cortex induces anhedonia Neuropsychopharmacology 37 2012 2467 2475
56. Y. Lee, D. Gaskins, A. Anand, and A. Shekhar Glia mechanisms in mood regulation: A novel model of mood disorders Psychopharmacology (Berl) 191 2007 55 65
57. G.E. Hardingham, and H. Bading Synaptic versus extrasynaptic NMDA receptor signalling: Implications for neurodegenerative disorders Nat Rev Neurosci 11 2010 682 696
58. T. Papouin, L. Ladepeche, J. Ruel, S. Sacchi, M. Labasque, and M. Hanini Synaptic and extrasynaptic NMDA receptors are gated by different endogenous coagonists Cell 150 2012 633 646
59. P.M. Beart, and R.D. O'Shea Transporters for L-glutamate: An update on their molecular pharmacology and pathological involvement Br J Pharmacol 150 2007 5 17
60. A. Omrani, M. Melone, M. Bellesi, V. Safiulina, T. Aida, and K. Tanaka Up-regulation of GLT-1 severely impairs LTD at mossy fibre - CA3 synapses J Physiol 587 2009 4575 4588
61. K. Zheng, A. Scimemi, and D.A. Rusakov Receptor actions of synaptically released glutamate: The role of transporters on the scale from nanometers to microns Biophys J 95 2008 4584 4596
62. V. Dave, and H.K. Kimelberg Na(+)-dependent, fluoxetine-sensitive serotonin uptake by astrocytes tissue-printed from rat cerebral cortex J Neurosci 14 1994 4972 4986
63. S. Kusakawa, K. Nakamura, Y. Miyamoto, A. Sanbe, T. Torii, and J. Yamauchi Fluoxetine promotes gliogenesis during neural differentiation in mouse embryonic stem cells J Neurosci Res 88 2010 3479 3487
64. S.H. Fatemi, T.D. Folsom, T.J. Reutiman, T. Pandian, N.N. Braun, and K. Haug Chronic psychotropic drug treatment causes differential expression of connexin 43 and GFAP in frontal cortex of rats Schizophr Res 104 2008 127 134
65. I. Sillaber, M. Panhuysen, M.S. Henniger, F. Ohl, C. Kuhne, and B. Putz Profiling of behavioral changes and hippocampal gene expression in mice chronically treated with the SSRI paroxetine Psychopharmacology (Berl) 200 2008 557 572
66. I. Allaman, H. Fiumelli, P.J. Magistretti, and J.L. Martin Fluoxetine regulates the expression of neurotrophic/growth factors and glucose metabolism in astrocytes Psychopharmacology (Berl) 216 2011 75 84
67. K. Ubhi, C. Inglis, M. Mante, C. Patrick, A. Adame, and B. Spencer Fluoxetine ameliorates behavioral and neuropathological deficits in a transgenic model mouse of alpha-synucleinopathy Exp Neurol 234 2012 405 416
68. H. Kong, L.L. Sha, Y. Fan, M. Xiao, J.H. Ding, and J. Wu Requirement of AQP4 for antidepressive efficiency of fluoxetine: Implication in adult hippocampal neurogenesis Neuropsychopharmacology 34 2009 1263 1276
69. Y.K. Li, F. Wang, W. Wang, Y. Luo, P.F. Wu, and J.L. Xiao Aquaporin-4 deficiency impairs synaptic plasticity and associative fear memory in the lateral amygdala: Involvement of downregulation of glutamate transporter-1 expression Neuropsychopharmacology 37 2012 1867 1878
70. M. Zink, S. Rapp, R. Donev, P.J. Gebicke-Haerter, and J. Thome Fluoxetine treatment induces EAAT2 expression in rat brain J Neural Transm 118 2011 849 855
71. Q. Liu, B. Li, H.Y. Zhu, Y.Q. Wang, J. Yu, and G.C. Wu Clomipramine treatment reversed the glial pathology in a chronic unpredictable stress-induced rat model of depression Eur Neuropsychopharmacol 19 2009 796 805
72. Q. Liu, H.Y. Zhu, B. Li, Y.Q. Wang, J. Yu, and G.C. Wu Chronic clomipramine treatment restores hippocampal expression of glial cell line-derived neurotrophic factor in a rat model of depression J Affect Disord 141 2012 367 372
73. P.S. Verhave, M.J. Jongsma, R.M. Van Den Berg, R.A. Vanwersch, A.B. Smit, and I.H. Philippens Neuroprotective effects of riluzole in early phase Parkinson's disease on clinically relevant parameters in the marmoset MPTP model Neuropharmacology 62 2012 1700 1707
74. M. Yoshizumi, J.C. Eisenach, and K. Hayashida Riluzole and gabapentinoids activate glutamate transporters to facilitate glutamate-induced glutamate release from cultured astrocytes Eur J Pharmacol 677 2012 87 92
75. E. Fumagalli, M. Funicello, T. Rauen, M. Gobbi, and T. Mennini Riluzole enhances the activity of glutamate transporters GLAST, GLT1 and EAAC1 Eur J Pharmacol 578 2008 171 176
76. A.Y. Liu, R. Mathur, N. Mei, C.G. Langhammer, B. Babiarz, and B.L. Firestein Neuroprotective drug riluzole amplifies the heat shock factor 1 (HSF1)- and glutamate transporter 1 (GLT1)-dependent cytoprotective mechanisms for neuronal survival J Biol Chem 286 2011 2785 2794
77. C. Pittenger, V. Coric, M. Banasr, M. Bloch, J.H. Krystal, and G. Sanacora Riluzole in the treatment of mood and anxiety disorders CNS Drugs 22 2008 761 786
78. A. Sugiyama, A. Saitoh, T. Iwai, K. Takahashi, M. Yamada, and S. Sasaki-Hamada Riluzole produces distinct anxiolytic-like effects in rats without the adverse effects associated with benzodiazepines Neuropharmacology 62 2012 2489 2498
79. K. Takahashi, H. Murasawa, K. Yamaguchi, M. Yamada, A. Nakatani, and M. Yoshida Riluzole rapidly attenuates hyperemotional responses in olfactory bulbectomized rats, an animal model of depression Behav Brain Res 216 2011 46 52
80. C. Pittenger, B. Kelmendi, S. Wasylink, M.H. Bloch, and V. Coric Riluzole augmentation in treatment-refractory obsessive-compulsive disorder: A series of 13 cases, with long-term follow-up J Clin Psychopharmacol 28 2008 363 367
81. L. Ibrahim, N. Diazgranados, J. Franco-Chaves, N. Brutsche, I.D. Henter, and P. Kronstein Course of improvement in depressive symptoms to a single intravenous infusion of ketamine vs add-on riluzole: Results from a 4-week, double-blind, placebo-controlled study Neuropsychopharmacology 37 2012 1526 1533
82. S.J. Mathew, J.W. Murrough, M. Aan Het Rot, K.A. Collins, D.L. Reich, and D.S. Charney Riluzole for relapse prevention following intravenous ketamine in treatment-resistant depression: A pilot randomized, placebo-controlled continuation trial Int J Neuropsychopharmacol 13 2010 71 82
83. B.P. Brennan, J.I. Hudson, J.E. Jensen, J. McCarthy, J.L. Roberts, and A.P. Prescot Rapid enhancement of glutamatergic neurotransmission in bipolar depression following treatment with riluzole Neuropsychopharmacology 35 2010 834 846
84. G.M. Chowdhury, M. Banasr, R.A. De Graaf, D.L. Rothman, K.L. Behar, and G. Sanacora Chronic riluzole treatment increases glucose metabolism in rat prefrontal cortex and hippocampus J Cereb Blood Flow Metab 28 2008 1892 1897
85. J.D. Rothstein, S. Patel, M.R. Regan, C. Haenggeli, Y.H. Huang, and D.E. Bergles Beta-lactam antibiotics offer neuroprotection by increasing glutamate transporter expression Nature 433 2005 73 77
86. B.R. Miller, J.L. Dorner, M. Shou, Y. Sari, S.J. Barton, and D.R. Sengelaub Up-regulation of GLT1 expression increases glutamate uptake and attenuates the Huntington's disease phenotype in the R6/2 mouse Neuroscience 153 2008 329 337
87. C. Thone-Reineke, C. Neumann, P. Namsolleck, K. Schmerbach, M. Krikov, and J.H. Schefe The beta-lactam antibiotic, ceftriaxone, dramatically improves survival, increases glutamate uptake and induces neurotrophins in stroke J Hypertens 26 2008 2426 2435
88. Y. Sari, M. Sakai, J.M. Weedman, G.V. Rebec, and R.L. Bell Ceftriaxone, a beta-lactam antibiotic, reduces ethanol consumption in alcohol-preferring rats Alcohol Alcohol 46 2011 239 246
89. L.A. Knackstedt, R.I. Melendez, and P.W. Kalivas Ceftriaxone restores glutamate homeostasis and prevents relapse to cocaine seeking Biol Psychiatry 67 2010 81 84
90. J. Miguel-Hidalgo, Y. Shoyama, and V. Wanzo Infusion of gliotoxins or a gap junction blocker in the prelimbic cortex increases alcohol preference in Wistar rats J Psychopharmacol 23 2009 550 557
91. Y.S. Mineur, M.R. Picciotto, and G. Sanacora Antidepressant-like effects of ceftriaxone in male C57BL/6J mice Biol Psychiatry 61 2007 250 252
92. N. Li, B. Lee, R.J. Liu, M. Banasr, J.M. Dwyer, and M. Iwata mTOR-dependent synapse formation underlies the rapid antidepressant effects of NMDA antagonists Science 329 2010 959 964
93. H. Koike, M. Iijima, and S. Chaki Involvement of AMPA receptor in both the rapid and sustained antidepressant-like effects of ketamine in animal models of depression Behav Brain Res 224 2011 107 111
94. J.M. Dwyer, A.E. Lepack, and R.S. Duman mTOR activation is required for the antidepressant effects of mGluR(2)/(3) blockade Int J Neuropsychopharmacol 15 2012 429 434
95. H. Koike, M. Iijima, and S. Chaki Involvement of the mammalian target of rapamycin signaling in the antidepressant-like effect of group II metabotropic glutamate receptor antagonists Neuropharmacology 61 2011 1419 1423
96. A.M. Feyissa, W.L. Woolverton, J.J. Miguel-Hidalgo, Z. Wang, P.B. Kyle, and G. Hasler Elevated level of metabotropic glutamate receptor 2/3 in the prefrontal cortex in major depression Prog Neuropsychopharmacol Biol Psychiatry 34 2010 279 283