Towards a glutamate hypothesis of depression

Sanacora, Gerard; Treccani, Giulia; Popoli, Maurizio

doi:10.1016/j.neuropharm.2011.07.036

Cited by 1,036Treatment of Major DepressionNeuroscience and Neuropharmacology ResearchNeurotransmitter Receptor Influence on Behavior

Towards a glutamate hypothesis of depression

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Sanacora, Gerard, Treccani, Giulia, Popoli, Maurizio·2012·Neuropharmacology

DOI 10.1016/j.neuropharm.2011.07.036PMC PMC3205453

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Abstract

Half a century after the first formulation of the monoamine hypothesis, compelling evidence implies that long-term changes in an array of brain areas and circuits mediating complex cognitive-emotional behaviors represent the biological underpinnings of mood/anxiety disorders. A large number of clinical studies suggest that pathophysiology is associated with dysfunction of the predominant glutamatergic system, malfunction in the mechanisms regulating clearance and metabolism of glutamate, and cytoarchitectural/morphological maladaptive changes in a number of brain areas mediating cognitive-emotional behaviors. Concurrently, a wealth of data from animal models have shown that different types of environmental stress enhance glutamate release/transmission in limbic/cortical areas and exert powerful structural effects, inducing dendritic remodeling, reduction of synapses and possibly volumetric reductions resembling those observed in depressed patients. Because a vast majority of neurons and synapses in these areas and circuits use glutamate as neurotransmitter, it would be limiting to maintain that glutamate is in some way 'involved' in mood/anxiety disorders; rather it should be recognized that the glutamatergic system is a primary mediator of psychiatric pathology and, potentially, also a final common pathway for the therapeutic action of antidepressant agents. A paradigm shift from a monoamine hypothesis of depression to a neuroplasticity hypothesis focused on glutamate may represent a substantial advancement in the working hypothesis that drives research for new drugs and therapies. Importantly, despite the availability of multiple classes of drugs with monoamine-based mechanisms of action, there remains a large percentage of patients who fail to achieve a sustained remission of depressive symptoms. The unmet need for improved pharmacotherapies for treatment-resistant depression means there is a large space for the development of new compounds with novel mechanisms of action such as glutamate transmission and related pathways. This article is part of a Special Issue entitled 'Anxiety and Depression'.

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Serotonin modulates glutamatergic transmission and might kindle NMDA receptor dependent plasticity.
“Serotonin modulates glutamatergic transmission and might kindle N-methyl-D-aspartate (NMDA) receptor dependent plasticity (Bennett, 2010;Sanacora et al., 2012).”
From Serotonin and neuroplasticity – Links between molecular, functional and structural pathophysiology in depression (2017) · cites this paper as Sanacora et al., 2012
Section 8.4 reports that acute fluoxetine, a selective serotonin-reuptake inhibitor, increased extracellular glutamate, providing indirect support for a link between serotonergic treatment and glutamatergic transmission. Section 8 says antidepressants affect synaptic plasticity and NMDA-receptor function, but the passages do not establish that serotonin itself kindles NMDA-receptor-dependent plasticity. No page numbers are available in our copy. (LLM, conf=0.78)
Experimental — accuracy not yet measured
The literature proposes three broad disease models for treatment resistance.
“There are three broad disease models proposed by the literature to explain treatment resistance, summarised in Figure 5 (see eAppendix 3 for search details). 48–51”
From Treatment resistance in psychiatry: state of the art and new directions (2022) · cites this paper as [50]
Glutamatergic neurotransmission is dysregulated in major depressive disorder.
“There has been suggestion that glutamatergic neurotransmission is dysregulated in MDD.83,84”
From Ketamine as an antidepressant: Overview of its mechanisms of action and potential predictive biomarkers (2020) · cites this paper as [83]
Stress-induced dysfunction in forebrain excitatory transmission led to the excitatory synaptic transmission hypothesis of depression.
“Stress-induced dysfunction in forebrain excitatory transmission has led to the development of the excitatory synaptic transmission hypothesis of depression (22, 32, 33).”
From Emerging Role for Nucleus Accumbens Medium Spiny Neuron Subtypes in Depression (2017) · cites this paper as [32]
Antidepressants are believed to exert one of their therapeutic effects by modulating the extracellular availability of glutamate.
“Interestingly, antidepressants are believed to exert one of the therapeutic effects by modulating the extracellular availability of this neurotransmitter [122,123,124,125].”
From P2X7 Receptor Signaling in Stress and Depression (2019) · cites this paper as [123]

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“…response is a complex physiological mechanism and, although much of this mechanism has been unveiled in recent years (de Kloet et al., 2005; McEwen, 2010; Sorrells et al., 2009), the way whereby an incorrect stress response is linked to pathophysiology is still far from being completely understood.”
Background
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Mapping the Matrix: The Ways of Neocortex
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The stress hormone corticosterone conditions AMPAR surface trafficking and synaptic potentiation
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“…sample of individuals with major depressive and bipolar disorder (Frye et al., 2007a) and an earlier study of CSF samples was unable to effectively measure glutamate levels but did report significantly higher CSF glutamine concentrations in subjects with major depression (Levine et al., 2000).”
Result
How can drug discovery for psychiatric disorders be improved?
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Glial fibrillary acidic protein is reduced in cerebellum of subjects with major depression, but not schizophrenia
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Modulation of synaptic plasticity by stress and antidepressants
Popoli, M., Gennarelli, M., & Racagni, G. (2002) · Bipolar Disorders · doi:10.1034/j.1399-5618.2002.01159.x · Cited by 139 · see citing works
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Differential Promotion of Glutamate Transporter Expression and Function by Glucocorticoids in Astrocytes from Various Brain Regions
Zschocke, J., Bayatti, N., Clement, A. M., Witan, H., Figiel, M., Engele, J., & Behl, C. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m502581200 · Cited by 138 · see citing works
Reduced Anterior Cingulate Glutamate in Pediatric Major Depression: A Magnetic Resonance Spectroscopy Study
Rosenberg, D. R., MacMaster, F. P., Mirza, Y., Smith, J. M., Easter, P. C., Banerjee, S. P., Bhandari, R. P., Boyd, C. C., Lynch, M. A., Rose, M., et al. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.05.007 · Cited by 137 · see citing works
Cell pathology in mood disorders
Rajkowska, G. (2002) · Seminars in Clinical Neuropsychiatry · doi:10.1053/scnp.2002.35228 · Cited by 135 · cited 1× · see citing works
“Interestingly, many of the regions showing volumetric reductions overlap with the regions demonstrated to have significant reductions in glial cell numbers and density, and neuronal atrophy (Rajkowska, 2002).”
Background
GABAergic Contributions to the Pathophysiology of Depression and the Mechanism of Antidepressant Action
Sanacora, G., & Sarıçiçek, A. (2007) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/187152707780363294 · Cited by 131 · see citing works
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Antidepressive-like effects of rapamycin in animal models: Implications for mTOR inhibition as a new target for treatment of affective disorders
Cleary, C., Linde, J. A. S., Hiscock, K. M., Hadas, I., Belmaker, R. H., Agam, G., Flaisher-Grinberg, S., & Einat, H. (2008) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2008.03.005 · Cited by 130 · see citing works
Corticosterone Alters AMPAR Mobility and Facilitates Bidirectional Synaptic Plasticity
Martin, S., Henley, J. M., Holman, D., Zhou, M., Wiegert, O., van Spronsen, M., Joëls, M., Hoogenraad, C. C., & Krugers, H. J. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004714 · Cited by 130 · see citing works
Reduced Anterior Cingulate Cortex Glutamatergic Concentrations in Childhood Major Depression
Mirza, Y., Tang, J., Russell, A., Banerjee, S. P., Bhandari, R. P., Ivey, J., Rose, M., Moore, G. J., & Rosenberg, D. R. (2004) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/00004583-200403000-00017 · Cited by 128 · see citing works
Chronic antidepressant treatment increases the membrane expression of AMPA receptors in rat hippocampus
Martínez-Turrillas, R. (2002) · Neuropharmacology · doi:10.1016/s0028-3908(02)00299-x · Cited by 122 · see citing works
Thinking Glutamatergically: Changing Concepts of Schizophrenia Based Upon Changing Neurochemical Models
Kantrowitz, J. T., & Javitt, D. C. (2010) · Clinical Schizophrenia & Related Psychoses · doi:10.3371/csrp.4.3.6 · Cited by 118 · see citing works
Long-term effects of early life deprivation on brain glia in Fischer rats
Leventopoulos, M., Rüedi‐Bettschen, D., Knuesel, I., Feldon, J., Pryce, C. R., & Opacka‐Juffry, J. (2007) · Brain Research · doi:10.1016/j.brainres.2007.01.039 · Cited by 118 · see citing works
Rapid microelectrode measurements and the origin and regulation of extracellular glutamate in rat prefrontal cortex
Hascup, E. R., Hascup, K. N., Humeidan, M., Pomerleau, F., Huettl, P. F., Gratton, A. P., & Gerhardt, G. A. (2010) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2010.07066.x · Cited by 115 · see citing works
Stress, glucocorticoids and glutamate release: Effects of antidepressant drugs
Musazzi, L., Racagni, G., & Popoli, M. (2011) · Neurochemistry International · doi:10.1016/j.neuint.2011.05.002 · Cited by 113 · see citing works
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Roles of glutamate signaling in preclinical and/or mechanistic models of depression
Tokita, K., Yamaji, T., & Hashimoto, K. (2011) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2011.04.016 · Cited by 103 · see citing works
Imipramine and phenelzine decrease glutamate overflow in the prefrontal cortex—a possible mechanism of neuroprotection in major depression?
Michael-Titus, A. T., Bains, S., Jeetle, J. K., & Whelpton, R. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)00390-0 · Cited by 103 · see citing works
Prenatal stress and subsequent exposure to chronic mild stress influence dendritic spine density and morphology in the rat medial prefrontal cortex
Michelsen, K. A., van den Hove, D. L., Schmitz, C., Segers, O., Prickaerts, J., & Steinbusch, H. W. (2007) · BMC Neuroscience · doi:10.1186/1471-2202-8-107 · Cited by 100 · see citing works
Cellular perspectives on the glutamate–monoamine interactions in limbic lobe structures and their relevance for some psychiatric disorders
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Metabotropic glutamate receptor 7: at the interface of cognition and emotion.
O'Connor, R., Finger, B. C., Flor, P., & Cryan, J. (2010) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2010.02.059 · Cited by 98 · see citing works
Brain amino acid concentrations and Ca2+-dependent release in intractable depression assessed antemortem
Francis, P. T., Poynton, A., Lowe, S. L., Najlerahim, A., Bridges, P. K., Bartlett, J. R., PROCTER, A. W., Bruton, C. J., & Bowen, D. M. (1989) · Brain Research · doi:10.1016/0006-8993(89)90600-8 · Cited by 96 · see citing works
Glial fibrillary acidic protein and glutamine synthetase in subregions of prefrontal cortex in schizophrenia and mood disorder
Toro, C. T., Hallak, J. E. C., Dunham, J. S., & Deakin, J. F. W. (2006) · Neuroscience Letters · doi:10.1016/j.neulet.2006.05.067 · Cited by 95 · see citing works
Stress generates emotional memories and retrograde amnesia by inducing an endogenous form of hippocampal LTP
Diamond, D. M., Park, C. R., & Woodson, J. C. (2004) · Hippocampus · doi:10.1002/hipo.10186 · Cited by 95 · see citing works
Regulation of Editing and Expression of Glutamate α-Amino-Propionic-Acid (AMPA)/Kainate Receptors by Antidepressant Drugs
Barbon, A., Popoli, M., Via, L. L., Moraschi, S., Vallini, I., Tardito, D., Tiraboschi, E., Musazzi, L., Giambelli, R., Gennarelli, M., et al. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.10.018 · Cited by 93 · see citing works
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Antidepressants reverse the attenuation of the neurotrophic MEK/MAPK cascade in frontal cortex by elevated platform stress; reversal of effects on LTP is associated with GluA1 phosphorylation
Qi, H., Mailliet, F., Spedding, M., Rocher, C., Zhang, X., Delagrange, P., McEwen, B. S., Jay, T. M., & Svenningsson, P. (2008) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.06.068 · Cited by 91 · see citing works
Metabolic alterations in medication-free patients with bipolar disorder: A 3T CSF-corrected magnetic resonance spectroscopic imaging study
Port, J. D., Unal, S. S., Mrazek, D. A., & Marcus, S. M. (2008) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2007.08.004 · Cited by 90 · see citing works
Decreased hippocampal volume on MRI is associated with increased extracellular glutamate in epilepsy patients
Cavus, I., Pan, J. W., Hetherington, H. P., Abi‐Saab, W., Zaveri, H. P., Vives, K. P., Krystal, J. H., Spencer, S. S., & Spencer, D. D. (2008) · Epilepsia · doi:10.1111/j.1528-1167.2008.01603.x · Cited by 89 · see citing works
Lack of persistent effects of ketamine in rodent models of depression
Popik, P., Kos, T., Sowa-Kućma, M., & Nowak, G. (2008) · Psychopharmacology · doi:10.1007/s00213-008-1158-z · Cited by 86 · see citing works
Metabotropic glutamate receptors in the tripartite synapse as a target for new psychotropic drugs
Wierońska, J. M., & Pilc, A. (2009) · Neurochemistry International · doi:10.1016/j.neuint.2009.02.019 · Cited by 86 · see citing works
Glutamate transporters in platelets: EAAT1 decrease in aging and in Alzheimer’s disease
Zoia, C., Cogliati, T., Tagliabue, E., Cavaletti, G., Sala, G., Galimberti, G., Rivolta, I., Rossi, V., Frattola, L., & Ferrarese, C. (2003) · Neurobiology of Aging · doi:10.1016/s0197-4580(03)00085-x · Cited by 85 · see citing works
Remodelling by early-life stress of NMDA receptor-dependent synaptic plasticity in a gene–environment rat model of depression
Ryan, B. K., Musazzi, L., Mallei, A., Tardito, D., Gruber, S. H. M., Khoury, A. E., Anwyl, R., Racagni, G., Mathé, A. A., Rowan, M. J., et al. (2008) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145708009607 · Cited by 79 · see citing works
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A Hypothesized Role for Dendritic Remodeling in the Etiology of Mood and Anxiety Disorders
Gorman, J. M., & Docherty, J. P. (2010) · Journal of Neuropsychiatry · doi:10.1176/jnp.2010.22.3.256 · Cited by 79 · see citing works
Antidepressant treatments and function of glutamate ionotropic receptors mediating amine release in hippocampus
Pittaluga, A., Raiteri, L., Longordo, F., Luccini, E., Barbiero, V. S., Racagni, G., Popoli, M., & Raiteri, M. (2007) · Neuropharmacology · doi:10.1016/j.neuropharm.2007.04.006 · Cited by 76 · see citing works
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Single voxel proton magnetic resonance spectroscopy in post-stroke depression
Głodzik-Sobańska, L., Słowik, A., McHugh, P. F., Sobiecka, B., Kozub, J., Rich, K. E., Urbanik, A., & Szczudlik, A. (2006) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2006.08.004 · Cited by 75 · see citing works
Repeated Restraint Stress Alters Hippocampal Glutamate Uptake and Release in the Rat
Fontella, F. U., Vendite, D., Tabajara, Â. S., Porciúncula, L. O., Torres, I. L. D. S., Jardim, F. M. A., Martini, L., Souza, D. O., Netto, C. A., & Dalmaz, C. (2004) · Neurochemical Research · doi:10.1023/b:nere.0000035805.46592.6c · Cited by 74 · see citing works
Neurochemistry of late‐life major depression: A pilot two‐dimensional MR spectroscopic study
Binesh, N., Kumar, A., Hwang, S., Mintz, J., & Thomas, M. A. (2004) · Journal of Magnetic Resonance Imaging · doi:10.1002/jmri.20214 · Cited by 72 · see citing works
Glutamate level detection by magnetic resonance spectroscopy in patients with post-stroke depression
Wang, X., Li, Y.-H., Li, M.-H., Lu, J., Zhao, J.-G., Sun, X.-J., Zhang, B., & Ye, J. (2012) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-011-0209-3 · Cited by 72 · see citing works
The Antidepressant Sertraline Inhibits Translation Initiation by Curtailing Mammalian Target of Rapamycin Signaling
Lin, C., Robert, F., Sukarieh, R., Michnick, S. W., & Pelletier, J. (2010) · Cancer Research · doi:10.1158/0008-5472.can-09-4072 · Cited by 69 · see citing works
Repeated administration of imipramine attenuates glutamatergic transmission in rat frontal cortex
Tokarski, K., Bobula, B., Wabno, J., & Hess, G. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.03.007 · Cited by 65 · see citing works
Enhancing AMPA to NMDA throughput as a convergent mechanism for antidepressant action
Du, J., Machado-Vieira, R., Maeng, S., Martinowich, K., Manji, H. K., & Zarate, C. A. (2006) · Drug Discovery Today: Therapeutic Strategies · doi:10.1016/j.ddstr.2006.11.012 · Cited by 64 · see citing works
Chronic imipramine treatment partially reverses the long-term changes of hippocampal synaptic plasticity in socially stressed rats
von Frijtag, J. C., Kamal, A., Reijmers, L. G. J. E., Schrama, L. H., van den Bos, R., & Spruijt, B. M. (2001) · Neuroscience Letters · doi:10.1016/s0304-3940(01)02062-6 · Cited by 62 · see citing works
Glia atrophy in the hippocampus of chronic unpredictable stress-induced depression model rats is reversed by electroacupuncture treatment
Liu, Q., Li, B., Zhu, H., Wang, Y.-Q., Yu, J. M., & Wu, G.-C. (2010) · Journal of Affective Disorders · doi:10.1016/j.jad.2010.07.007 · Cited by 61 · see citing works

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The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission
Popoli, M., Yan, Z., McEwen, B. S., & Sanacora, G. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3138 · Cited by 1,393 · see citing works
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Inflammatory cytokines in depression: neurobiological mechanisms and therapeutic implications
Felger, J. C., & Lotrich, F. E. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.04.060 · Cited by 1,180 · see citing works
Neuroinflammation and depression: A review
Troubat, R., Barone, P., Leman, S., Desmidt, T., Cressant, A., Atanasova, B., Brizard, B., El Hage, W., Surget, A., Belzung, C., et al. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.14720 · Cited by 1,107 · see citing works
Altered Connectivity in Depression: GABA and Glutamate Neurotransmitter Deficits and Reversal by Novel Treatments
Duman, R. S., Sanacora, G., & Krystal, J. H. (2019) · Neuron · doi:10.1016/j.neuron.2019.03.013 · Cited by 1,026 · see citing works
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Management of Depression in Older Adults: A Review
Kok, R. M., & Reynolds, C. F. (2017) · JAMA · doi:10.1001/jama.2017.5706 · Cited by 890 · see citing works
Skeletal Muscle PGC-1α1 Modulates Kynurenine Metabolism and Mediates Resilience to Stress-Induced Depression
Agudelo, L. Z., Femenía, T., Orhan, F., Porsmyr-Palmertz, M., Goiny, M., Martinez-Redondo, V., Correia, J. C., Izadi, M., Bhat, M., Schuppe-Koistinen, I., et al. (2014) · Cell · doi:10.1016/j.cell.2014.07.051 · Cited by 739 · see citing works
Neuroinflammation and psychiatric illness
Najjar, S., Pearlman, D. M., Alper, K., Najjar, A., & Devinsky, O. (2013) · Journal of Neuroinflammation · doi:10.1186/1742-2094-10-43 · Cited by 733 · see citing works
R-ketamine: a rapid-onset and sustained antidepressant without psychotomimetic side effects
Yang, C., Shirayama, Y., Zhang, J.-C., Ren, Q., Yao, W., Ma, M., Dong, C., & Hashimoto, K. (2015) · Translational Psychiatry · doi:10.1038/tp.2015.136 · Cited by 605 · see citing works
Neural Mechanisms of Stress Resilience and Vulnerability
Franklin, T. B., Saab, B. J., & Mansuy, I. M. (2012) · Neuron · doi:10.1016/j.neuron.2012.08.016 · Cited by 500 · see citing works
Glutamate and Gamma-Aminobutyric Acid Systems in the Pathophysiology of Major Depression and Antidepressant Response to Ketamine
Lener, M. S., Niciu, M. J., Ballard, E. D., Park, M., Park, L. T., Nugent, A. C., & Zarate, C. A. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.05.005 · Cited by 468 · see citing works
Serotonin and neuroplasticity – Links between molecular, functional and structural pathophysiology in depression
Kraus, C., Castrén, E., Kasper, S., & Lanzenberger, R. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.03.007 · Cited by 457 · see citing works
Treatment resistance in psychiatry: state of the art and new directions
Howes, O. D., Thase, M. E., & Pillinger, T. (2022) · Molecular Psychiatry · doi:10.1038/s41380-021-01200-3 · Cited by 413 · see citing works
Problematic assumptions have slowed down depression research: Why symptoms, not syndromes are the way forward
Fried, E. I. (2015) · Frontiers in Psychology · doi:10.3389/fpsyg.2015.00309 · Cited by 367 · see citing works
Animal models of major depression and their clinical implications
Czéh, B., Fuchs, E., Wiborg, O., & Simon, M. (2016) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2015.04.004 · Cited by 375 · see citing works
Somatostatin-Positive Gamma-Aminobutyric Acid Interneuron Deficits in Depression: Cortical Microcircuit and Therapeutic Perspectives
Fee, C., Banasr, M., & Sibille, E. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.05.024 · Cited by 329 · see citing works
Child abuse, depression, and methylation in genes involved with stress, neural plasticity, and brain circuitry
Weder, N., Zhang, H., Jensen, K., Yang, B. Z., Simen, A., Jackowski, A., Lipschitz, D., Douglas-Palumberi, H., Ge, M., Perepletchikova, F., et al. (2014) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2013.12.025 · Cited by 324 · see citing works
Microglial Dysregulation in Psychiatric Disease
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Is serotonin an upper or a downer? The evolution of the serotonergic system and its role in depression and the antidepressant response.
Andrews, P. W., Bharwani, A., Lee, K. R., Fox, M., & Thomson, J. A. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.01.018 · Cited by 281 · see citing works
Density of GFAP-immunoreactive astrocytes is decreased in left hippocampi in major depressive disorder
Cobb, J. A., O’Neill, K., Milner, J., Mahajan, G. J., Lawrence, T. J., May, W. L., Miguel-Hidalgo, J., Rajkowska, G., & Stockmeier, C. A. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2015.12.044 · Cited by 254 · see citing works
Genome-wide analysis of over 106 000 individuals identifies 9 neuroticism-associated loci
Smith, D. J., Escott-Price, V, Davies, G., Bailey, M. E. S., Colodro-Conde, L., Ward, J., Vedernikov, A., Marioni, R., Cullen, B., Lyall, D., et al. (2016) · Molecular Psychiatry · doi:10.1038/mp.2016.49 · Cited by 259 · see citing works
Conceptual convergence: increased inflammation is associated with increased basal ganglia glutamate in patients with major depression
Haroon, E., Fleischer, C. C., Felger, J. C., Chen, X., Woolwine, B. J., Patel, T., Hu, X. P., & Miller, A. H. (2016) · Molecular Psychiatry · doi:10.1038/mp.2015.206 · Cited by 250 · see citing works
From Serotonin to Neuroplasticity: Evolvement of Theories for Major Depressive Disorder
Liu, B., Liu, J., Wang, M., Zhang, Y., & Li, L. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00305 · Cited by 249 · see citing works
Emerging Role for Nucleus Accumbens Medium Spiny Neuron Subtypes in Depression
Francis, T. C., & Lobo, M. K. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.09.007 · Cited by 230 · see citing works
An astroglial basis of major depressive disorder? An overview
Wang, Q., Jie, W., Liu, J., Yang, J., & Gao, T. (2017) · Glia · doi:10.1002/glia.23143 · Cited by 222 · see citing works
Lanicemine: a low-trapping NMDA channel blocker produces sustained antidepressant efficacy with minimal psychotomimetic adverse effects
Sanacora, G., Smith, M. A., Pathak, S., Su, H.-L., Boeijinga, P. H., McCarthy, D. J., & Quirk, M. C. (2014) · Molecular Psychiatry · doi:10.1038/mp.2013.130 · Cited by 236 · see citing works
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Blood microRNA changes in depressed patients during antidepressant treatment
Bocchio-Chiavetto, L., Maffioletti, E., Bettinsoli, P., Giovannini, C., Bignotti, S., Tardito, D., Corrada, D., Milanesi, L., & Gennarelli, M. (2013) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2012.06.013 · Cited by 238 · see citing works
Chronic stress increases prefrontal inhibition: a mechanism for stress-induced prefrontal dysfunction
McKlveen, J. M., Morano, R. L., Fitzgerald, M., Zoubovsky, S., Cassella, S. N., Scheimann, J. R., Ghosal, S., Mahbod, P., Packard, B. A., Myers, B., et al. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.03.2101 · Cited by 224 · see citing works
Stratification of astrocytes in healthy and diseased brain
Verkhratsky, A., Zorec, R., & Parpura, V. (2017) · Brain Pathology · doi:10.1111/bpa.12537 · Cited by 236 · see citing works
Cellular and molecular basis for stress-induced depression
Seo, J.-S., Wei, J., Qin, L., Kim, Y., Yan, Z., & Greengard, P. (2017) · Molecular Psychiatry · doi:10.1038/mp.2016.118 · Cited by 235 · see citing works
Prefrontal excitatory/inhibitory balance in stress and emotional disorders: Evidence for over-inhibition
Page, C. E., & Coutellier, L. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.07.024 · Cited by 213 · see citing works
Neural correlates of change in major depressive disorder anhedonia following open-label ketamine
Lally, N., Nugent, A. C., Luckenbaugh, D. A., Niciu, M. J., Roiser, J. P., & Zarate, C. A. (2015) · Journal of Psychopharmacology · doi:10.1177/0269881114568041 · Cited by 224 · see citing works
The neurobiology of depression, ketamine and rapid-acting antidepressants: Is it glutamate inhibition or activation?
Abdallah, C. G., Sanacora, G., Duman, R. S., & Krystal, J. H. (2018) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2018.05.010 · Cited by 219 · see citing works
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Brain-derived neurotrophic factor Val66Met polymorphism and antidepressant efficacy of ketamine in depressed patients
Laje, G., Lally, N., Mathews, D., Brutsche, N., Chemerinski, A., Akula, N., Kelmendi, B., Simen, A., McMahon, F. J., Sanacora, G., et al. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.05.031 · Cited by 213 · see citing works
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Ketamine as an antidepressant: Overview of its mechanisms of action and potential predictive biomarkers
Matveychuk, D., Thomas, R. K., Swainson, J., Khullar, A., MacKay, M.-A., Baker, G. B., & Dursun, S. M. (2020) · Therapeutic Advances in Psychopharmacology · doi:10.1177/2045125320916657 · Cited by 209 · see citing works
The stressed synapse 2.0: pathophysiological mechanisms in stress-related neuropsychiatric disorders
Sanacora, G., Yan, Z., & Popoli, M. (2022) · Nature Reviews Neuroscience · doi:10.1038/s41583-021-00540-x · Cited by 197 · see citing works
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Fast-acting antidepressant activity of ketamine: Highlights on brain serotonin, glutamate, and GABA neurotransmission in preclinical studies
Pham, T. H., & Gardier, A. M. (2019) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2019.02.017 · Cited by 186 · see citing works
A new generation of antidepressants: an update on the pharmaceutical pipeline for novel and rapid-acting therapeutics in mood disorders based on glutamate/GABA neurotransmitter systems
Wilkinson, S. T., & Sanacora, G. (2019) · Drug Discovery Today · doi:10.1016/j.drudis.2018.11.007 · Cited by 173 · see citing works
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Glutamatergic Neurotransmission: Pathway to Developing Novel Rapid-Acting Antidepressant Treatments
Kadriu, B., Musazzi, L., Henter, I. D., Graves, M., Popoli, M., & Zarate, C. A. (2019) · International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyy094 · Cited by 165 · see citing works
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Ketamine enhances structural plasticity in mouse mesencephalic and human iPSC-derived dopaminergic neurons via AMPAR-driven BDNF and mTOR signaling
Cavalleri, L., Merlo Pich, E., Millan, M. J., Chiamulera, C., Kunath, T., Spano, P. F., & Collo, G. (2018) · Molecular Psychiatry · doi:10.1038/mp.2017.241 · Cited by 156 · see citing works
Serotonergic modulation of glutamate neurotransmission as a strategy for treating depression and cognitive dysfunction
Pehrson, A. L., & Sanchez, C. (2014) · CNS Spectrums · doi:10.1017/s1092852913000540 · Cited by 161 · see citing works
( 2R,6R )-hydroxynorketamine exerts mGlu 2 receptor-dependent antidepressant actions
Zanos, P., Highland, J. N., Stewart, B. W., Georgiou, P., Jenne, C. E., Lovett, J., Morris, P. J., Thomas, C. J., Moaddel, R., Zarate, C. A., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1819540116 · Cited by 152 · see citing works
IFN-Alpha-Induced Cortical and Subcortical Glutamate Changes Assessed by Magnetic Resonance Spectroscopy
Haroon, E., Woolwine, B. J., Chen, X., Pace, T. W., Parekh, S., Spivey, J. R., Hu, X. P., & Miller, A. H. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.25 · Cited by 154 · see citing works
Dysfunctional astrocytic and synaptic regulation of hypothalamic glutamatergic transmission in a mouse model of early-life adversity: relevance to neurosteroids and programming of the stress response
Gunn, B. G., Cunningham, L., Cooper, M. A., Corteen, N. L., Seifi, M., Swinny, J. D., Lambert, J. J., & Belelli, D. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.1337-13.2013 · Cited by 151 · see citing works
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Authors: Sanacora, G., Treccani, G., & Popoli, M.
Affiliations: Yale University (US)
University of Milan (IT)
Corresponding author: Popoli, Maurizio
ORCID: Sanacora, Gerard
Treccani, Giulia
Popoli, Maurizio
Venue: Neuropharmacology
Publisher: Elsevier BV
Published: 2012-01
Volume: 62
Issue: 1
Pages: 63-77
ISSN: 0028-3908 (ISSN-L)
DOI: 10.1016/j.neuropharm.2011.07.036
PMC: PMC3205453
OpenAlex: W72199885
Cited by: 1,036
References: 230
Citations by year: 2026: 48 · 2025: 61 · 2024: 66 · 2023: 74 · 2022: 80 · 2021: 80 · 2020: 89 · 2019: 67 · 2018: 62 · 2017: 66 · 2016: 83 · 2015: 90 · 2014: 71 · 2013: 55 · 2012: 38
FWCI: 6.75
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neuropharmacology (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Mental Health (R01MH081211, K02MH076222)
Topics: Health Sciences › Medicine › Pharmacology › Treatment of Major Depression
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords: depression, glutamate hypothesis, glutamatergic system, monoamine hypothesis, mood disorders, anxiety disorders, environmental stress, dendritic remodeling, synaptic loss, neuroplasticity, antidepressant mechanism, treatment-resistant depression, glutamate metabolism, limbic system
MeSH terms: Animals, Antidepressive Agents, Brain, Drug Evaluation, Preclinical, gamma-Aminobutyric Acid, Glucocorticoids, Humans, Synaptic Transmission, Magnetic Resonance Spectroscopy, Receptors, N-Methyl-D-Aspartate, Glutamic Acid, Mood Disorders

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Towards a glutamate hypothesis of depression

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