The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission

Popoli, Maurizio; Yan, Zhen; McEwen, Bruce S.; Sanacora, Gerard

doi:10.1038/nrn3138

Cited by 1,393Stress Responses and CortisolNeuroscience and Neuropharmacology ResearchNeurotransmitter Receptor Influence on Behavior

The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission

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Popoli, Maurizio, Yan, Zhen, McEwen, Bruce S., Sanacora, Gerard·2012·Nature Reviews Neuroscience

DOI 10.1038/nrn3138PMC PMC3645314

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Abstract

Mounting evidence suggests that acute and chronic stress, especially the stress-induced release of glucocorticoids, induces changes in glutamate neurotransmission in the prefrontal cortex and the hippocampus, thereby influencing some aspects of cognitive processing. In addition, dysfunction of glutamatergic neurotransmission is increasingly considered to be a core feature of stress-related mental illnesses. Recent studies have shed light on the mechanisms by which stress and glucocorticoids affect glutamate transmission, including effects on glutamate release, glutamate receptors and glutamate clearance and metabolism. This new understanding provides insights into normal brain functioning, as well as the pathophysiology and potential new treatments of stress-related neuropsychiatric disorders.

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Somatostatin regulates ACTH secretion and loss of somatostatin-expressing interneurons increases glucocorticoid signaling and glutamate neurotransmission in the hippocampus.
“Somatostatin regulates ACTH secretion and loss of somatostatin-expressing interneurons increases glucocorticoid signaling and glutamate neurotransmission in the hippocampus (147).”
From Chronic stress, neuroinflammation, and depression: an overview of pathophysiological mechanisms and emerging anti-inflammatories (2023) · cites this paper as [147]
The Introduction and the section on acute stress and glutamate release report that glucocorticoids can increase glutamate release in the hippocampus. The paper does not support the attributed link to loss of somatostatin-expressing interneurons, or the statement that somatostatin regulates ACTH secretion (searched: somatostatin, ACTH secretion, interneuron loss). (LLM, conf=0.83)
Experimental — accuracy not yet measured
Traumatic stress causes trophic changes and synaptogenesis in the amygdala.
“The research conducted by Popoli et al. (2011) showed that traumatic stress causes trophic changes and synaptogenesis in the amygdala.”
From Neuroimaging research in posttraumatic stress disorder – Focus on amygdala, hippocampus and prefrontal cortex (2019) · cites this paper as Popoli et al. (2011)
In the section on stress and glucocorticoid effects on glutamatergic transmission (page not available), the review says a single traumatic stressor causes basolateral amygdala neurons to grow new spines over 10 days. It also reports amygdala neuronal growth after chronic stress, but explicitly says the single traumatic stressor did not cause dendritic growth. The passage supports stress-related structural change, but does not establish synaptogenesis or the broader trophic changes attributed to traumatic stress. (LLM, conf=0.82)
Experimental — accuracy not yet measured
Trauma and stress induce synaptic degeneration and neuronal atrophy in the hippocampus.
“Trauma and stress induce synaptic degeneration, and neuronal atrophy in the hippocampus (Popoli et al., 2011)”
From Neuroimaging research in posttraumatic stress disorder – Focus on amygdala, hippocampus and prefrontal cortex (2019) · cites this paper as Popoli et al., 2011
The section on stress and glutamatergic transmission (page unavailable) reports that chronic stress causes dendritic shrinkage in hippocampal CA3 and spine loss in CA1. It also says that head trauma can cause irreversible hippocampal damage, but does not specify that trauma causes both synaptic degeneration and neuronal atrophy. The claim omits the chronic-stress qualifier. (LLM, conf=0.84)
Experimental — accuracy not yet measured
Stress-induced structural changes in the PFC contribute to the pathophysiology of neuropsychiatric conditions.
“Although stress-induced structural changes in the PFC are equally important in their contribution to the pathophysiology of neuropsychiatric conditions [256–262]”
From Development of prefrontal cortex (2022) · cites this paper as [257]
The section on stress effects reports chronic-stress-induced dendritic shrinkage and spine loss in the medial PFC, and the Introduction says impaired PFC plasticity is thought to be a core feature of several neuropsychiatric disorders. The Conclusions link stress-related synaptic changes to psychiatric pathophysiology more cautiously; they do not establish that the PFC structural changes themselves contribute to it, or that their contribution is ‘equally important.’ No page numbers are available in our copy. (LLM, conf=0.84)
Experimental — accuracy not yet measured
In animals, chronic stress results in prolonged release of glucocorticoids and leads to hypertrophy of the amygdala and nucleus accumbens, atrophy of the hippocampus and prefrontal cortex, and functional impairment of the PFC.
“In animals, chronic stress results in the prolonged release of glucocorticoids and leads to hypertrophy of the amygdala and nucleus accumbens, atrophy of the hippocampus and prefrontal cortex (PFC), and functional impairment of the PFC (44–55).”
From Psychedelics and Other Psychoplastogens for Treating Mental Illness. (2021) · cites this paper as [51]
In the section on stress and glucocorticoid effects on glutamatergic transmission (page unavailable), the review reports chronic-stress-related dendritic shrinkage in the hippocampus and medial PFC, growth of basolateral amygdala neurons, and disruption of PFC-dependent tasks. It does not report chronic-stress-induced hypertrophy of the nucleus accumbens or establish that chronic stress causes prolonged glucocorticoid release; its discussion of prolonged release concerns glutamate. (LLM, conf=0.88)
Experimental — accuracy not yet measured

Neurotransmitters such as glutamate, serotonin, and γ-aminobutyric acid (GABA) are involved in stress signal transmission.
“Neurotransmitters such as glutamate, serotonin (89), and γ-aminobutyric acid (GABA) are involved in this signal transmission.”
From Epigenetic Modifications in Stress Response Genes Associated With Childhood Trauma (2019) · cites this paper as [89]
Overwhelming evidence indicates PFC is uniquely important brain region for highest level of executive function, which drives self-regulatory and goal-directed behaviors.
“Overwhelming evidence has indicated that PFC is a uniquely important brain region for the highest level of excecutive function, which drives self-regulatory and goal-directed behaviors 261–263.”
From Mechanisms of synaptic transmission dysregulation in the prefrontal cortex: pathophysiological implications (2022) · cites this paper as [262]
Functional connectivity results from activity of synapses, and is hence modulated by the number of synapses and the robustness of their function.
“Functional connectivity results from activity of synapses, and is hence modulated by the number of synapses and the robustness of their function.126,127”
From Preferential loss of dorsal-hippocampus synapses underlies memory impairments provoked by short, multimodal stress (2014) · cites this paper as [127]
Increased glutamate levels have been associated with mechanisms involved in stress and depression, such as neuro-inflammatory process, decreased levels of neurotrophic factors, diminished neurogenesis, and neuroplasticity impairment.
“Importantly, increased glutamate levels has been associated with mechanisms involved in stress and depression, such as neuro-inflammatory process, decreased levels of neurotrophic factors, diminished neurogenesis, and neuroplasticity impairment [116,117].”
From P2X7 Receptor Signaling in Stress and Depression (2019) · cites this paper as [116]
Postsynaptic expression of AMPA and NMDA is enhanced under acute stress and corticosterone treatment.
“In contrast, postsynaptic expression of AMPA and NMDA is enhanced under acute stress and corticosterone treatment (Popoli et al., 2011).”
From Glutamate receptors in domestication and modern human evolution (2020) · cites this paper as Popoli et al., 2011
The prefrontal cortex and hippocampus are more sensitive than the hypothalamus to inflammation and the neurotoxic effects of GCs.
“For example, the prefrontal cortex and hippocampus were both found to be more sensitive than the hypothalamus to inflammation and the neurotoxic effects of GCs (142, 143, 159).”
From The HPA â€“ Immune Axis and the Immunomodulatory Actions of Glucocorticoids in the Brain (2014) · cites this paper as [159]
Glia play an important role in regulating the synthesis and reuptake of glutamate and thereby influence synaptic function and morphology.
“Glia also play an important role in regulating the synthesis and reuptake of glutamate and thereby influence synaptic function and morphology16,17.”
From Synaptic plasticity and depression: new insights from stress and rapid-acting antidepressants (2016) · cites this paper as [17]
Glucocorticoids produce effects in the brain both genomically and non-genomically via multiple sites and pathways, and they have biphasic effects in which the timing and level of glucocorticoid receptor expression are critical.
“Glucocorticoids produce effects in the brain both genomically and non-genomically via multiple sites and pathways, and they have biphasic effects in which the timing and the level of glucocorticoid response (GR) expression are critical.”
From Neurobiological and Systemic Effects of Chronic Stress (2017) · cites this paper as [26]
Corticosterone acts directly via membrane-associated mineralocorticoid receptors and glucocorticoid receptors to cause glutamate release.
“Indeed, corticosterone acts directly via membrane associated mineralocorticoid receptors (MR) and GR to cause glutamate release.”
From Neurobiological and Systemic Effects of Chronic Stress (2017) · cites this paper as [26]

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“This process could be involved in the cellular change”
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Stress at Learning Facilitates Memory Formation by Regulating AMPA Receptor Trafficking Through a Glucocorticoid Action
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TNF-α potentiates glutamate-induced spinal cord motoneuron death via NF-κB
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Synaptic plasticity and depression: new insights from stress and rapid-acting antidepressants
Duman, R. S., Aghajanian, G. K., Sanacora, G., & Krystal, J. H. (2016) · Nature Medicine · doi:10.1038/nm.4050 · Cited by 1,750 · see citing works
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Stress Effects on Neuronal Structure: Hippocampus, Amygdala, and Prefrontal Cortex
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Mechanisms of stress in the brain
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Childhood adversity and neural development: Deprivation and threat as distinct dimensions of early experience
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“Glucocorticoids produce effects in the brain both genomically and non-genomically via multiple sites and pathways, and they have biphasic effects in which the timing and the level of glucocorticoid response (GR) expression are critical.(25,26) Glucocorticoid actions via the genome involve both direct interactions with…”
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Altered Connectivity in Depression: GABA and Glutamate Neurotransmitter Deficits and Reversal by Novel Treatments
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Social influences on neuroplasticity: stress and interventions to promote well-being
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The Semantics of Microglia Activation: Neuroinflammation, Homeostasis, and Stress
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Neurobiological Interactions Between Stress and the Endocannabinoid System
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The organization of the stress system and its dysregulation in depressive illness
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Sustained rescue of prefrontal circuit dysfunction by antidepressant-induced spine formation
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The effects of aging in the hippocampus and cognitive decline
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The Role of Genes, Stress, and Dopamine in the Development of Schizophrenia
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Glucocorticoids and fetal programming part 1: outcomes
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Chronic stress, neuroinflammation, and depression: an overview of pathophysiological mechanisms and emerging anti-inflammatories
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“Somatostatin regulates ACTH secretion and loss of somatostatinexpressing interneurons increases glucocorticoid signaling and glutamate neurotransmission in the hippocampus (147).”
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A conceptual framework for the neurobiological study of resilience
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Neural Mechanisms of Stress Resilience and Vulnerability
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Targeting glutamate signalling in depression: progress and prospects
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Dendritic Spines in Depression: What We Learned from Animal Models
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Neuropathology of stress
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Ketamine and Rapid-Acting Antidepressants: A Window into a New Neurobiology for Mood Disorder Therapeutics
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Unraveling the Time Domains of Corticosteroid Hormone Influences on Brain Activity: Rapid, Slow, and Chronic Modes
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The HPA â€“ Immune Axis and the Immunomodulatory Actions of Glucocorticoids in the Brain
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Pharmacology of cognitive enhancers for exposure-based therapy of fear, anxiety and trauma-related disorders
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Development of prefrontal cortex
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Coping with the Forced Swim Stressor: Towards Understanding an Adaptive Mechanism
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Circadian glucocorticoid oscillations promote learning-dependent synapse formation and maintenance.
Liston, C., Cichon, J. M., Jeanneteau, F., Jia, Z., Chao, M. V., & Gan, W.-B. (2013) · Nature Neuroscience · doi:10.1038/nn.3387 · Cited by 358 · see citing works
Revisiting the roles of progesterone and allopregnanolone in the nervous system: Resurgence of the progesterone receptors
Schumacher, M., Mattern, C., Ghoumari, A. M., Oudinet, J., Lière, P., Labombarda, F., Sitruk-Ware, R. L., Nicola, A. F. D., & Guennoun, R. (2013) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2013.09.004 · Cited by 353 · see citing works
The Consequences of Early‐Life Adversity: Neurobiological, Behavioural and Epigenetic Adaptations
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Glucocorticoid actions on synapses, circuits, and behavior: Implications for the energetics of stress
Myers, B., McKlveen, J. M., & Herman, J. P. (2014) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2013.12.003 · Cited by 318 · see citing works
Role of BDNF in the Pathophysiology and Treatment of Depression: Activity-Dependent Effects Distinguish Rapid-Acting Antidepressants
Duman, R. S., Deyama, S., & Fogaça, M. V. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.14630 · Cited by 321 · see citing works
Adolescent Stress–Induced Epigenetic Control of Dopaminergic Neurons via Glucocorticoids
Niwa, M., Jaaro-Peled, H., Tankou, S., Seshadri, S., Hikida, T., Matsumoto, Y., Cascella, N. G., Kano, S.-I., Ozaki, N., Nabeshima, T., et al. (2013) · Science · doi:10.1126/science.1226931 · Cited by 318 · see citing works
Stress and glucocorticoid receptor-dependent mechanisms in long-term memory: From adaptive responses to psychopathologies
Finsterwald, C., & Alberini, C. M. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.09.017 · Cited by 311 · see citing works
Synaptic plasticity in depression: Molecular, cellular and functional correlates
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The neural diathesis-stress model of schizophrenia revisited: an update on recent findings considering illness stage and neurobiological and methodological complexities
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Non-Genetic Factors in Schizophrenia
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Neurosteroids as novel antidepressants and anxiolytics: GABA-A receptors and beyond
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Mechanisms of synaptic transmission dysregulation in the prefrontal cortex: pathophysiological implications
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Caffeine acts through neuronal adenosine A <sub>2A</sub> receptors to prevent mood and memory dysfunction triggered by chronic stress
Kaster, M. P., Machado, N. J., Silva, H. B., Nunes, A., Ardais, A. P., Santana, M., Baqi, Y., Müller, C. E., Rodrigues, A. L. S., Porciúncula, L. O., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1423088112 · Cited by 312 · see citing works
Microglia, Lifestyle Stress, and Neurodegeneration
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Social Isolation Stress Induces Anxious-Depressive-Like Behavior and Alterations of Neuroplasticity-Related Genes in Adult Male Mice
Ieraci, A., Mallei, A., & Popoli, M. (2016) · Neural Plasticity · doi:10.1155/2016/6212983 · Cited by 294 · see citing works
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Recognizing resilience: Learning from the effects of stress on the brain
McEwen, B. S., Gray, J. D., & Nasca, C. (2015) · Neurobiology of Stress · doi:10.1016/j.ynstr.2014.09.001 · Cited by 292 · see citing works
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Authors: Popoli, M., Yan, Z., McEwen, B. S., & Sanacora, G.
Affiliations: University of Milan (IT)
University at Buffalo, State University of New York (US)
Rockefeller University (US)
Yale University (US)
Corresponding author: Sanacora, Gerard
ORCID: Popoli, Maurizio
Yan, Zhen
McEwen, Bruce S.
Sanacora, Gerard
Venue: Nature Reviews Neuroscience
Publisher: Springer Science and Business Media LLC
Published: 2011-11-30
Volume: 13
Issue: 1
Pages: 22-37
ISSN: 1471-003X (ISSN-L)
1471-0048
DOI: 10.1038/nrn3138
PMC: PMC3645314
OpenAlex: W2031598294
Cited by: 1,393
References: 231
Citations by year: 2026: 90 · 2025: 88 · 2024: 80 · 2023: 98 · 2022: 92 · 2021: 118 · 2020: 125 · 2019: 118 · 2018: 105 · 2017: 118 · 2016: 84 · 2015: 86 · 2014: 86 · 2013: 57 · 2012: 44
FWCI: 5.20
Type: journal article
Language: en
Open access: green
europepmc.org
Licence: www.springer.com/tdm (tdm)
Locations: Nature reviews. Neuroscience (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Mental Health (MH-41256, R01MH085774, R37MH041256, P50MH058911, R01MH081211, R01MH084233, R01MH041256, R01MH071676, MH85774, MH84233, 5-P50MH58911)
Topics: Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords: stress, glucocorticoids, glutamatergic neurotransmission, prefrontal cortex, hippocampus, stress-related neuropsychiatric disorders, glutamate release, glutamate receptors, glutamate clearance, glutamate metabolism, cognitive processes, chronic stress, acute stress
MeSH terms: Animals, Brain, Glucocorticoids, Humans, Models, Neurological, Neuroglia, Neurons, Stress, Psychological, Synapses, Glutamic Acid

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The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission

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