An excitatory synapse hypothesis of depression

Thompson, Scott M.; Kallarackal, Angy J.; Kvarta, Mark D.; Van Dyke, Adam M.; LeGates, Tara A.; Cai, Xiang

doi:10.1016/j.tins.2015.03.003

Cited by 267Treatment of Major DepressionNeuroscience and Neuropharmacology ResearchNeurotransmitter Receptor Influence on Behavior

An excitatory synapse hypothesis of depression

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Thompson, Scott M., Kallarackal, Angy J., Kvarta, Mark D., Van Dyke, Adam M., LeGates, Tara A., Cai, Xiang·2015·Trends in Neurosciences

DOI 10.1016/j.tins.2015.03.003PMC PMC4417609

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Abstract

Depression is a common cause of mortality and morbidity, but the biological bases of the deficits in emotional and cognitive processing remain incompletely understood. Current antidepressant therapies are effective in only some patients and act slowly. Here, we propose an excitatory synapse hypothesis of depression in which chronic stress and genetic susceptibility cause changes in the strength of subsets of glutamatergic synapses at multiple locations, including the prefrontal cortex (PFC), hippocampus, and nucleus accumbens (NAc), leading to a dysfunction of corticomesolimbic reward circuitry that underlies many of the symptoms of depression. This hypothesis accounts for current depression treatments and suggests an updated framework for the development of better therapeutic compounds.

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Stronger excitatory neurotransmission, especially via AMPARs, appears to be a shared requirement for antidepressant efficacy across classical and rapid-acting drugs.
“It appears that increased strength of excitatory neurotransmission, in particular involving AMPARs, represents a common downstream target that is necessary for antidepressant efficacy among classical and rapid-acting antidepressants (Alt et al., 2006; Gould et al., 2019; Thompson et al., 2015).”
From Mechanisms of ketamine and its metabolites as antidepressants (2022) · cites this paper as Thompson et al., 2015
The Formal statement of the excitatory synapse hypothesis (page unavailable) calls restoration of excitatory synaptic strength critical for both conventional antidepressants and ketamine. The Ketamine and NMDAR antagonists section says ketamine loses its antidepressant effect without functional AMPARs. The SSRIs section links their therapeutic effects to potentiated excitation, but does not establish that AMPAR involvement is necessary for classical antidepressants. (LLM, conf=0.86)
Experimental — accuracy not yet measured
The patterns observed in human patients are consistent with the premise that neuronal and molecular plasticity deficits may feed forward to impairments in the coordinated function of prefrontal and limbic regions, resulting in impaired PFC regulation and unchecked stimulus-driven responses to salient negative stimuli.
“Collectively, these patterns observed in human patients are consistent with the premise that neuronal and molecular plasticity deficits may feed forward to impairments in the coordinated function of prefrontal and limbic regions 66 , resulting in impaired PFC regulation and unchecked stimulus-driven responses to salient negative stimuli.”
From Neuroplasticity in cognitive and psychological mechanisms of depression: an integrative model (2020) · cites this paper as [66]
Split into 2 atoms — 1 confirmed, 1 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
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 [259]
The Prefrontal Cortex section reports that chronic stress causes PFC dendritic atrophy and spine loss in animal models, while the Stress and depression section links reduced PFC volume in depressed patients to pathophysiology. The paper supports the claim in the context of depression, but does not establish its broader application to neuropsychiatric conditions generally or that PFC changes are “equally important” relative to other changes. (LLM, conf=0.84)
Experimental — accuracy not yet measured
Conventional antidepressants including selective serotonin reuptake inhibitors, ketamine, and brain stimulation may alleviate depression by acting on excitatory brain systems.
“Conventional antidepressant therapeutics including selective serotonin reuptake inhibitors (SSRIs) or non-typical therapeutics, including ketamine and brain stimulation, may alleviate depression symptoms by acting on excitatory brain systems (33).”
From Emerging Role for Nucleus Accumbens Medium Spiny Neuron Subtypes in Depression (2017) · cites this paper as [33]
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 [33]

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Mechanisms of ketamine action as an antidepressant
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Impaired GABA synthesis, uptake and release are associated with depression-like behaviors induced by chronic mild stress
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“It is hypothesized that antidepressant-mediated synaptic potentiation occurs selectively in circuits that are abnormally weakened in depression (5, 123) (Figure 3).”
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GABAA receptors as targets for treating affective and cognitive symptoms of depression
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Prefrontal parvalbumin cells are sensitive to stress and mediate anxiety-related behaviors in female mice
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The Role of a Gut Microbial-Derived Metabolite, Trimethylamine N-Oxide (TMAO), in Neurological Disorders
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Negr1 controls adult hippocampal neurogenesis and affective behaviors
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Authors: Thompson, S. M., Kallarackal, A. J., Kvarta, M. D., Van Dyke, A. M., LeGates, T. A., & Cai, X.
Affiliations: University of Maryland, Baltimore (US)
Southern Illinois University Carbondale (US)
Corresponding author: Thompson, Scott M.
ORCID: Thompson, Scott M.
Kallarackal, Angy J.
Kvarta, Mark D.
LeGates, Tara A.
Cai, Xiang
Venue: Trends in Neurosciences
Publisher: Elsevier BV
Published: 2015-05
Volume: 38
Issue: 5
Pages: 279-294
ISSN: 0166-2236 (ISSN-L)
DOI: 10.1016/j.tins.2015.03.003
PMC: PMC4417609
OpenAlex: W2088861514
Cited by: 265
References: 203
Citations by year: 2026: 5 · 2025: 17 · 2024: 23 · 2023: 34 · 2022: 23 · 2021: 33 · 2020: 29 · 2019: 28 · 2018: 20 · 2017: 22 · 2016: 17 · 2015: 14
FWCI: 3.05
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Trends in Neurosciences (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health (2t32ns063391-21)
National Institute of Mental Health (R01MH086828)
National Institute of General Medical Sciences (T32GM008181, T32GM092237)
National Institute of Neurological Disorders and Stroke (T32NS007375, T32-NS063391)
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, glutamatergic synapses, chronic stress, genetic susceptibility, prefrontal cortex, hippocampus, nucleus accumbens, antidepressant treatment, synaptic plasticity
MeSH terms: Animals, Antidepressive Agents, Brain, Depression, Humans, Synapses, Excitatory Postsynaptic Potentials

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An excitatory synapse hypothesis of depression

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