Local potentiation of excitatory synapses by serotonin and its alteration in rodent models of depression
Open accessAbstract
The causes of major depression remain unknown. Antidepressants elevate concentrations of monoamines, particularly serotonin, but it remains uncertain which downstream events are critical to their therapeutic effects. We found that endogenous serotonin selectively potentiated excitatory synapses formed by the temporoammonic pathway with CA1 pyramidal cells via activation of serotonin receptors (5-HT(1B)Rs), without affecting nearby Schaffer collateral synapses. This potentiation was expressed postsynaptically by AMPA-type glutamate receptors and required calmodulin-dependent protein kinase-mediated phosphorylation of GluA1 subunits. Because they share common expression mechanisms, long-term potentiation and serotonin-induced potentiation occluded each other. Long-term consolidation of spatial learning, a function of temporoammonic-CA1 synapses, was enhanced by 5-HT(1B)R antagonists. Serotonin-induced potentiation was quantitatively and qualitatively altered in a rat model of depression, restored by chronic antidepressants, and required for the ability of chronic antidepressants to reverse stress-induced anhedonia. Changes in serotonin-mediated potentiation, and its recovery by antidepressants, implicate excitatory synapses as a locus of plasticity in depression.
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Dopamine, norepinephrine, and serotonin signaling are linked to AMPAR strengthening via phosphorylation and membrane insertion, likely contributing to ketamine's antidepressant effects.
“dopamine, norepinephrine, and serotonin signaling have all been associated with strengthening AMPAR signaling through phosphorylation and membrane insertion which likely contribute to the antidepressant effects of ketamine (Cai et al., 2013; Diering & Huganir, 2018; Hu et al., 2007; Sun et al., 2005).”
From Mechanisms of ketamine and its metabolites as antidepressants (2022) · cites this paper as Cai et al., 2013
The Results section (‘Molecular basis of 5-HT-mediated potentiation’; page not supplied) reports that serotonin strengthens AMPA receptor responses through CaMK-dependent GluA1 phosphorylation. It does not establish membrane insertion or the same AMPAR mechanism for dopamine or norepinephrine. The Discussion mentions ketamine’s potentiation of excitatory synapses, but does not link the serotonin mechanism to ketamine’s antidepressant effects. (LLM, conf=0.88)
Experimental — accuracy not yet measuredMice with GluA1 that cannot be phosphorylated by CaMK, impairing synaptic insertion, show sucrose preference and novelty suppressed feeding changes identical to chronic stress.
“Mice in which the GluA1 gene cannot be phosphorylated by calcium/ calmodulin-dependent kinase (CaMK), thereby impairing their insertion into synapses, display altered behavior in the sucrose preference and novelty suppressed feeding tests, identical to those produced by chronic stress [44].”
From Plasticity of synapses and reward circuit function in the genesis and treatment of depression (2023) · cites this paper as [44]
Chronic, but not acute, fluoxetine restores stress-weakened TA-CA1 excitatory synapse strength and normal hedonic behavior.
“We have observed that chronic, but not acute, administration of fluoxetine restores the strength of stress-weakened TA-CA1 excitatory synapses, concomitant with the recovery of normal hedonic behavior [44,120].”
From Plasticity of synapses and reward circuit function in the genesis and treatment of depression (2023) · cites this paper as [44]
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- Authors
- Cai, X., Kallarackal, A. J., Kvarta, M. D., Goluskin, S., Gaylor, K., Bailey, A. M., Lee, H.-K., Huganir, R. L., & Thompson, S. M.
- Affiliations
- University of Maryland, Baltimore (US)
- St. Mary's College of Maryland (US)
- Johns Hopkins University (US)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Thompson, Scott M
- ORCID
- Venue
- Nature Neuroscience
- Published
- 2013-03-17
- Volume
- 16
- Issue
- 4
- Pages
- 464-472
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC3609911
- OpenAlex
- W2142688387
- Cited by
- 180
- References
- 52
- Citations by year
- 2026: 8 · 2025: 14 · 2024: 18 · 2023: 10 · 2022: 10 · 2021: 14 · 2020: 16 · 2019: 10 · 2018: 13 · 2017: 12 · 2016: 18 · 2015: 16 · 2014: 15 · 2013: 6
- FWCI
- 9.00
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institute of Mental Health (R01MH086828)
- National Institute of General Medical Sciences (T32GM008181)
- National Institute of Neurological Disorders and Stroke (R01NS036715)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Health Sciences › Medicine › Pharmacology › Treatment of Major Depression
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- serotonin, 5-HT1B receptor, temporoammonic pathway, CA1 pyramidal neurons, hippocampus, chronic unpredictable mild stress, depression, fluoxetine, antidepressants, AMPA receptors, GluA1 phosphorylation, calcium/calmodulin-dependent protein kinase, long-term potentiation, spatial learning, anhedonia, synaptic plasticity
- MeSH terms
- Animals, Antidepressive Agents, Depression, Disease Models, Animal, Male, Mice, Inbred C57BL, Random Allocation, Serotonin, Synapses, Rats, Sprague-Dawley, Long-Term Potentiation, Excitatory Postsynaptic Potentials, Mice, Rats, Mice, 129 Strain, Serotonin 5-HT1 Receptor Antagonists
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