Short-Term Plasticity at Hippocampal Mossy Fiber Synapses Is Induced by Natural Activity Patterns and Associated with Vesicle Pool Engram Formation
Open accessAbstract
Post-tetanic potentiation (PTP) is an attractive candidate mechanism for hippocampus-dependent short-term memory. Although PTP has a uniquely large magnitude at hippocampal mossy fiber-CA3 pyramidal neuron synapses, it is unclear whether it can be induced by natural activity and whether its lifetime is sufficient to support short-term memory. We combined in vivo recordings from granule cells (GCs), in vitro paired recordings from mossy fiber terminals and postsynaptic CA3 neurons, and "flash and freeze" electron microscopy. PTP was induced at single synapses and showed a low induction threshold adapted to sparse GC activity in vivo. PTP was mainly generated by enlargement of the readily releasable pool of synaptic vesicles, allowing multiplicative interaction with other plasticity forms. PTP was associated with an increase in the docked vesicle pool, suggesting formation of structural "pool engrams." Absence of presynaptic activity extended the lifetime of the potentiation, enabling prolonged information storage in the hippocampal network.
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High-frequency stimulation induces several cAMP-dependent forms of presynaptic plasticity.
“For example, high-frequency stimulation (HFS) induces several cyclic adenosine monophosphate (cAMP)-dependent forms of presynaptic plasticity [21,28–33].”
From Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons (2024) · cites this paper as [21]
The Results sections “Superbursts in GCs Induce PTP” and “Pool Refilling Determines PTP” report that high-frequency stimulation induces post-tetanic potentiation (PTP) at hippocampal mossy fiber synapses and that PTP involves the cAMP–PKA pathway (page numbers unavailable). The cited paper therefore supports one cAMP-dependent form of presynaptic plasticity, but it does not establish that stimulation induces several such forms. (LLM, conf=0.88)
Experimental — accuracy not yet measuredBoth short- and long-term mechanisms may involve the formation of vesicle pool engrams.
“Thus, both short- and long-term mechanisms may involve the formation of vesicle pool engrams [21].”
From Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons (2024) · cites this paper as [21]
The Discussion (page not provided) links short-term post-tetanic potentiation to a vesicle-pool mechanism and suggests that changes in docked vesicles may contribute to engram formation. The cited passages do not establish that long-term mechanisms involve vesicle pool engrams; the Results examine persistence over minutes, not a long-term mechanism. (LLM, conf=0.86)
Experimental — accuracy not yet measuredFacilitation and PTP may lead to conditional detonation or plasticity-dependent detonation at this synapse.
“Previous work showed that facilitation and PTP may lead to conditional detonation or plasticity-dependent detonation at this synapse [21,51].”
From Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons (2024) · cites this paper as [21]
The Discussion (page unavailable) says mossy fiber plasticity can change transmission modes: increased release probability may enable burst-to-spike transmission, while increased readily releasable pool size could facilitate burst-to-burst transmission. It links the latter pool change to PTP, but does not specifically say that facilitation and PTP produce conditional or plasticity-dependent detonation. (LLM, conf=0.79)
Experimental — accuracy not yet measuredChemical potentiation primarily involves an increase in pool size but also an increase in Pr, reminiscent of hippocampal mossy fiber PTP.
“Thus, chemical potentiation primarily involved an increase in pool size but also an increase in Pr, reminiscent of hippocampal mossy fiber PTP [21].”
From Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons (2024) · cites this paper as [21]
The mossy fiber-CA3 PN synapse has a unique extent of presynaptic plasticity, including facilitation, post-tetanic potentiation, and long-term potentiation.
“Second, it has a unique extent of presynaptic plasticity, including facilitation, post-tetanic potentiation (PTP) [21], and long-term potentiation (LTP) [27].”
From Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons (2024) · cites this paper as [21]
The H-89-induced increase in WPD is consistent with a decrease in strength of synaptic transmission after H-89 application.
“This is consistent with a decrease in strength of synaptic transmission after H-89 application [21].”
From Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons (2024) · cites this paper as [21]
Baseline activity of cAMP-PKA signaling pathway is important for coupling distance, basal synaptic transmission, and the induction of presynaptic potentiation.
“Moreover, our results revealed that baseline activity of cAMP-PKA signaling pathway is important for coupling distance, basal synaptic transmission, and the induction of presynaptic potentiation, as the application of PKA antagonists led to “uncoupling” of Munc13-1 and CaV2.1 (Figs 5 and S9) and a decrease in synaptic strength [21].”
From Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons (2024) · cites this paper as [21]
Changes in both RRP and Pr have been reported during post-tetanic potentiation (PTP).
“Changes in both RRP and Pr have been also reported during PTP [21].”
From Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons (2024) · cites this paper as [21]
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- Authors
- Vandael, D., Borges-Merjane, C., Zhang, X., & Jonas, P.
- Affiliations
- Institute of Science and Technology Austria (AT)
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2020-08
- Volume
- 107
- Issue
- 3
- Pages
- 509-521.e7
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC7427323
- OpenAlex
- W3032084133
- Cited by
- 114
- References
- 80
- Citations by year
- 2026: 16 · 2025: 13 · 2024: 17 · 2023: 24 · 2022: 15 · 2021: 23 · 2020: 6
- FWCI
- 7.79
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Neuron (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Funders
- Horizon 2020 (692692)
- European Research Council
- Austrian Science Fund (V 739-B27, Z 312-B27)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- post-tetanic potentiation, short-term plasticity, mossy fiber synapses, hippocampus, CA3 pyramidal cells, granule cells, synaptic vesicle pools, readily releasable pool, docked vesicles, short-term memory, synaptic plasticity, presynaptic activity
- MeSH terms
- Action Potentials, Animals, Memory, Short-Term, Microscopy, Electron, Neuronal Plasticity, Synapses, Synaptic Vesicles, Pyramidal Cells, Patch-Clamp Techniques, Dentate Gyrus, Mossy Fibers, Hippocampal, Mice, Rats, Synaptic Potentials, CA3 Region, Hippocampal
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