Locally dynamic synaptic learning rules in pyramidal neuron dendrites
Open accessAbstract
Long-term potentiation (LTP) of synaptic transmission underlies aspects of learning and memory. LTP is input-specific at the level of individual synapses, but neural network models predict interactions between plasticity at nearby synapses. Here we show in mouse hippocampal pyramidal cells that LTP at individual synapses reduces the threshold for potentiation at neighbouring synapses. After input-specific LTP induction by two-photon glutamate uncaging or by synaptic stimulation, subthreshold stimuli, which by themselves were too weak to trigger LTP, caused robust LTP and spine enlargement at neighbouring spines. Furthermore, LTP induction broadened the presynaptic-postsynaptic spike interval for spike-timing-dependent LTP within a dendritic neighbourhood. The reduction in the threshold for LTP induction lasted approximately 10 min and spread over approximately 10 microm of dendrite. These local interactions between neighbouring synapses support clustered plasticity models of memory storage and could allow for the binding of behaviourally linked information on the same dendritic branch.
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Rho-Rock and Ras-ERK signaling pathways lower the threshold for LTP in neighboring spines.
“In addition, Rho-Rock and Ras-ERK signaling pathways lower the threshold for LTP in neighboring spines (Zhu et al., 2002; Harvey and Svoboda, 2007; Harvey et al., 2008; Lee et al., 2009).”
From Barriers in the brain: resolving dendritic spine morphology and compartmentalization (2014) · cites this paper as Harvey and Svoboda, 2007
The Abstract reports that LTP at one spine lowered the threshold for potentiation at neighboring spines. The Discussion (page unavailable) proposes a spreading intracellular signaling factor but does not identify Rho–ROCK or Ras–ERK as the pathways responsible. Thus the neighboring-spine effect is supported, but the named mechanism is not. (LLM, conf=0.88)
Experimental — accuracy not yet measuredLTP-inducing stimuli cause rapid addition of AMPARs to classical dendritic spines.
“These synapses contain AMPARs, but LTP-inducing stimuli cause a rapid addition of AMPARs to the synapse (246–250).”
From Synaptic memory and CaMKII (2023) · cites this paper as [246]
The passage labeled Abstract (page not provided) reports that LTP induction increased spine volume and synaptic current, and says spine volume is associated with the number of AMPA receptors in the postsynaptic density. It does not show that AMPARs were rapidly added to those synapses after stimulation; receptor addition was not directly measured. (LLM, conf=0.83)
Experimental — accuracy not yet measuredLTP can be induced at a single synapse without causing postsynaptic potentiation or depression of neighboring synapses.
“Experiments using this approach to induce NMDAR-dependent LTP have shown that LTP can be induced at a single synapse without causing postsynaptic potentiation or depression of neighboring synapses (Matsuzaki et al. 2004;Harvey and Svoboda 2007; but see Engert and Bonhoeffer 1997).”
From NMDA receptor-dependent long-term potentiation and long-term depression (LTP/LTD). (2012) · cites this paper as Harvey and Svoboda 2007
Spines associated with synapses that underwent LTP enlarge.
“Insertion of additional receptors therefore is likely to affect the ultrastructure of the synapse, and in fact, spines associated with synapses that underwent LTP enlarge (Matsuzaki et al. 2004;Harvey and Svoboda 2007;Holtmaat and Svoboda 2009;Kasai et al. 2010).”
From NMDA receptor-dependent long-term potentiation and long-term depression (LTP/LTD). (2012) · cites this paper as Harvey and Svoboda 2007
Two-photon glutamate uncaging experiments on single spines indicate that synapses that already express functional AMPARs can be further enhanced by inducing LTP.
“Furthermore, two-photon glutamate uncaging experiments on single spines indicate that synapses that already express functional AMPARs can be further enhanced by inducing LTP (246–248).”
From Synaptic memory and CaMKII (2023) · cites this paper as [246]
Uncaging glutamate near the tip of a single dendritic spine results in a coordinated increase in spine volume and enhanced synaptic function lasting for more than an hour.
“Uncaging glutamate near the tip of a single dendritic spine [single spine glutamate uncaging (SSGU)] results in a coordinated increase in spine volume and enhanced synaptic function lasting for more than an hour (20, 21).”
From Synaptic evidence for the efficacy of spaced learning (2012) · cites this paper as [20]
Induction of plasticity at a single spine transiently lowers the plasticity threshold at adjacent spines.
“Recent studies have shown that induction of plasticity at a single spine transiently lowers the plasticity threshold at adjacent spines (20).”
From Synaptic evidence for the efficacy of spaced learning (2012) · cites this paper as [20]
This form of plasticity shares many properties with Schaffer collateral LTP, including dependence on NMDARs, Rho GTPase signaling, CaMKII phosphorylation, F-actin polymerization and synaptic AMPAR insertion.
“This form of plasticity shares many properties with Schaffer collateral LTP, including dependence on N-methyl-d-aspartate receptors (NMDARs), Rho GTPase signaling, Ca2+/calmodulin-dependent protein kinase II (CaMKII) phosphorylation, F-actin polymerization and synaptic AMPAR insertion (20–24).”
From Synaptic evidence for the efficacy of spaced learning (2012) · cites this paper as [20]
The low success rate in adults was unlikely related to technical issues because a strong induction protocol caused structural plasticity in >80% of young spines.
“The low success rate in adults was unlikely related to technical issues because we used a strong induction protocol (20) that caused structural plasticity in >80% of young spines (Fig. 3C), a value in good agreement with previous studies (20, 21).”
From Synaptic evidence for the efficacy of spaced learning (2012) · cites this paper as [20]
Uncaged glutamate is known from past work to produce robust, NMDAR-dependent excitatory responses at nearly all spines under the conditions used in our experiments.
“Notably, uncaged glutamate is known from past work to produce robust, NMDAR-dependent excitatory responses at nearly all spines (20, 21) under the conditions used in our experiments.”
From Synaptic evidence for the efficacy of spaced learning (2012) · cites this paper as [20]
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- Authors
- Harvey, C. D., & Svoboda, K.
- Affiliations
- Howard Hughes Medical Institute (US)
- Corresponding author
- Svoboda, Karel
- Venue
- Nature
- Published
- 2007-12
- Volume
- 450
- Issue
- 7173
- Pages
- 1195-1200
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC3425382
- OpenAlex
- W2118069376
- Cited by
- 625
- References
- 53
- Citations by year
- 2026: 20 · 2025: 22 · 2024: 34 · 2023: 34 · 2022: 22 · 2021: 27 · 2020: 24 · 2019: 31 · 2018: 28 · 2017: 32 · 2016: 36 · 2015: 32 · 2014: 48 · 2013: 43 · 2012: 40
- FWCI
- 15.33
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Cold Spring Harbor Laboratory Institutional Repository (Cold Spring Harbor Laboratory) (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- 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
- long-term potentiation, synaptic plasticity, dendritic plasticity, hippocampal pyramidal neurons, dendritic spines, spike-timing-dependent plasticity, synaptic interactions, glutamate uncaging, memory storage, information integration
- MeSH terms
- Animals, Dendrites, Learning, Models, Neurological, Synapses, Long-Term Potentiation, Pyramidal Cells, Glutamic Acid, Excitatory Postsynaptic Potentials, Mice, In Vitro Techniques
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