The DOI matches its Crossref record; 25 of the 25 references it cites were found in a registry or an index.
Synaptic tagging and long-term potentiation
Abstract
Repeated stimulation of hippocampal neurons can induce an immediate and prolonged increase in synaptic strength that is called long-term potentiation (LTP)-the primary cellular model of memory in the mammalian brain. An early phase of LTP (lasting less than three hours) can be dissociated from late-phase LTP by using inhibitors of transcription and translation, Because protein synthesis occurs mainly in the cell body, whereas LTP is input-specific, the question arises of how the synapse specificity of late LTP is achieved without elaborate intracellular protein trafficking. We propose that LTP initiates the creation of a short-lasting protein-synthesis-independent 'synaptic tag' at the potentiated synapse which sequesters the relevant protein(s) to establish late LTP. In support of this idea, we now show that weak tetanic stimulation, which ordinarily leads only to early LTP, or repeated tetanization in the presence of protein-synthesis inhibitors, each results in protein-synthesis-dependent late LTP, provided repeated tetanization has already been applied at another input to the same population of neurons. The synaptic tag decays in less than three hours. These findings indicate that the persistence of LTP depends not only on local events during its induction, but also on the prior activity of the neuron.
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“BDNF action was selective on the spines that showed immediate enlargement, which may act as the structural tag for selective trapping (26) of the protein-synthetic machinery (11, 27) and the capture of plasticity proteins (2, 28) for long-term spine-head enlargement.”
From Protein synthesis and neurotrophin-dependent structural plasticity of single dendritic spines (2008) · cites this paper as [28]
In the citing paper
“stronger stimulation produces the dopamine-dependent protein synthesis that allows late LTP.”
From A neoHebbian framework for episodic memory; role of dopamine-dependent late LTP (2011) · cites this paper as [9]
In the citing paper
“According to this model, weak stimulation induces only early LTP.”
From A neoHebbian framework for episodic memory; role of dopamine-dependent late LTP (2011) · cites this paper as [9]
In the citing paper
“However, the synapses that produce the PRPs can be different from those at which the tag is set.”
From A neoHebbian framework for episodic memory; role of dopamine-dependent late LTP (2011) · cites this paper as [9]
Citations
Cites
A synaptic model of memory: long-term potentiation in the hippocampus
Bliss, T. V. P., & Collingridge, G. L. (1993) · Nature · doi:10.1038/361031a0 · Cited by 11,566
Metaplasticity: the plasticity of synaptic plasticity
Abraham, W. C., & Bear, M. F. (1996) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)80018-x · Cited by 1,833
Brown, R., & Kulik, J. (1977) · Cognition · doi:10.1016/0010-0277(77)90018-x · Cited by 1,373
A Requirement for Local Protein Synthesis in Neurotrophin-Induced Hippocampal Synaptic Plasticity
Kang, H., & Schuman, E. M. (1996) · Science · doi:10.1126/science.273.5280.1402 · Cited by 996
Requirement of a Critical Period of Transcription for Induction of a Late Phase of LTP
Nguyen, P. V., Abel, T., & Kandel, E. R. (1994) · Science · doi:10.1126/science.8066450 · Cited by 888
Frey, U., Krug, M., Reymann, K. G., & Matthies, H. (1988) · Brain Research · doi:10.1016/0006-8993(88)90008-x · Cited by 806
Somatodendritic expression of an immediate early gene is regulated by synaptic activity.
Link, W., Konietzko, U., Kauselmann, G., Krug, M., Schwanke, B., Frey, U., & Kuhl, D. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.12.5734 · Cited by 710
Induction of synaptic potentiation in hippocampus by patterned stimulation involves two events
Larson, J., & Lynch, G. (1986) · Science · doi:10.1126/science.3704635 · Cited by 597
Associations across time: The hippocampus as a temporary memory store
Rawlins, J. N. P. (1985) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00001291 · Cited by 561
Krug, M., Lössner, B., & Ott, T. (1984) · Brain Research Bulletin · doi:10.1016/0361-9230(84)90005-4 · Cited by 509
Flagged first, then by citations
Research works printed but not linked: 1
- Hebb, D. O. The Organization of Behaviour (Wiley, New York, 1949).
Cited by
Sorted by citations
A theory of cortical responses.
Friston, K. (2005) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2005.1622 · Cited by 4,578
“Calcium entry renders the post-synaptic specialization eligible for future potentiation by promoting the formation of synaptic ‘tags’ (e.g. Frey & Morris 1997) and other calciumdependent intracellular mechanisms.”
BackgroundThe molecular biology of memory storage: a dialogue between genes and synapses
Kandel, E. R. (2001) · Science · doi:10.1126/science.1067020 · Cited by 3,917
“At a given synapse synaptic plasticity can either be short- or long-lived depending on the number of spaced repetitions of the learning stimulus, and these parallel not only the behavioral changes of short-term memory [7, 43, 93].”
BackgroundFear memories require protein synthesis in the amygdala for reconsolidation after retrieval
Nader, K., Schafe, G. E., & Le Doux, J. E. (2000) · Nature · doi:10.1038/35021052 · Cited by 2,706
“It is possible that some modification of the synaptic tagging hypothesi”
BackgroundSynaptic Plasticity and Memory: An Evaluation of the Hypothesis
Martin, S. J., Grimwood, P. D., & Morris, R. G. M. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.649 · Cited by 2,794
“A possible resolution of this issue was suggested by Frey & Morris (1997), who introduced the concept of synaptic tagging.”
BackgroundSynaptic Plasticity: Multiple Forms, Functions, and Mechanisms
Citri, A., & Malenka, R. C. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301559 · Cited by 2,323
“An intriguing hypothesis is that during the synaptic activation to induce LTP a ‘synaptic tag’ is generated that functions to capture or sequester plasticity related proteins, which in turn are required to stabilize the increase in synaptic strength (Frey and Morris, 1997).”
BackgroundHippocampal sharp wave-ripple: A cognitive biomarker for episodic memory and planning
Buzsáki, G. (2015) · Hippocampus · doi:10.1002/hipo.22488 · Cited by 1,759
The molecular basis of CaMKII function in synaptic and behavioural memory
Lisman, J., Schulman, H., & Cline, H. (2002) · Nature Reviews Neuroscience · doi:10.1038/nrn753 · Cited by 1,860
“According to this view, CaMKII acts as a synaptic ta”
BackgroundFunction and regulation of CREB family transcription factors in the nervous system
Lonze, B. E., & Ginty, D. D. (2002) · Neuron · doi:10.1016/s0896-6273(02)00828-0 · Cited by 2,127
Emergent Properties of Networks of Biological Signaling Pathways
Bhalla, U. S., & Iyengar, R. (1999) · Science · doi:10.1126/science.283.5400.381 · Cited by 1,686
The Neurobiology of Consolidations, Or, How Stable is the Engram?
Dudai, Y. (2004) · Annual Review of Psychology · doi:10.1146/annurev.psych.55.090902.142050 · Cited by 1,671
“…postactivation period and during this tagging period could be stabilized in response to concurrent activity in other synapses on the same neuron (Frey & Morris 1997), permitting generalization and binding at the synaptic level within the circuit (Dudai & Morris 2000; for a harbinger of this…”
BackgroundInfluentialThe principal features and mechanisms of dopamine modulation in the prefrontal cortex
Seamans, J. K., & Yang, C. R. (2004) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2004.05.006 · Cited by 1,592
Mechanisms of emotional arousal and lasting declarative memory.
Cahill, L., & McGaugh, J. L. (1998) · Trends in Neurosciences · doi:10.1016/s0166-2236(97)01214-9 · Cited by 1,575
Ca2+ Influx Regulates BDNF Transcription by a CREB Family Transcription Factor-Dependent Mechanism
Tao, X., Finkbeiner, S., Arnold, D. B., Shaywitz, A. J., & Greenberg, M. E. (1998) · Neuron · doi:10.1016/s0896-6273(00)81010-7 · Cited by 1,561
Schemas and Memory Consolidation.
Tse, D., Langston, R. F., Kakeyama, M., Bethus, I., Spooner, P. A., Wood, E. R., Witter, M. P., & Morris, R. G. M. (2007) · Science · doi:10.1126/science.1135935 · Cited by 1,244
Self-citationSynaptic plasticity, memory and the hippocampus: a neural network approach to causality
Neves, G., Cooke, S. F., & Bliss, T. (2007) · Nature reviews. Neuroscience · doi:10.1038/nrn2303 · Cited by 1,287
“The strategy is to target the free-standing LTP device to recently potentiated synapses expressing synaptic tags , as postulated by Frey and Morri”
BDNF function in adult synaptic plasticity: The synaptic consolidation hypothesis
Bramham, C. R., & Messaoudi, E. (2005) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2005.06.003 · Cited by 1,193
Addiction, Dopamine, and the Molecular Mechanisms of Memory
Berke, J. D., & Hyman, S. E. (2000) · Neuron · doi:10.1016/s0896-6273(00)81056-9 · Cited by 1,184
The Molecular and Systems Biology of Memory
Kandel, E. R., Dudai, Y., & Mayford, M. R. (2014) · Cell · doi:10.1016/j.cell.2014.03.001 · Cited by 1,134
The Intersection of Amyloid Beta and Tau at Synapses in Alzheimer’s Disease
Spires-Jones, T. L., & Hyman, B. T. (2014) · Neuron · doi:10.1016/j.neuron.2014.05.004 · Cited by 1,201
Metaplasticity: tuning synapses and networks for plasticity
Abraham, W. C. (2008) · Nature reviews. Neuroscience · doi:10.1038/nrn2356 · Cited by 1,166
“However, if a strong HFS that induces protein-synthesis-dependent LTP in one input pathway precedes a weak HFS to a second, independent pathway, this enables the second pathway to establish a late phase of LT”
BackgroundRapid Spine Delivery and Redistribution of AMPA Receptors After Synaptic NMDA Receptor Activation
Shi, S.-H., Hayashi, Y., Petralia, R. S., Zaman, S. H., Wenthold, R. J., Svoboda, K., & Malinow, R. (1999) · Science · doi:10.1126/science.284.5421.1811 · Cited by 1,276
Young blood reverses age-related impairments in cognitive function and synaptic plasticity in mice
Villeda, S. A., Plambeck, K. E., Middeldorp, J., Castellano, J. M., Mosher, K. I., Luo, J., Smith, L. K., Bieri, G., Lin, K., Berdnik, D., et al. (2014) · Nature Medicine · doi:10.1038/nm.3569 · Cited by 1,081
BDNF and synaptic plasticity, cognitive function, and dysfunction
Lu, B., Nagappan, G., & Lu, Y. (2014) · Handbook of Experimental Pharmacology · doi:10.1007/978-3-642-45106-5_9 · Cited by 1,043
BDNF and Activity-Dependent Synaptic Modulation: Figure 1.
Lu, B. (2003) · Learning & Memory · doi:10.1101/lm.54603 · Cited by 945
The Spike-Timing Dependence of Plasticity
Feldman, D. E. (2012) · Neuron · doi:10.1016/j.neuron.2012.08.001 · Cited by 1,071
The molecular biology of memory: cAMP, PKA, CRE, CREB-1, CREB-2, and CPEB
Kandel, E. R. (2012) · Molecular Brain · doi:10.1186/1756-6606-5-14 · Cited by 931
“Frey U, Morris RG: Weak before strong: dissociating synaptic tagging and plasticity-factor accounts of late-LTP.”
BackgroundResultInfluentialDendritic Protein Synthesis, Synaptic Plasticity, and Memory
Sutton, M. A., & Schuman, E. M. (2006) · Cell · doi:10.1016/j.cell.2006.09.014 · Cited by 938
“…can drive local synthesis, but whether those products are then dedicated to that synapse or other sites may be subject to additional regulatory mechanisms such as translation-independent recruitment processes (for instance, synaptic tagging/capture; Frey and Morris, 1997; Martin et al., 1997).”
BackgroundResultThe neuropharmacology of butyrate: the bread and butter of the microbiota-gut-brain axis
Stilling, R. M., van de Wouw, M., Clarke, G., Stanton, C., Dinan, T. G., & Cryan, J. F. (2016) · Neurochemistry International · doi:10.1016/j.neuint.2016.06.011 · Cited by 891
“transcriptional regulation specifically during long-term memory formation or late LTP has sparked the generation of the synaptic tagging and capturing hypothesis (Frey and Morris, 1997; Redondo and Morris, 2011; Viosca et al., 2007).”
BackgroundFlavell, S. W., & Greenberg, M. E. (2008) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.31.060407.125631 · Cited by 832
Translational Control by MAPK Signaling in Long-Term Synaptic Plasticity and Memory
Kelleher, R. J., Govindarajan, A., Jung, H.-Y., Kang, H., & Tonegawa, S. (2004) · Cell · doi:10.1016/s0092-8674(04)00115-1 · Cited by 845
Structure-stability-function relationships of dendritic spines
Kasai, H., Matsuzaki, M., Noguchi, J., Yasumatsu, N., & Nakahara, H. (2003) · Trends in Neurosciences · doi:10.1016/s0166-2236(03)00162-0 · Cited by 847
Cerebellar Long-Term Depression: Characterization, Signal Transduction, and Functional Roles
Ito, M. (2001) · Physiological Reviews · doi:10.1152/physrev.2001.81.3.1143 · Cited by 855
“The translational inhibitors depress the late phase of LTP in hippocampal neurons (152, 153, 411).”
BackgroundLocus coeruleus and dopaminergic consolidation of everyday memory
Takeuchi, T., Duszkiewicz, A. J., Sonneborn, A., Spooner, P. A., Yamasaki, M., Watanabe, M., Smith, C. C., Fernández, G., Deisseroth, K., Greene, R. W., et al. (2016) · Nature · doi:10.1038/nature19325 · Cited by 827
Kosik, K. S. (2006) · Nature reviews. Neuroscience · doi:10.1038/nrn2037 · Cited by 834
“By contrast, enduring synaptic plasticity is a systems function of a neuron that requires protein synthesi”
BackgroundSerotonin receptor 1A knockout: An animal model of anxiety-related disorder
Ramboz, S., Oosting, R. S., Amara, D. A., Kung, H. F., Blier, P., Mendelsohn, M. M., Mann, J. J., Brunner, D., & Hen, R. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.24.14476 · Cited by 831
Steward, O., Wallace, C. S., Lyford, G., & Worley, P. (1998) · Neuron · doi:10.1016/s0896-6273(00)80591-7 · Cited by 845
The role of the GluR2 subunit in AMPA receptor function and synaptic plasticity
Isaac, J. T. R., Ashby, M. C., & McBain, C. J. (2007) · Neuron · doi:10.1016/j.neuron.2007.06.001 · Cited by 802
Making memories last: the synaptic tagging and capture hypothesis
Redondo, R. L., & Morris, R. G. M. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn2963 · Cited by 792
“The core concepts of the STC hypothesis A core concept of the STC hypothesi”
BackgroundSelf-citationArc/Arg3.1 Mediates Homeostatic Synaptic Scaling of AMPA Receptors
Shepherd, J. D., Rumbaugh, G., Wu, J., Chowdhury, S., Plath, N., Kuhl, D., Huganir, R. L., & Worley, P. F. (2006) · Neuron · doi:10.1016/j.neuron.2006.08.034 · Cited by 779
“1’s effects on LTP/LTD are secondary to poor homeostatic scaling in neurons or that these two processes may be independent of each other.”
BackgroundInfluentialThe Consolidation and Transformation of Memory
Dudai, Y., Karni, A., & Born, J. (2015) · Neuron · doi:10.1016/j.neuron.2015.09.004 · Cited by 741
“The molecular mechanisms of this tagging are possibly unique to sleep-dependent consolidation and may differ from those synaptic tag-and-capture mechanisms (Frey and Morris, 1997; Martin et al., 1997) that have been hypothesized to underlie retroactive enhancement of weakly encoded associative memories by subsequent s…”
BDNF: A key regulator for protein synthesis-dependent LTP and long-term memory?
Lü, Y., Christian, K. M., & Lu, B. (2007) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2007.08.018 · Cited by 807
Cellular and Systems Reconsolidation in the Hippocampus
Dębiec, J., LeDoux, J. E., & Nader, K. (2002) · Neuron · doi:10.1016/s0896-6273(02)01001-2 · Cited by 772
A comprehensive review on emerging artificial neuromorphic devices
Zhu, J., Zhang, T., Yang, Y., & Huang, R. (2020) · Applied Physics Reviews · doi:10.1063/1.5118217 · Cited by 783
Okamoto, K.-I., Nagai, T., Miyawaki, A., & Hayashi, Y. (2004) · Nature Neuroscience · doi:10.1038/nn1311 · Cited by 854
“Because actin polymerization does not require new protein synthesis, it may explain the 'synapse tagging' effect of synaptic plasticity, whereby newly synthesized molecules necessary for late-phase of LTP affect only the synapse undergoing the synaptic plasticit”
Postsynaptic BDNF‐TrkB signaling in synapse maturation, plasticity, and disease
Yoshii, A., & Constantine‐Paton, M. (2010) · Developmental Neurobiology · doi:10.1002/dneu.20765 · Cited by 744
Learning and inference in the brain
Friston, K. (2003) · Neural Networks · doi:10.1016/j.neunet.2003.06.005 · Cited by 724
“Schematic illustrating hierarchical structures in the brain and the distinction between forward, backward and lateral connections. the formation of synaptic 'tags' (e.g. Frey & Morris, 1997) and other calcium-dependant intracellular mechanisms.”
BackgroundIzquierdo, I., & Medina, J. H. (1997) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1997.3799 · Cited by 959
Martin, K. C., Casadio, A., Zhu, H., Yaping, E., Rose, J. C., Chen, M., Bailey, C. H., & Kandel, E. R. (1997) · Cell · doi:10.1016/s0092-8674(00)80484-5 · Cited by 740
“…modulate emerged from studies of the late phase of long-term the strength of their synaptic connections in response potentiation in the hippocampus (Frey and Morris, 1997). to their cellular experience and environment, appears to These studies were based on populations of neurons contribute to a…”
BackgroundProtein synthesis at synaptic sites on dendrites.
Steward, O., & Schuman, E. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.299 · Cited by 731
The Passion of World Politics: Propositions on Emotion and Emotional Relationships
Crawford, N. C. (2000) · International Security · doi:10.1162/016228800560327 · Cited by 691
The synaptic plasticity and memory hypothesis: encoding, storage and persistence
Takeuchi, T., Duszkiewicz, A. J., & Morris, R. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0288 · Cited by 712
Neurotrophin secretion: current facts and future prospects
Leßmann, V., Gottmann, K., & Malcangio, M. (2003) · Progress in Neurobiology · doi:10.1016/s0301-0082(03)00019-4 · Cited by 683
“The impairment of LTP in BDNF-deficient mice (Korte et al., 1995; Patterson et al., 1996) can be accounted for in part by presynaptic vesicle depletion resulting in synaptic fatigue of glutamate release upon tetanic synaptic stimulation, which is observed when BDNF supply is low (Figurov et al., 1996; Gottschalk et al…”
BackgroundInfluentialSolving the Distal Reward Problem through Linkage of STDP and Dopamine Signaling
Izhikevich, E. M. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhl152 · Cited by 658
Tang, S. J., Reis, G., Kang, H., Gingras, A.-C., Sonenberg, N., & Schuman, E. M. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.012605299 · Cited by 734
The Restless Engram: Consolidations Never End
Dudai, Y. (2012) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062111-150500 · Cited by 644
Protein synthesis and neurotrophin-dependent structural plasticity of single dendritic spines
Tanaka, J.-I., Horiike, Y., Matsuzaki, M., Miyazaki, T., Ellis-Davies, G. C. R., & Kasai, H. (2008) · Science · doi:10.1126/science.1152864 · Cited by 615
Labelling and optical erasure of synaptic memory traces in the motor cortex
Hayashi-Takagi, A., Yagishita, S., Nakamura, M., Shirai, F., Wu, Y. I., Loshbaugh, A. L., Kuhlman, B., Hahn, K. M., & Kasai, H. (2015) · Nature · doi:10.1038/nature15257 · Cited by 624
Dendritic Spine Structural Anomalies in Fragile-X Mental Retardation Syndrome
Irwin, S. A. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.10.1038 · Cited by 626
Locally dynamic synaptic learning rules in pyramidal neuron dendrites
Harvey, C. D., & Svoboda, K. (2007) · Nature · doi:10.1038/nature06416 · Cited by 625
“Previous studies have suggested that synaptic plasticity can be influenced by prior neural activity 6,7,11,12,41–43 .”
The Autistic Neuron: Troubled Translation?
Kelleher, R. J., & Bear, M. F. (2008) · Cell · doi:10.1016/j.cell.2008.10.017 · Cited by 598
“The phenomenon of synaptic tagging and capture suggests that synaptic stimulation creates an immobile “tag” at active synapses that “captures” essential protein products (Frey and Morris, 1997).”
BackgroundThe labile nature of consolidation theory
Nader, K., Schafe, G. E., & LeDoux, J. E. (2000) · Nature Reviews Neuroscience · doi:10.1038/35044580 · Cited by 613
“How could this distinction be made? Current models of how specific connections are marked during synaptic plasticity invoke a molecular tag of a poorly understood natur”
Synaptic tagging: implications for late maintenance of hippocampal long-term potentiation
Frey, U., & Morris, R. G. M. (1998) · Trends in Neurosciences · doi:10.1016/s0166-2236(97)01189-2 · Cited by 615
Self-citationClopath, C., Buesing, L., Vasilaki, E., & Wulfram Gerstner, B. (2009) · Nature Precedings · doi:10.1038/nn.2479 · Cited by 627
“Third, additional mechanisms need to be implemented to describe the transition from early to late LTP/LT”
BackgroundBarco, A., Alarcon, J. M., & Kandel, E. (2002) · Cell · doi:10.1016/s0092-8674(02)00657-8 · Cited by 595
“, 1997) and rats (Frey and Morris, 1997) using two- pocampal infusion of CREB antisense oligonucleotides disrupts long-term spatial memory in rats, but does not affect short-term memory (Guzowski and McGaugh, 3 Correspondence: erk5@columbia.”
BackgroundMethodMartin, K. C., Michael, D., Rose, J. C., Barad, M., Casadio, A., Zhu, H., & Kandel, E. R. (1997) · Neuron · doi:10.1016/s0896-6273(00)80330-x · Cited by 545
Hippocampal-Neocortical Interactions in Memory Formation, Consolidation, and Reconsolidation
Wang, S., & Morris, R. (2009) · Annual Review of Psychology · doi:10.1146/annurev.psych.093008.100523 · Cited by 570
Nuclear calcium signaling controls CREB-mediated gene expression triggered by synaptic activity
Hardingham, G. E., Arnold, F. J. L., & Bading, H. (2001) · Nature Neuroscience · doi:10.1038/85109 · Cited by 537
Mayford, M., Siegelbaum, S. A., & Kandel, E. R. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a005751 · Cited by 500
Park, S., Park, J. M., Kim, S., Kim, J.-A., Shepherd, J. D., Smith-Hicks, C. L., Chowdhury, S., Kaufmann, W., Kuhl, D., Ryazanov, A. G., et al. (2008) · Neuron · doi:10.1016/j.neuron.2008.05.023 · Cited by 516
“The products of de novo protein synthesis are hypothesized to be ‘‘captured’’ at active synapses (Frey and Morris, 1997), but their identity remains unknown.”
BackgroundTranslational Regulatory Mechanisms in Persistent Forms of Synaptic Plasticity
Kelleher, R. J., Govindarajan, A., & Tonegawa, S. (2004) · Neuron · doi:10.1016/j.neuron.2004.09.013 · Cited by 592
“immediate effect (Nguyen et al., 1994; Frey et al., 1996; Frey and Morris, 1997; Scharf et ton et al., 2001). al., 2002).”
BackgroundInfluentialPhenomenological models of synaptic plasticity based on spike timing
Morrison, A., Diesmann, M., & Gerstner, W. (2008) · Biological Cybernetics · doi:10.1007/s00422-008-0233-1 · Cited by 593
Depolarization and cAMP Elevation Rapidly Recruit TrkB to the Plasma Membrane of CNS Neurons
Meyer-Franke, A., Wilkinson, G. A., Kruttgen, A., Hu, M., Munro, E., Hanson, M. G., Reichardt, L. F., & Barres, B. A. (1998) · Neuron · doi:10.1016/s0896-6273(00)80586-3 · Cited by 516
Mesolimbic dopaminergic pathways in fear conditioning
Pezze, M. A., & Feldon, J. (2004) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2004.09.004 · Cited by 519
Impaired Spatial Learning after Saturation of Long-Term Potentiation
Moser, E. I., Krobert, K. A., Moser, M.-B., & Morris, R. G. M. (1998) · Science · doi:10.1126/science.281.5385.2038 · Cited by 505
Self-citationCasadio, A., Martin, K. C., Giustetto, M., Zhu, H., Chen, M., Bartsch, D., Bailey, C. H., & Kandel, E. R. (1999) · Cell · doi:10.1016/s0092-8674(00)81653-0 · Cited by 503
A neuromodulatory role of interleukin-1β in the hippocampus
Schneider, H., Pitossi, F., Balschun, D., Wagner, A., del Rey, A., & Besedovsky, H. O. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.13.7778 · Cited by 498
Wu, L., Wells, D., Tay, J., Mendis, D., Abbott, M.-A., Barnitt, A., Quinlan, E., Heynen, A., Fallon, J. R., & Richter, J. D. (1998) · Neuron · doi:10.1016/s0896-6273(00)80630-3 · Cited by 488
“…are synthesized in the cell body and then tarand dictates which mRNAs are polyadenylated (Fox etgeted to the synapse that was “tagged” during the initial al., 1989; McGrew et al., 1989; Huarte et al., 1992; re-stimulation (Sossin, 1996; Frey and Morris, 1997; Schuviewed in Richter, 1996).”
BackgroundMorris, R., Moser, E. I., Riedel, G., Martin, S. J., Sandin, J., Day, M., & O’Carroll, C. (2003) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2002.1264 · Cited by 493
“A new perspective on these ideas is the synaptic tagging hypothesis of memory trace formation (Frey & Morris 1997, 1998a,b; Morris & Frey 1997; Dudai & Morris 2001).”
BackgroundPlant, K., Pelkey, K. A., Bortolotto, Z. A., Morita, D., Terashima, A., McBain, C. J., Collingridge, G. L., & Isaac, J. T. R. (2006) · Nature Neuroscience · doi:10.1038/nn1678 · Cited by 542
In situ visualization and dynamics of newly synthesized proteins in rat hippocampal neurons
Dieterich, D. C., Hodas, J. J. L., Gouzer, G., Shadrin, I. Y., Ngo, J. T., Triller, A., Tirrell, D. A., & Schuman, E. M. (2010) · Nature Neuroscience · doi:10.1038/nn.2580 · Cited by 470
“Thus far, the capture of new proteins has been inferred by clever electrophysiological and pharmacological manipulation”
BackgroundA neoHebbian framework for episodic memory; role of dopamine-dependent late LTP
Lisman, J., Grace, A. A., & Duzel, E. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.07.006 · Cited by 465
Calcium Regulation of Dendritic Growth via CaM Kinase IV and CREB-Mediated Transcription
Redmond, L., Kashani, A. H., & Ghosh, A. (2002) · Neuron · doi:10.1016/s0896-6273(02)00737-7 · Cited by 462
Jordan, J. D., Landau, E. M., & Iyengar, R. (2000) · Cell · doi:10.1016/s0092-8674(00)00112-4 · Cited by 459
New views of Arc, a master regulator of synaptic plasticity
Shepherd, J. D., & Bear, M. F. (2011) · Nature Neuroscience · doi:10.1038/nn.2708 · Cited by 481
“From the point of view of hippocampal LTP and LTD, one might therefore conclude that Arc induction is critical for protein synthesis–dependent consolidation of synaptic modifications, regardless of the polarity of the change.”
ResultDevelopment and arealization of the cerebral cortex
Cadwell, C. R., Bhaduri, A., Mostajo-Radji, M. A., Keefe, M. G., & Nowakowski, T. J. (2019) · Neuron · doi:10.1016/j.neuron.2019.07.009 · Cited by 408
Izquierdo, I., Furini, C. R. G., & Myskiw, J. C. (2016) · Physiological Reviews · doi:10.1152/physrev.00018.2015 · Cited by 453
Steward, O., & Worley, P. (2001) · Neuron · doi:10.1016/s0896-6273(01)00275-6 · Cited by 474
The staufen/pumilio Pathway Is Involved in Drosophila Long-Term Memory
Dubnau, J., Chiang, A., Grady, L., Barditch, J., Gossweiler, S., McNeil, J., Smith, P., Buldoc, F., Scott, R., Certa, U., et al. (2003) · Current Biology · doi:10.1016/s0960-9822(03)00064-2 · Cited by 449
The role of calmodulin as a signal integrator for synaptic plasticity
Xia, Z., & Storm, D. R. (2005) · Nature reviews. Neuroscience · doi:10.1038/nrn1647 · Cited by 454
New life in an old idea: The synaptic plasticity and memory hypothesis revisited
Martin, S. J., & Morris, R. (2002) · Hippocampus · doi:10.1002/hipo.10107 · Cited by 461
BDNF and Hippocampal Synaptic Plasticity
Leal, G., Bramham, C. R., & Duarte, C. B. (2017) · Vitamins and Hormones · doi:10.1016/bs.vh.2016.10.004 · Cited by 425
Si, K., Giustetto, M., Etkin, A., Hsu, R., Janisiewicz, A. M., Miniaci, M. C., Kim, J., Zhu, H., & Kandel, E. R. (2003) · Cell · doi:10.1016/s0092-8674(03)01021-3 · Cited by 442
Barad, M., Bourtchouladze, R., Winder, D. G., Golan, H. M., & Kandel, E. R. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.25.15020 · Cited by 430
Ostroff, L. E., Fiala, J. C., Allwardt, B., & Harris, K. M. (2002) · Neuron · doi:10.1016/s0896-6273(02)00785-7 · Cited by 461
“Frey and Morris (1997) have proposed that stimulated synapses produce local “tags” that recruit Discussion newly synthesized macromolecules into dendritic spines.”
BackgroundBiochemical mechanisms for translational regulation in synaptic plasticity
Klann, E., & Dever, T. E. (2004) · Nature reviews. Neuroscience · doi:10.1038/nrn1557 · Cited by 433
“This enduring phase has distinct kinetic patterns of sensitivity to transcription and translation inhibitors: the former producing a delayed inhibition, and the latter impeding the initiation of the enduring plasticit”
BackgroundNeuromodulated Spike-Timing-Dependent Plasticity, and Theory of Three-Factor Learning Rules
Frémaux, N., & Wulfram Gerstner, B. (2016) · Frontiers in Neural Circuits · doi:10.3389/fncir.2015.00085 · Cited by 449
“The biological plausibility of eligibility traces and its potential relation to synaptic “tags” (Frey and Morris, 1997; Bailey et al., 2000; Redondo and Morris, 2011) will be explored in the discussion section.”
BackgroundInfluentialNoradrenergic mechanisms in neurodegenerative diseases: a theory
Marien, M. R., Colpaert, F. C., & Rosenquist, A. C. (2004) · Brain Research Reviews · doi:10.1016/j.brainresrev.2004.02.002 · Cited by 425
Translational control of hippocampal synaptic plasticity and memory by the eIF2α kinase GCN2
Costa‐Mattioli, M., Gobert, D., Harding, H. P., Herdy, B., Azzi, M., Bruno, M. A., Bidinosti, M., Mamou, C. B., Marcinkiewicz, E., Yoshida, M., et al. (2005) · Nature · doi:10.1038/nature03897 · Cited by 412
Nitric Oxide Signaling Contributes to Late-Phase LTP and CREB Phosphorylation in the Hippocampus
Lü, Y.-F., Kandel, E. R., & Hawkins, R. D. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-23-10250.1999 · Cited by 411
“…and Apl ysia suggests that local events that occur during early-phase LTP or facilitation somehow " tag " the active synapses, so that those synapses can use the newly synthesized proteins when they arrive from the cell body for the late phase (Frey and Morris, 1997; Martin et al., 1997a).”
BackgroundCommunication Between the Synapse and the Nucleus in Neuronal Development, Plasticity, and Disease
Cohen, S., & Greenberg, M. E. (2008) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.24.110707.175235 · Cited by 400
“Late-LTP also requires protein synthesis: An initial, strong, late-LTP-inducing stimulus at one set of inputs allows the subsequent weak stimulation of a separate synapse—one that, if given on its own, would normally not induce late-LTP—to induce late-LTP at the second synapse (Frey & Morris 1997).”
Background
Metadata
- Authors
- Frey, U., & Morris, R. G. M.
- Venue
- Nature
- Published
- 1997-02
- Volume
- 385
- Issue
- 6616
- Pages
- 533-536
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2011882079
- Cited by
- 1,736
- References
- 25
- Citations by year
- 2026: 56 · 2025: 48 · 2024: 94 · 2023: 65 · 2022: 75 · 2021: 78 · 2020: 69 · 2019: 68 · 2018: 72 · 2017: 66 · 2016: 72 · 2015: 78 · 2014: 104 · 2013: 56 · 2012: 59
- FWCI
- 17.67
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- 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
- synaptic tagging, long-term potentiation, late-phase LTP, protein synthesis, hippocampal neurons, tetanic stimulation, synaptic specificity, memory, synaptic plasticity
- MeSH terms
- Animals, Anisomycin, Electric Stimulation, Evoked Potentials, Hippocampus, Male, Memory, Models, Neurological, Protein Synthesis Inhibitors, Synapses, Protein Biosynthesis, Rats, Wistar, Long-Term Potentiation, Rats, In Vitro Techniques
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