Cited by 204Memory and Neural MechanismsNeuroscience and Neuropharmacology ResearchNeurogenesis and neuroplasticity mechanisms

The DOI matches its Crossref record; 39 of the 39 references it cites were found in a registry or an index.

Protein Synthesis Is Required for the Enhancement of Long-Term Potentiation and Long-Term Memory by Spaced Training

Scharf, Matthew T., Woo, Newton H., Lattal, K. Matthew, Young, Jennie Z., Nguyen, Peter V., Abel, Ted·2002·Journal of Neurophysiology

DOI 10.1152/jn.2002.87.6.2770

Open this paper in CoChat — free account

Abstract

Spaced training is generally more effective than massed training for learning and memory, but the molecular mechanisms underlying this trial spacing effect remain poorly characterized. One potential molecular basis for the trial spacing effect is the differential modulation, by distinct temporal patterns of neuronal activity, of protein synthesis-dependent processes that contribute to the expression of specific forms of synaptic plasticity in the mammalian brain. Long-term potentiation (LTP) is a type of synaptic modification that may be important for certain forms of memory storage in the mammalian brain. To explore the role of protein synthesis in the trial spacing effect, we assessed the protein synthesis dependence of hippocampal LTP induced by 100-Hz tetraburst stimulation delivered to mouse hippocampal slices in either a temporally massed (20-s interburst interval) or spaced (5-min interburst interval) fashion. To extend our studies to the behavioral level, we trained mice in fear conditioning using either a massed or spaced training protocol and examined the sensitivity of long-term memory to protein synthesis inhibition. Larger LTP was induced by spaced stimulation in hippocampal slices. This improvement of synaptic potentiation following temporally spaced synaptic stimulation in slices was attenuated by bath application of an inhibitor of protein synthesis. Further, the maintenance of LTP induced by spaced synaptic stimulation was more sensitive to disruption by anisomycin than the maintenance of LTP elicited following massed stimulation. Temporally spaced behavioral training improved long-term memory for contextual but not for cued fear conditioning, and this enhancement of memory for contextual fear was also protein synthesis dependent. Our data reveal that altering the temporal spacing of synaptic stimulation and behavioral training improved hippocampal LTP and enhanced contextual long-term memory. From a broad perspective, these results suggest that the recruitment of protein synthesis-dependent processes important for long-term memory and for long-lasting forms of LTP can be modulated by the temporal profiles of behavioral training and synaptic stimulation.

Integrity signals

Registry

Crossref · 10.1152/jn.2002.87.6.2770

Cites

39 of 39 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

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
Emotion circuits in the brain
LeDoux, J. E. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.155 · Cited by 8,444
Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex
Bienenstock, E., Cooper, L., & Munro, P. (1982) · The Journal of Neuroscience · doi:10.1523/jneurosci.02-01-00032.1982 · Cited by 2,896
Synaptic 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
Memory deficits associated with senescence: A neurophysiological and behavioral study in the rat.
Barnes, C. A. (1979) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0077579 · Cited by 2,088
Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein
Bourtchuladze, R., Frenguelli, B., Blendy, J., Cioffi, D., Schutz, G., & Silva, A. J. (1994) · Cell · doi:10.1016/0092-8674(94)90400-6 · Cited by 1,800
Protein synthesis and memory: A review.
Davis, H. P., & Squire, L. R. (1984) · Psychological Bulletin · doi:10.1037/0033-2909.96.3.518 · Cited by 1,505
Genetic Demonstration of a Role for PKA in the Late Phase of LTP and in Hippocampus-Based Long-Term Memory
Abel, T., Nguyen, P. V., Barad, M., Deuel, T. A. S., Kandel, E. R., & Bourtchouladze, R. (1997) · Cell · doi:10.1016/s0092-8674(00)81904-2 · Cited by 1,217
Self-citation
The MAPK cascade is required for mammalian associative learning
Atkins, C. M., Selcher, J. C., Petraitis, J. J., Trzaskos, J. M., & Sweatt, J. D. (1998) · Nature Neuroscience · doi:10.1038/2836 · Cited by 1,083
Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila
Yin, J. C. P., Wallach, J. S., Del Vecchio, M., Wilder, E. L., Zhou, H., Quinn, W. G., & Tully, T. (1994) · Cell · doi:10.1016/0092-8674(94)90399-9 · Cited by 959

Flagged first, then by citations

Show all 39 references

Research works printed but not linked: 2

Pittenger C, 2000, Soc Neurosci Abstr, 26, 1509
Woo NH, 2000, Soc Neurosci Abstr, 26, 355

Sorted by citations

Items 101–200 of 203

Differential effects of spaced vs. massed training in long-term object-identity and object-location recognition memory
Bello-Medina, P. C., Carrasco, L., González-Ornelas, N. R., Jeffery, K. J., & Ramı́rez-Amaya, V. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.04.047 · Cited by 29
An ACT-R Model of the Spacing Effect
Pavlik, P. I., & Anderson, J. R. (2018) · KiltHub Repository · doi:10.1184/r1/6613424 · Cited by 27
Calcium/calmodulin-dependent kinase IV contributes to translation-dependent early synaptic potentiation in the anterior cingulate cortex of adult mice
Toyoda, H., Zhao, M., Mercaldo, V., Chen, T., Descalzi, G., Kida, S., & Zhuo, M. (2010) · Molecular Brain · doi:10.1186/1756-6606-3-27 · Cited by 27
A specific role for hippocampal mossy fiber's zinc in rapid storage of emotional memoriesPreprint
Ceccom, J., Halley, H., Daumas, S., & Lassalle, J. M. (2014) · Learning & Memory · doi:10.1101/lm.033472.113 · Cited by 27
Very Similar Spacing-Effect Patterns in Very Different Learning/Practice Domains
Kornmeier, J., Spitzer, M., & Sosic-Vasic, Z. (2014) · PLoS ONE · doi:10.1371/journal.pone.0090656 · Cited by 25
Temporal pattern and synergy influence activity of ERK signaling pathways during L-LTP induction
Zobon, N. T. M., Jędrzejewska‐Szmek, J., & Blackwell, K. T. (2021) · eLife · doi:10.7554/elife.64644 · Cited by 25
TESTING OF INFORMATION CONDENSATION IN A MODEL REVERBERATING SPIKING NEURAL NETWORK
Vidybida, A. K. (2011) · International Journal of Neural Systems · doi:10.1142/s0129065711002742 · Cited by 24
Perspective on Sleep and Aging
Monjan, A. A. (2010) · Frontiers in Neurology · doi:10.3389/fneur.2010.00124 · Cited by 24
From membrane receptors to protein synthesis and actin cytoskeleton: Mechanisms underlying long lasting forms of synaptic plasticity
Jędrzejewska‐Szmek, J., & Blackwell, K. T. (2019) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2019.01.006 · Cited by 24
Noradrenergic gating of long-lasting synaptic potentiation in the hippocampus: from neurobiology to translational biomedicine
Nguyen, P., & Gelinas, J. N. (2018) · Journal of Neurogenetics · doi:10.1080/01677063.2018.1497630 · Cited by 22
Self-citation
Selective role of the translin/trax RNase complex in hippocampal synaptic plasticity
Park, A. J., Shetty, M. S., Baraban, J. M., & Abel, T. G. (2020) · Molecular Brain · doi:10.1186/s13041-020-00691-5 · Cited by 20
Self-citation
The Spacing Effect for Structural Synaptic Plasticity Provides Specificity and Precision in Plastic Changes
Martín, A. S., Rela, L., Gelb, B. D., & Pagani, M. R. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.2607-16.2017 · Cited by 19
Latent inhibition of cued fear conditioning: an NMDA receptor‐dependent process that can be established in the presence of anisomycin
Lewis, M. C., & Gould, T. J. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03531.x · Cited by 20
Conversion of short-term potentiation to long-term potentiation in mouse CA1 by coactivation of β-adrenergic and muscarinic receptorsPreprint
Connor, S. A., Maity, S., Roy, B., Ali, D. W., & Nguyen, P. (2012) · Learning & Memory · doi:10.1101/lm.026898.112 · Cited by 24
Self-citation
Genetic Approaches to the Study of Synaptic Plasticity and Memory Storage
Abel, T. G., & Kaplan, M. P. (2003) · CNS Spectrums · doi:10.1017/s1092852900018873 · Cited by 19
Self-citation
Intermittent but not sustained moderate hypoxia elicits long-term facilitation of hypoglossal motor output
Wilkerson, J. R., Devinney, M. J., & Mitchell, G. S. (2017) · Respiratory Physiology & Neurobiology · doi:10.1016/j.resp.2017.10.005 · Cited by 18
CaMKII binding to GluN2B is important for massed spatial learning in the Morris water maze
Stein, I. S., Donaldson, M. S., & Hell, J. W. (2014) · F1000Research · doi:10.12688/f1000research.4660.1 · Cited by 20
Intra-spaced stimulation and protein phosphatase 1 dictate the direction of synaptic plasticity
Genoux, D., Bezerra, P., & Montgomery, J. M. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07669.x · Cited by 17
Variation in the persistence of memory: An interplay between actin dynamics and AMPA receptors
Rudy, J. W. (2014) · Brain Research · doi:10.1016/j.brainres.2014.12.009 · Cited by 18
Mathematical modeling the neuroregulation of blood pressure using a cognitive top-down approach
Ewing, G. W. (2010) · North American Journal of Medical Sciences · doi:10.4297/najms.2010.2341 · Cited by 17
The Rates of Protein Synthesis and Degradation Account for the Differential Response of Neurons to Spaced and Massed Training Protocols
Naqib, F., Farah, C. A., Pack, C. C., & Sossin, W. S. (2011) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002324 · Cited by 17
Histone deacetylase inhibition facilitates massed pattern-induced synaptic plasticity and memoryPreprint
Pandey, K. R., Sharma, K. P., & Sharma, S. K. (2015) · Learning & Memory · doi:10.1101/lm.039289.115 · Cited by 18
High-frequency stimulation-induced synaptic potentiation in dorsal and ventral CA1 hippocampal synapses: the involvement of NMDA receptors, mGluR5, and (L-type) voltage-gated calcium channelsPreprint
Papatheodoropoulos, C., & Kouvaros, S. (2016) · Learning & Memory · doi:10.1101/lm.042531.116 · Cited by 17
Spaced training improves learning in Ts65Dn and Ube3a mouse models of intellectual disabilities
Lauterborn, J. C., Schultz, M. N., Le, A. A., Amani, M., Friedman, A. E., Leach, P. T., Gall, C. M., LYNCH, G. S., & Crawley, J. N. (2019) · Translational Psychiatry · doi:10.1038/s41398-019-0495-5 · Cited by 17
Serotonin Signals Modulate Mushroom Body Output Neurons for Sustaining Water-Reward Long-Term Memory in Drosophila
Lee, W.-P., Chiang, M.-H., Chang, L.-Y., Shyu, W.-H., Chiu, T.-H., Fu, T., Wu, T., & Wu, C. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.755574 · Cited by 17
Extinction trial spacing across days differentially impacts fear regulation in adult and adolescent male mice
Gerhard, D. M., & Meyer, H. C. (2021) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2021.107543 · Cited by 17
Spatial memory: behavioral determinants of persistence in the watermaze delayed matching-to-place taskPreprint
da Silva, B. M., Bast, T., & Morris, R. (2013) · Learning & Memory · doi:10.1101/lm.032169.113 · Cited by 23
Anti-kindling Induced by Two-Stage Coordinated Reset Stimulation with Weak Onset Intensity
Zeitler, M., & Tass, P. A. (2016) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2016.00044 · Cited by 14
Emotional Memory Formation Under Lower Versus Higher Stress Conditions
Kogan, I., & Richter‐Levin, G. (2010) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2010.00183 · Cited by 15
Neuroscience and education: Mind the gap
Morris, J., & Sah, P. (2016) · Australian Journal of Education · doi:10.1177/0004944116652913 · Cited by 15
The Ins and Outs of miRNA-Mediated Gene Silencing during Neuronal Synaptic Plasticity
Rajgor, D., & Hanley, J. G. (2016) · Non-Coding RNA · doi:10.3390/ncrna2010001 · Cited by 15
Supraphysiological Levels of Oxygen Exposure During the Neonatal Period Impairs Signaling Pathways Required for Learning and Memory
Ramani, M., Kumar, R., Halloran, B., Lal, C. V., Ambalavanan, N., & McMahon, L. L. (2018) · Scientific Reports · doi:10.1038/s41598-018-28220-4 · Cited by 14
Early patterned stimulation leads to changes in adult behavior and gene expression in C. elegans
Ebrahimi, C. M., & Rankin, C. H. (2006) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2006.00278.x · Cited by 14
A TrkB and TrkC partial agonist restores deficits in synaptic function and promotes activity‐dependent synaptic and microglial transcriptomic changes in a late‐stage Alzheimer's mouse model
Latif‐Hernandez, A., Yang, T., Butler, R. R., Losada, P. M., Minhas, P. S., White, H., Tran, K. C., Liu, H., Simmons, D. A., Langness, V. F., et al. (2024) · Alzheimer s & Dementia · doi:10.1002/alz.13857 · Cited by 13
G-protein coupled receptors and synaptic plasticity in sleep deprivation
Parmar, S., Tadavarty, R., & Sastry, B. R. (2021) · World Journal of Psychiatry · doi:10.5498/wjp.v11.i11.954 · Cited by 11
Delayed intensive acquisition training alleviates the lesion-induced place learning deficits after fimbria–fornix transection in the rat
Malá, H., Castro, M. R., Pearce, H. L., Kingod, S. C., Nedergaard, S., Scharff, Z., Zandersen, M., & Mogensen, J. (2012) · Brain Research · doi:10.1016/j.brainres.2012.01.035 · Cited by 12
Identification of Flap Structure-Specific Endonuclease 1 as a Factor Involved in Long-Term Memory Formation of Aversive Learning
Saavedra-Rodríguez, L., Vázquez, A., Ortiz‐Zuazaga, H., Chorna, N., González, F. A., Andres, L. M., Rodriguez, K. M. L., Ramírez, F., Rodríguez, A., & de Ortı́z, S. P. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.4033-08.2009 · Cited by 11
Short-Term Dosage Regimen for Stimulation-Induced Long-Lasting Desynchronization
Manos, T., Zeitler, M., & Tass, P. A. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.00376 · Cited by 11
Making Memories: Why Time Matters
Kelley, P., Evans, M. D. R., & Kelley, J. (2018) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2018.00400 · Cited by 10
Emetine treatment masks initial LTP without affecting long-term stability
Abbas, A.-K., Huang, F., Li, R., Ekström, J., & Wigström, H. (2011) · Brain Research · doi:10.1016/j.brainres.2011.10.010 · Cited by 10
Predator fear memory depends on glucocorticoid receptors and protein synthesis in the basolateral amygdala and ventral hippocampus
Reis, F. M., Novaes, L. S., dos Santos, N. B., Ferreira-Rosa, K. C., Perfetto, J. G., Baldo, M. V. C., Munhoz, C. D., & Canteras, N. S. (2022) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2022.105757 · Cited by 10
Dose-Dependent Nonassociative Olfactory Learning in a Fly
Barbarossa, I. T., Muroni, P. P., Setzu, M. D., & Angioy, A. M. (2007) · Chemical Senses · doi:10.1093/chemse/bjm022 · Cited by 10
e-REAL: Enhanced Reality Lab
Salvetti, F., & Bertagni, B. (2014) · International Journal of Advanced Corporate Learning (iJAC) · doi:10.3991/ijac.v7i3.4033 · Cited by 10
Intermittent apnea elicits inactivity-induced phrenic motor facilitation via a retinoic acid- and protein synthesis-dependent pathway
Baertsch, N. A., & Baker, T. L. (2017) · Journal of Neurophysiology · doi:10.1152/jn.00212.2017 · Cited by 9
The Determining Conditions for Pavlovian Learning
Nasser, H. M., & Delamater, A. R. (2016) · Wiley eBooks · doi:10.1002/9781118650813.ch2 · Cited by 11
Conditioned preferences and aversions in infant rats mediated through ethanol inhalation
Nizhnikov, M. E., Pautassi, R. M., Molina, J. C., & Spear, N. E. (2009) · Alcohol · doi:10.1016/j.alcohol.2008.09.006 · Cited by 8
Memory out of context: Spacing effects and decontextualization in a computational model of the medial temporal lobe
Antony, J. W., Liu, X. L., Zheng, Y., Ranganath, C., & O’Reilly, R. C. (2026) · doi:10.21428/8e6ba8ef.d9f5dd19 · Cited by 7
Mechanisms of action of transcranial direct current stimulation
Yavari, F., Chhabra, H., Polanía, R., & Nitsche, M. A. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-18496-3.00006-9 · Cited by 5
Comment les intervalles temporels entre les répétitions d’une information en influencent-ils la mémorisation ? Revue théorique des effets de pratique distribuée
Gerbier, É., & Koenig, O. (2015) · L’Année psychologique · doi:10.3917/anpsy.153.0435 · Cited by 14
Transcription Control Pathways Decode Patterned Synaptic Inputs into Diverse mRNA Expression Profiles
Jain, P., & Bhalla, U. S. (2014) · PLoS ONE · doi:10.1371/journal.pone.0095154 · Cited by 6
Effects of Probiotics, Prebiotics and Synbiotic Supplementation on Cognitive Impairment: A Review
Mukilan, M. (2022) · Journal of Experimental Biology and Agricultural Sciences · doi:10.18006/2022.10(1).1.11 · Cited by 5
Impact of Pseudomonas aeruginosa, Bacillus subtilis, Staphylococcus aureus, and Escherichia coli Oral Infusions on Cognitive Memory Decline in Mild Cognitive Impairment
Mukilan, M. (2023) · Journal of Experimental Biology and Agricultural Sciences · doi:10.18006/2023.11(3).581.592 · Cited by 6
The influence of pathologies upon sensory perception and sensory coordination in children with developmental dyslexia and learning disorders: A unified theory of developmental dyslexia
Gw, E., & Parvez, S. H. (2012) · North American Journal of Medical Sciences · doi:10.4103/1947-2714.93878 · Cited by 6
PRECLINICAL STUDY: Pentylenetetrazole‐induced status epilepticus following training does not impair expression of morphine‐induced conditioned place preference
Zhang, J., Tan, H. T., Niu, H. C., Wang, J. H., Tang, X., Sanford, L. D., & Ma, Y. (2008) · Addiction Biology · doi:10.1111/j.1369-1600.2008.00122.x · Cited by 5
A meta-analysis of the effect of protein synthesis inhibitors on rodent fear conditioning
Carneiro, C. F. D., Amorim, F. E., & Amaral, O. B. (2023) · Peer Community Journal · doi:10.24072/pcjournal.339 · Cited by 7
Dynamic cognitive maps for agent landmark navigation in unseen environments
Sohn, S. S., DeStefani, S., & Kapadia, M. (2018) · Motion in Games · doi:10.1145/3274247.3274518 · Cited by 5
Mechanisms of Fear Extinction: Toward Improved Treatment for Anxiety
Barad, M., & Cain, C. K. (2007) · Cambridge University Press eBooks · doi:10.1017/cbo9780511500008.008 · Cited by 5
On the theory of mental representation block. a novel perspective on learning and behavior
Tobore, T. O. (2021) · Communicative & Integrative Biology · doi:10.1080/19420889.2021.1898752 · Cited by 4
Protein Synthesis and Memory
Gold, P. E. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.21119-x · Cited by 4
Anesthesia Resistant Memories in Drosophila, a Working Perspective
Bourouliti, A., & Skoulakis, E. M. C. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23158527 · Cited by 4
Enhancing Associative Learning in Rats With a Computationally Designed Training Protocol
Zhang, X. O., Zhang, Y., Cho, C. E., Engelke, D. S., Smolen, P. D., Byrne, J. H., & Monte, F. H. D. (2023) · Biological Psychiatry Global Open Science · doi:10.1016/j.bpsgos.2023.07.006 · Cited by 4
Hjernens plastisitet– perspektiver for rehabilitering etter hjerneslag
Dietriech, E. (2007) · NORA - Norwegian Open Research Archives · Cited by 4
Acute physical exercise prevents memory amnesia caused by protein synthesis inhibition in rats' hippocampus
Lima, K. R., das Neves, B.-H. S., Sigaran, G. J., da Rosa, A. C. D. S., Gomes, G. C. M., de Gomes, M. G., & Mello‐Carpes, P. B. (2024) · Neurochemistry International · doi:10.1016/j.neuint.2024.105740 · Cited by 4
The impact of temporal distribution on fear extinction learning
Ma, Y., Kyuchukova, D., Jiao, F., Batsikadze, G., Nitsche, M. A., & Yavari, F. (2025) · International Journal of Clinical and Health Psychology · doi:10.1016/j.ijchp.2024.100536 · Cited by 4
PKMζ-PKCι/λ double-knockout demonstrates atypical PKC is crucial for the persistence of hippocampal LTP and spatial memory
Tsokas, P., Hsieh, C., Grau-Perales, A. B., Tcherepanov, A., Kwok, L., Rodriguez-Valencia, L. M., Cano, D. A., Allen, K., Smith, H. J. H., Kubayeva, S., et al. (2026) · eLife · doi:10.7554/elife.110499.3 · Cited by 3
A behavioral tagging account of kinase contribution to memory formation after spaced aversive training
Budriesi, P., Tintorelli, R., Correa, J., Villar, M. E., Marchal, P., Giurfa, M., & Viola, H. (2023) · iScience · doi:10.1016/j.isci.2023.107278 · Cited by 3
Fear Conditioning and Extinction as a Model of PTSD in Mice
Gafford, G. M., & Ressler, K. J. (2011) · Neuromethods · doi:10.1007/978-1-61779-313-4_11 · Cited by 3
Spacing effects in learning and memory
Carpenter, S. K., & Pan, S. C. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-15754-7.00020-1 · Cited by 4
Bridging consensus and controversy in fear conditioning research via meta-analysis
Garofalo, S. (2023) · Peer community in neuroscience. · doi:10.24072/pci.neuro.100144 · Cited by 1
Emerging evidence for P body function in the peripheral nervous system
Tan, A. M. (2013) · Neuroscience Letters · doi:10.1016/j.neulet.2013.10.059 · Cited by 2
Mechanism based approaches for rescuing and enhancing cognition
LYNCH, G. S., & Gall, C. M. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00101 · Cited by 2
CREB: A Cornerstone of Memory Consolidation?
Josselyn, S. A., Mortezavi, M., & Silva, A. J. (2005) · Springer eBooks · doi:10.1007/0-387-25443-9_21 · Cited by 2
Comment les intervalles temporels entre les répétitions d’une information en influencent-ils la mémorisation ? Revue théorique des effets de pratique distribuée
Gerbier, É., & Koenig, O. (2015) · L’Année psychologique · doi:10.4074/s0003503315000159 · Cited by 3
Activity drives local CaMKII synthesis and subcellular localization via autophosphorylation-dependent pathwaysPreprint
Clements, K. J., Chen, N., Gonzalez, K. C., Zhang, Y., Rodal, A. A., & Griffith, L. C. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.11.03.686364 · Cited by 2
First insights on the signaling pathways related to CDKL5 regulation and on its possible involvement in synaptic plasticity
Montanara, P. L. (2013) · IrInSubria (University of Insubria) · Cited by 1
Chemosensory context conditioning in Caenorhabditis elegans
Lau, H. L. (2010) · cIRcle (University of British Columbia) · doi:10.14288/1.0071000 · Cited by 1
Trial-Spacing Effect in Associative Learning
Todd, T. P., & Bouton, M. E. (2012) · Springer eBooks · doi:10.1007/978-1-4419-1428-6_950 · Cited by 1
PKMζ-PKCι/λ double-knockout demonstrates atypical PKC is crucial for the persistence of hippocampal LTP and spatial memoryPreprint
Tsokas, P., Hsieh, C., Grau-Perales, A. B., Tcherepanov, A., Kwok, L., Rodriguez-Valencia, L. M., Cano, D. A., Allen, K. D., Smith, H. J., Kubayeva, S., et al. (2026) · eLife · doi:10.7554/elife.110499.1 · Cited by 1
Exploring exposure in vivo in chronic pain
de Jong, J. R. (2010) · doi:10.26481/dis.20101125jj
Cellular mechanisms of synaptic plasticity in hippocampal area CA1
Guire, E. S. (2006) · doi:10.6083/m4mw2fdw
The Role of the E3 Ubiquitin Ligases Nedd4-1 and Nedd4-2 in Synaptic Transmission and Plasticity
Takeda, M. (2013) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-3862
NEUROBIOLOGICAL PERSPECTIVES ON TRAUMA
Kirmayer, L. J., Lemelson, R., & Barad, M. (2007) · Cambridge University Press eBooks · doi:10.1017/cbo9780511500008.004 · Cited by 1
Mecanismos neurobiológicos involucrados en la persistencia de la memoria de largo término: rol de C-fos en hipocampo y corteza retrosplenial
Katche, C. (2011) · Repositorio Digital Institucional de la Universidad de Buenos Aires (Universidad de Buenos Aires)
THE ROLES OF NITRIC OXIDE SIGNALING AND cAMP RESPONSE ELEMENT BINDING PROTEIN IN FEAR CONDITIONING By
Kelley, J. B., & Kelley, J. B. (2016)
Re-evaluation of the hypothesis that LTP has two temporal phases and that the late phase is protein synthesis- dependent
Abbas, A.-K. (2015) · Gothenburg University Publications Electronic Archive (Gothenburg University)
All spaced out over memory and LTP
Nguyen, P. (2002) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(02)01968-x
Self-citation
All spaced out over memory and LTP
Nguyen, P. (2002) · Trends in Neurosciences · doi:10.1016/s0166-2236(02)02217-8
Self-citation
EL AULA COMO UN LECHO DE PROCUSTO: SOFISMAS YMANIPULACIÓN EN ENSEÑANZA DE LENGUAS EXTRANJERAS
Carvajal, C. A. B., & Gutiérrez, Y. A. (2014) · Espiral Revista de Docencia e Investigación · doi:10.15332/erdi.v4i1.555
Positive reinforcement training for laboratory mice
Cederwall, M. (2014) · Epsilon Archive for Student Projects (University of Southampton)
RoleoftheNeurograninConcentratedinSpinesinthe InductionofLong-TermPotentiation
NicholasCamp, R. (2006)
Fever and sickness behaviour during simulated Mycoplasma infection in rats
Swanepoel, T. (2013) · University of the Witwatersrand, Johannesburg Institutional Repository on DSpace (University of the Witwatersrand, Johannesburg)
A Study Of The Effects On Retention Of Different Time Intervals Between Opportunities To Learn
Clark, B. (2014) · UC Research Repository (University of Canterbury) · doi:10.26021/5021
Enhancing Motor Learning through Theoretical and Experimental Methods Acquisition, Retention, and Learning Strategies By
Huang, V. (2007)
Acute Synaptic Activity Causes Differential miRNA Expression in the Drosophila melanogaster Larval Central Nervous System
Sand, R. I. (2011) · Digital Commons - DU (University of Denver)
A loss-of-function study of CRTC1 in hippocampal neurons at basal state and during long-term synaptic plasticity
Lim, A. F. Y. (2019) · doi:10.32657/10220/49191
Neural Circuitry of Upper Airway Respiratory Plasticity: Identifying the Neural Circuitry Underlying Long-term Facilitation of Inspiratory Genioglossus Motor Output
Lui, S. K. C. (2019) · TSpace (University of Toronto)
Sulfotransferase activity contributes to long-term potentiation and long-term memoryPreprint
Sahoo, B., & Sharma, S. K. (2022) · Learning & Memory · doi:10.1101/lm.053538.121
Learning in motion for inclusion at school
Anello, F., Ferrara, G., & Pedone, F. (2024) · Pedagogical Perspective · doi:10.29329/pedper.2024.33
Olfactory Learning in Greater Short-Nosed Fruit Bat (Cynopterus sphinx)
Rajan, K. E., Mukilan, M., & Rajathei, D. M. (2025) · Springer eBooks · doi:10.1007/978-981-97-7324-4_12
PKMζ-PKCι/λ double-knockout demonstrates atypical PKC is crucial for the persistence of hippocampal LTP and spatial memoryPreprint
Tsokas, P., Hsieh, C., Grau-Perales, A. B., Tcherepanov, A., Kwok, L., Rodriguez-Valencia, L. M., Cano, D. A., Allen, K. D., Smith, H. J., Kubayeva, S., et al. (2026) · eLife · doi:10.7554/elife.110499

Authors: Scharf, M. T., Woo, N. H., Lattal, K. M., Young, J. Z., Nguyen, P. V., & Abel, T.
Affiliations: University of Pennsylvania (US)
Physiology and
Department of Biology and
University of Alberta (CA)
ORCID: Scharf, Matthew T.
Lattal, K. Matthew
Nguyen, Peter V.
Abel, Ted
Venue: Journal of Neurophysiology
Publisher: American Physiological Society
Published: 2002-06-01
Volume: 87
Issue: 6
Pages: 2770-2777
ISSN: 0022-3077 (ISSN-L)
1522-1598
DOI: 10.1152/jn.2002.87.6.2770
OpenAlex: W2259231394
Cited by: 204
References: 39
Citations by year: 2026: 7 · 2025: 3 · 2024: 5 · 2023: 7 · 2022: 6 · 2021: 5 · 2020: 4 · 2019: 6 · 2018: 9 · 2017: 6 · 2016: 11 · 2015: 9 · 2014: 11 · 2013: 13 · 2012: 8
FWCI: 5.84
Type: journal article
Language: en
Open access: closed
Locations: Journal of Neurophysiology (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute on Aging (AG18199, R01AG018199)
National Institute of Mental Health (R01MH060244, MH 60244)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (P30HD026979, HD 26979)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Keywords: spaced training, massed training, long-term potentiation, protein synthesis, long-term memory, contextual fear conditioning, hippocampus, synaptic plasticity, anisomycin, memory consolidation
MeSH terms: Animals, Anisomycin, Conditioning, Psychological, Electric Stimulation, Fear, Female, Hippocampus, Male, Memory, Mice, Inbred C57BL, Organ Culture Techniques, Protein Synthesis Inhibitors, Synapses, Long-Term Potentiation, Excitatory Postsynaptic Potentials, Mice

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Protein Synthesis Is Required for the Enhancement of Long-Term Potentiation and Long-Term Memory by Spaced Training

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks