BDNF activates mTOR to regulate GluR1 expression required for memory formation

Slipczuk, Leandro; Bekinschtein, Pedro; Katche, Cynthia; Cammarota, Martín; Izquierdo, Iván; Medina, Jorge H.

doi:10.1371/journal.pone.0006007

Cited by 246Memory and Neural MechanismsNeuroscience and Neuropharmacology ResearchPI3K/AKT/mTOR signaling in cancer

BDNF activates mTOR to regulate GluR1 expression required for memory formation

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Slipczuk, Leandro, Bekinschtein, Pedro, Katche, Cynthia, Cammarota, Martín, Izquierdo, Iván, Medina, Jorge H.·2009·PLoS ONE

DOI 10.1371/journal.pone.0006007PMC PMC2695538

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Abstract

BACKGROUND: The mammalian target of Rapamycin (mTOR) kinase plays a key role in translational control of a subset of mRNAs through regulation of its initiation step. In neurons, mTOR is present at the synaptic region, where it modulates the activity-dependent expression of locally-translated proteins independently of mRNA synthesis. Indeed, mTOR is necessary for different forms of synaptic plasticity and long-term memory (LTM) formation. However, little is known about the time course of mTOR activation and the extracellular signals governing this process or the identity of the proteins whose translation is regulated by this kinase, during mnemonic processing. METHODOLOGY/PRINCIPAL FINDINGS: Here we show that consolidation of inhibitory avoidance (IA) LTM entails mTOR activation in the dorsal hippocampus at the moment of and 3 h after training and is associated with a rapid and rapamycin-sensitive increase in AMPA receptor GluR1 subunit expression, which was also blocked by intra-hippocampal delivery of GluR1 antisense oligonucleotides (ASO). In addition, we found that pre- or post-training administration of function-blocking anti-BDNF antibodies into dorsal CA1 hampered IA LTM retention, abolished the learning-induced biphasic activation of mTOR and its readout, p70S6K and blocked GluR1 expression, indicating that BDNF is an upstream factor controlling mTOR signaling during fear-memory consolidation. Interestingly, BDNF ASO hindered LTM retention only when given into dorsal CA1 1 h after but not 2 h before training, suggesting that BDNF controls the biphasic requirement of mTOR during LTM consolidation through different mechanisms: an early one involving BDNF already available at the moment of training, and a late one, happening around 3 h post-training that needs de novo synthesis of this neurotrophin. CONCLUSIONS/SIGNIFICANCE: IN CONCLUSION, OUR FINDINGS DEMONSTRATE THAT: 1) mTOR-mediated mRNA translation is required for memory consolidation during at least two restricted time windows; 2) this kinase acts downstream BDNF in the hippocampus and; 3) it controls the increase of synaptic GluR1 necessary for memory consolidation.

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BDNF is a potent activator of mTOR signaling.
“Previous work has shown that BDNF is a potent activator of mTOR signaling (Jourdi et al., 2009; Takei et al., 2004; Slipczuk et al., 2009), and mTOR is a key integrator for many signaling pathways (see Costa-Mattioli and Monteggia, 2013).”
From BDNF - a key transducer of antidepressant effects (2016) · cites this paper as Slipczuk et al., 2009

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Cammarota, M., Izquierdo, I., Wolfman, C., DESTEIN, M. L., Bernabeu, R., Jerusalinsky, D. A., & Medina, J. H. (1995) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1995.0008 · Cited by 54 · see citing works
Self-citation
The substrate for long-lasting memory: If not protein synthesis, then what?
Routtenberg, A. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2007.10.012 · Cited by 40 · see citing works
Signaling Logic of Activity-Triggered Dendritic Protein Synthesis: An mTOR Gate But Not a Feedback Switch
Jain, P., & Bhalla, U. S. (2009) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000287 · Cited by 40 · see citing works
Is it systems or cellular consolidation? Time will tell. An alternative interpretation of the Morris group’s recent science paper
Rudy, J. W., & Sutherland, R. J. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2007.07.017 · Cited by 37 · see citing works
Spinal Astrocyte Glutamate Receptor 1 Overexpression after Ischemic Insult Facilitates Behavioral Signs of Spasticity and Rigidity
Hefferan, M. P., Kuchárová, K., Kinjo, K., Kakinohana, O., Sekerková, G., Nakamura, S., Fuchigami, T., Tomori, Z., Yaksh, T. L., Kurtz, N. M., et al. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.0989-07.2007 · Cited by 37 · see citing works
Amnesic Effects of Preacquisition, Postacquisition, or Preretrieval Tetrodotoxin Administration into the Medial Septal Area on Rat's Passive Avoidance Memorization
Lorenzini, C. A., Baldi, E., Bucherelli, C., & Tassoni, G. (1996) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1996.0045 · Cited by 18 · see citing works
Does assimilation into schemas involve systems or cellular consolidation? It’s not just time
Tse, D., Langston, R. F., Bethus, I., Wood, E. R., Witter, M. P., & Morris, R. (2007) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2007.09.007 · Cited by 16 · see citing works
Long-term potentiation and memory
Morris, R. (2004) · doi:10.1093/oso/9780198530305.003.0007 · Cited by 16 · see citing works

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mTOR signaling: At the crossroads of plasticity, memory and disease
Hoeffer, C. A., & Klann, E. (2010) · Trends in Neurosciences · doi:10.1016/j.tins.2009.11.003 · Cited by 1,128 · see citing works
BDNF - a key transducer of antidepressant effects
Björkholm, C., & Monteggia, L. M. (2016) · Neuropharmacology · doi:10.1016/j.neuropharm.2015.10.034 · Cited by 958 · see citing works
“Previous work has shown that BDNF is a potent activator of mTOR signaling (Jourdi et al., 2009; Takei et al., 2004; Slipczuk et al., 2009), and mTOR is a key integrator for many signaling pathways (see Costa-Mattioli and Monteggia, 2013).”
Background
A simple role for BDNF in learning and memory?
Cunha, C. (2010) · Frontiers in Molecular Neuroscience · doi:10.3389/neuro.02.001.2010 · Cited by 778 · see citing works
BDNF mediates adaptive brain and body responses to energetic challenges
Marosi, K., & Mattson, M. P. (2014) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2013.10.006 · Cited by 568 · see citing works
Signaling pathways underlying the rapid antidepressant actions of ketamine
Duman, R. S., Li, N., Liu, R.-J., Duric, V., & Aghajanian, G. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.08.044 · Cited by 537 · see citing works
Fear memory
Izquierdo, I., Furini, C. R. G., & Myskiw, J. C. (2016) · Physiological Reviews · doi:10.1152/physrev.00018.2015 · Cited by 453 · see citing works
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Neural and cellular mechanisms of fear and extinction memory formation
Orsini, C. A., & Maren, S. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.12.014 · Cited by 429 · see citing works
A critical role for IGF-II in memory consolidation and enhancement
Chen, D. Y., Stern, S. A., García‐Osta, A., Saunier-Rebori, B., Pollonini, G., Bambah-Mukku, D., Blitzer, R. D., & Alberini, C. M. (2011) · Nature · doi:10.1038/nature09667 · Cited by 421 · see citing works
Brain-Derived Neurotrophic Factor Val66Met Allele Impairs Basal and Ketamine-Stimulated Synaptogenesis in Prefrontal Cortex
Liu, R.-J., Lee, F. S., Li, X.-Y., Bambico, F., Duman, R. S., & Aghajanian, G. K. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.09.030 · Cited by 403 · see citing works
Exercise and time-dependent benefits to learning and memory
Berchtold, N. C., Castello, N. A., & Cotman, C. W. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.02.050 · Cited by 371 · see citing works
BDNF release is required for the behavioral actions of ketamine
Lepack, A. E., Fuchikami, M., Dwyer, J. M., Banasr, M., & Duman, R. S. (2015) · International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyu033 · Cited by 368 · see citing works
BDNF and memory processing
Bekinschtein, P., Cammarota, M., & Medina, J. H. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.04.024 · Cited by 351 · see citing works
Self-citation
Synaptic plasticity in depression: molecular, cellular and functional correlates.
Marsden, W. N. (2013) · Progress in Neuro-psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2012.12.012 · Cited by 321 · see citing works
Mammalian/mechanistic target of rapamycin (mTOR) complexes in neurodegeneration
Querfurth, H., & Lee, H.-K. (2021) · Molecular Neurodegeneration · doi:10.1186/s13024-021-00428-5 · Cited by 288 · see citing works
Effects of environmental enrichment and voluntary exercise on neurogenesis, learning and memory, and pattern separation: BDNF as a critical variable?
Bekinschtein, P., Oomen, C. A., Saksida, L. M., & Bussey, T. J. (2011) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2011.07.002 · Cited by 256 · see citing works
Self-citation
The neuroprotective effects of glucagon-like peptide 1 in Alzheimer’s and Parkinson’s disease: An in-depth review
Reich, N., & Hölscher, C. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.970925 · Cited by 248 · see citing works
mTOR: on target for novel therapeutic strategies in the nervous system
Maiese, K., Chong, Z. Z., Shang, Y., & Wang, S. (2012) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2012.11.001 · Cited by 226 · see citing works
The Persistence of Hippocampal-Based Memory Requires Protein Synthesis Mediated by the Prion-like Protein CPEB3
Fioriti, L., Myers, C., Huang, Y.-Y., Li, X., Stephan, J. S., Trifilieff, P., Colnaghi, L., Kosmidis, S., Drisaldi, B., Pavlopoulos, E., et al. (2015) · Neuron · doi:10.1016/j.neuron.2015.05.021 · Cited by 221 · see citing works
Targeting the Glutamatergic System to Treat Major Depressive Disorder: Rationale and Progress to Date
Mathews, D. C., Henter, I. D., & Zarate, C. A. (2012) · Drugs · doi:10.2165/11633130-000000000-00000 · Cited by 220 · see citing works
AMPA Receptor Synaptic Plasticity Induced by Psychostimulants: The Past, Present, and Therapeutic Future
Bowers, M. S., Chen, B. T., & Bonci, A. (2010) · Neuron · doi:10.1016/j.neuron.2010.06.004 · Cited by 218 · see citing works
Targeting molecules to medicine with mTOR, autophagy and neurodegenerative disorders
Maiese, K. (2015) · British Journal of Clinical Pharmacology · doi:10.1111/bcp.12804 · Cited by 200 · see citing works
Hippocampal–Prefrontal BDNF and Memory for Fear Extinction
Rosas-Vidal, L. E., Do-Monte, F. H., Sotres-Bayon, F., & Quirk, G. J. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.64 · Cited by 184 · see citing works
The Interaction between Early Life Epilepsy and Autistic-Like Behavioral Consequences: A Role for the Mammalian Target of Rapamycin (mTOR) Pathway
Talos, D. M., Sun, H., Zhou, X., Fitzgerald, E. C., Jackson, M. C., Klein, P., Lan, V. J., Joseph, A., & Jensen, F. E. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035885 · Cited by 182 · see citing works
Contextual learning requires synaptic AMPA receptor delivery in the hippocampus
Mitsushima, D., Ishihara, K., Sano, A., Kessels, H. W. H. G., & Takahashi, T. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1104558108 · Cited by 163 · see citing works
Clinically Significant Drug Interactions with Newer Antidepressants
Spina, E., Trifirò, G., & Caraci, F. (2011) · CNS Drugs · doi:10.2165/11594710-000000000-00000 · Cited by 160 · see citing works
Mammalian Target of Rapamycin: Hitting the Bull′s‐Eye for Neurological Disorders
Chong, Z. Z., Shang, Y., Zhang, L., Wang, S., & Maiese, K. (2010) · Oxidative Medicine and Cellular Longevity · doi:10.4161/oxim.3.6.14787 · Cited by 149 · see citing works
A Positive Autoregulatory BDNF Feedback Loop via C/EBPβ Mediates Hippocampal Memory Consolidation
Bambah-Mukku, D., Travaglia, A., Chen, D. Y., Pollonini, G., & Alberini, C. M. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.0324-14.2014 · Cited by 145 · see citing works
Estradiol-induced object recognition memory consolidation is dependent on activation of mTOR signaling in the dorsal hippocampusPreprint
Fortress, A. M., Fan, L., Orr, P. T., Zhao, Z., & Frick, K. M. (2013) · Learning & Memory · doi:10.1101/lm.026732.112 · Cited by 141 · see citing works
Role for mammalian target of rapamycin complex 1 signaling in neuroadaptations underlying alcohol-related disorders
Neasta, J., Hamida, S. B., Yowell, Q. V., Carnicella, S., & Dorit Ron, A. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1005554107 · Cited by 136 · see citing works
VGF function in depression and antidepressant efficacy
Jiang, C. S., Lin, W.-J., Sadahiro, M., Labonté, B., Ménard, C., Pfau, M. L., Tamminga, C. A., Turecki, G., Nestler, E. J., Russo, S. J., et al. (2017) · Molecular Psychiatry · doi:10.1038/mp.2017.233 · Cited by 123 · see citing works
Behavioral tagging of extinction learning
Myskiw, J. D. C., Benetti, F., & Izquierdo, I. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1220875110 · Cited by 124 · see citing works
Self-citation
mTOR complex 1: a key player in neuroadaptations induced by drugs of abuse
Neasta, J., Barak, S., Hamida, S. B., & Ron, D. (2014) · Journal of Neurochemistry · doi:10.1111/jnc.12725 · Cited by 114 · see citing works
A Critical Kinase Cascade In Neurological Disorders: Pi3K, Akt and Mtor
Chong, Z. Z., Shang, Y., Wang, S., & Maiese, K. (2012) · Future Neurology · doi:10.2217/fnl.12.72 · Cited by 119 · see citing works
Brain-derived neurotrophic factor activation of CaM-kinase kinase via transient receptor potential canonical channels induces the translation and synaptic incorporation of GluA1-containing calcium-permeable AMPA receptors
Fortin, D. A., Srivastava, T., Dwarakanath, D., Pierre, P., Nygaard, S., Derkach, V. A., & Soderling, T. R. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.6034-11.2012 · Cited by 120 · see citing works
Shedding new light on neurodegenerative diseases through the mammalian target of rapamycin
Chong, Z. Z., Shang, Y. C., Wang, S., & Maiese, K. (2012) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2012.08.001 · Cited by 119 · see citing works
Memory Retrieval Requires Ongoing Protein Synthesis and NMDA Receptor Activity-Mediated AMPA Receptor Trafficking
Lopez, J., Gamache, K., Schneider, R. E., & Nader, K. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.0735-14.2015 · Cited by 114 · see citing works
Consolidation and reconsolidation of contextual fear memory requires mammalian target of rapamycin-dependent translation in the dorsal hippocampus
Gafford, G. M., Parsons, R. G., & Helmstetter, F. J. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.03.023 · Cited by 110 · see citing works
Synaptic regulation of affective behaviors; role of BDNF
Ninan, I. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.04.011 · Cited by 111 · see citing works
Oxidant Stress and Signal Transduction in the Nervous System with the PI 3-K, Akt, and mTOR Cascade
Maiese, K., Chong, Z. Z., Wang, S., & Shang, Y. C. (2012) · International Journal of Molecular Sciences · doi:10.3390/ijms131113830 · Cited by 109 · see citing works
The Multiple Roles of Autophagy in Neural Function and Diseases
Li, Y., Qin, Z., & Sheng, R. (2023) · Neuroscience Bulletin · doi:10.1007/s12264-023-01120-y · Cited by 106 · see citing works
The antidepressant-like effects of glutamatergic drugs ketamine and AMPA receptor potentiator LY 451646 are preserved in bdnf+/− heterozygous null mice
Lindholm, J., Autio, H., Vesa, L., Antila, H., Lindemann, L., Hoener, M. C., Skolnick, P., Rantamäki, T., & Ċastrén, E. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.08.015 · Cited by 102 · see citing works
Glucocorticoids Modulate the mTOR Pathway in the Hippocampus: Differential Effects Depending on Stress History
Polman, J. A. E., Hunter, R. G., Speksnijder, N., van den Oever, J. M. E., Korobko, O. B., McEwen, B. S., de Kloet, E. R., & Datson, N. A. (2012) · Endocrinology · doi:10.1210/en.2012-1255 · Cited by 100 · see citing works
Exercise increases mTOR signaling in brain regions involved in cognition and emotional behavior
Lloyd, B. A., Hake, H. S., Ishiwata, T., Farmer, C. E., Loetz, E. C., Fleshner, M., Bland, S. T., & Greenwood, B. N. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.01.033 · Cited by 101 · see citing works
Environmental and pharmacological modulations of cellular plasticity: Role in the pathophysiology and treatment of depression
Ota, K. T., & Duman, R. S. (2013) · Neurobiology of Disease · doi:10.1016/j.nbd.2012.05.022 · Cited by 94 · see citing works
Deconvoluting mTOR biology
Weber, J. D., & Gutmann, D. H. (2012) · Cell Cycle · doi:10.4161/cc.11.2.19022 · Cited by 92 · see citing works
Frontier of Epilepsy Research - mTOR signaling pathway
Cho, C. (2011) · Experimental & Molecular Medicine · doi:10.3858/emm.2011.43.5.032 · Cited by 92 · see citing works
Inhibition of mTOR by rapamycin in the amygdala or hippocampus impairs formation and reconsolidation of inhibitory avoidance memory
Jobim, P. F. C., Pedroso, T. R., Christoff, R. R., Werenicz, A., Maurmann, N., Reolon, G. K., & Roesler, R. (2012) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2011.10.002 · Cited by 92 · see citing works
The mTOR Signaling Pathway in the Brain: Focus on Epilepsy and Epileptogenesis
Russo, E., Citraro, R., Constanti, A., & Sarro, G. D. (2012) · Molecular Neurobiology · doi:10.1007/s12035-012-8314-5 · Cited by 94 · see citing works
The First Alcohol Drink Triggers mTORC1-Dependent Synaptic Plasticity in Nucleus Accumbens Dopamine D1 Receptor Neurons
Beckley, J. T., Laguesse, S., Phamluong, K., Morisot, N., Wegner, S. A., & Dorit Ron, A. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.2254-15.2016 · Cited by 89 · see citing works
Signaling Pathways Mediating Alcohol Effects
Dorit Ron, A., & Messing, R. O. (2011) · Current topics in behavioral neurosciences · doi:10.1007/7854_2011_161 · Cited by 85 · see citing works
The integrated role of ACh, ERK and mTOR in the mechanisms of hippocampal inhibitory avoidance memory
Giovannini, M. G., Lana, D., & Pepeu, G. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.12.014 · Cited by 87 · see citing works
Mammalian Target of Rapamycin: Its Role in Early Neural Development and in Adult and Aged Brain Function
Garza-Lombó, C., & Gonsebatt, M. E. (2016) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2016.00157 · Cited by 85 · see citing works
SynGAP Regulates Protein Synthesis and Homeostatic Synaptic Plasticity in Developing Cortical Networks
Wang, C.-C., Held, R. G., & Hall, B. J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0083941 · Cited by 84 · see citing works
An Increase in Basal BDNF Provokes Hyperactivation of the Akt-Mammalian Target of Rapamycin Pathway and Deregulation of Local Dendritic Translation in a Mouse Model of Down's Syndrome
Troca-Marín, J. A., Alves-Sampaio, A., & Montesinos, M. L. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0011-11.2011 · Cited by 79 · see citing works
Is the mTOR‐signalling cascade disrupted in Schizophrenia?
Gururajan, A., & van den Buuse, M. (2014) · Journal of Neurochemistry · doi:10.1111/jnc.12622 · Cited by 81 · see citing works
Postsynaptic BDNF signalling regulates long‐term potentiation at thalamo‐amygdala afferents
Meis, S., Endres, T., & Leßmann, V. (2011) · The Journal of Physiology · doi:10.1113/jphysiol.2011.220434 · Cited by 76 · see citing works
GABAA Receptor Blockade Enhances Memory Consolidation by Increasing Hippocampal BDNF Levels
Kim, D. H., Kim, J. M., Park, S. J., Cai, M., Liu, X., Lee, S., Shin, C. Y., & Ryu, J. H. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.189 · Cited by 75 · see citing works
AMPA Receptor antagonist NBQX attenuates later-life epileptic seizures and autistic-like social deficits following neonatal seizures
Lippman-Bell, J. J., Rakhade, S., Klein, P. M., Obeid, M., Jackson, M., Joseph, A., & Jensen, F. E. (2013) · Epilepsia · doi:10.1111/epi.12378 · Cited by 68 · see citing works
Hippocampal noradrenergic activation is necessary for object recognition memory consolidation and can promote BDNF increase and memory persistence
Mello-Carpes, P. B., da Silva de Vargas, L., Gayer, M. C., Roehrs, R., & Izquierdo, I. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.11.014 · Cited by 75 · see citing works
Self-citation
Antigenic and mechanistic characterization of anti‐ AMPA receptor encephalitis
Gleichman, A. J., Panzer, J. A., Baumann, B. H., Dalmau, J. O., & Lynch, D. R. (2014) · Annals of Clinical and Translational Neurology · doi:10.1002/acn3.43 · Cited by 76 · see citing works
Molecular signatures and mechanisms of long-lasting memory consolidation and storage
Katche, C., Cammarota, M., & Medina, J. H. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.06.018 · Cited by 74 · see citing works
Self-citation
Neuronal stress signaling and eIF2α phosphorylation as molecular links between Alzheimer's disease and diabetes
Lourenco, M. V., Ferreira, S. T., & Felice, F. G. D. (2015) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2015.03.003 · Cited by 71 · see citing works
Sustained, neuron-specific IKK/NF-κB activation generates a selective neuroinflammatory response promoting local neurodegeneration with aging
Maqbool, A., Lattke, M., Wirth, T., & Baumann, B. (2013) · Molecular Neurodegeneration · doi:10.1186/1750-1326-8-40 · Cited by 72 · see citing works
Retrograde changes in presynaptic function driven by dendritic mTORC1
Henry, F. E., McCartney, A. J., Neely, R., Perez, A. S., Carruthers, C., Stuenkel, E., Inoki, K., & Sutton, M. A. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.2149-12.2012 · Cited by 68 · see citing works
Memory Reconsolidation
Alberini, C. M., Johnson, S. A., & Ye, X. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-386892-3.00005-6 · Cited by 69 · see citing works
Novelty exposure overcomes foot shock-induced spatial-memory impairment by processes of synaptic-tagging in rats
Almaguer‐Melian, W., Bergado, J. A., Fuentes, N. P., Alberti‐Amador, E., Mercerón‐Martínez, D., & Frey, J. U. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1114198109 · Cited by 70 · see citing works
Elimination of the vesicular acetylcholine transporter in the forebrain causes hyperactivity and deficits in spatial memory and long-term potentiation
Martyn, A. C., Jaeger, X. D., Magalhães, A. C., Kesarwani, R., Gonçalves, D. F., Raulic, S., Guzmán, M. S., Jackson, M. F., Izquierdo, I., MacDonald, J. F., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1215381109 · Cited by 69 · see citing works
Self-citation
Impairment of object recognition memory by rapamycin inhibition of mTOR in the amygdala or hippocampus around the time of learning or reactivation
Jobim, P. F. C., Pedroso, T. R., Werenicz, A., Christoff, R. R., Maurmann, N., Reolon, G. K., Schröder, N., & Roesler, R. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.12.004 · Cited by 68 · see citing works
Systemic inhibition of mTOR kinase via rapamycin disrupts consolidation and reconsolidation of auditory fear memory.
MacCallum, P. E., Hebert, M., Adamec, R., & Blundell, J. J. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.08.014 · Cited by 66 · see citing works
Hypothesized mechanisms through which acute exercise influences episodic memory
Loprinzi, P. D., Ponce, P., & Frith, E. (2018) · Physiology International · doi:10.1556/2060.105.2018.4.28 · Cited by 67 · see citing works
BDNF contributes to both rapid and homeostatic alterations in AMPA receptor surface expression in nucleus accumbens medium spiny neurons
Reimers, J. M., Loweth, J. A., & Wolf, M. E. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12422 · Cited by 66 · see citing works
β-Hydroxy-β-Methylbutyrate (HMB) Promotes Neurite Outgrowth in Neuro2a Cells
Salto, R., Vílchez, J. D., Girón, M. D., Cabrera, E., Campos, N., Manzano, M., Rueda, R., & López-Pedrosa, J. M. (2015) · PLoS ONE · doi:10.1371/journal.pone.0135614 · Cited by 65 · see citing works
Rapamycin attenuates the expression of cocaine‐induced place preference and behavioral sensitization
Bailey, J., Ma, D., & Szumlinski, K. K. (2012) · Addiction Biology · doi:10.1111/j.1369-1600.2010.00311.x · Cited by 61 · see citing works
BDNF controls object recognition memory reconsolidation
Radiske, A., Rossato, J. I., González, M. C., Köhler, C. A., Bevilaqua, L. R., & Cammarota, M. (2017) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2017.02.018 · Cited by 62 · see citing works
Self-citation
Alteration of BDNF in the medial prefrontal cortex and the ventral hippocampus impairs extinction of avoidance
Rosas-Vidal, L. E., Lozada-Miranda, V., Cantres-Rosario, Y. M., Vega-Medina, A., Meléndez, L. M., & Quirk, G. J. (2018) · Neuropsychopharmacology · doi:10.1038/s41386-018-0176-8 · Cited by 62 · see citing works
Utility of 7,8-dihydroxyflavone in preventing astrocytic and synaptic deficits in the hippocampus elicited by PTSD
Wang, J., Gao, F., Cui, S., Yang, S., Gao, F., Wang, X., & Zhu, G. (2022) · Pharmacological Research · doi:10.1016/j.phrs.2022.106079 · Cited by 61 · see citing works
Brain‐derived neurotrophic factor rapidly increases AMPA receptor surface expression in rat nucleus accumbens
Li, X., & Wolf, M. E. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07754.x · Cited by 57 · see citing works
Novel Insights into Depression and Antidepressants: A Synergy Between Synaptogenesis and Neurogenesis?
Bambico, F. R., & Belzung, C. (2012) · Current topics in behavioral neurosciences · doi:10.1007/7854_2012_234 · Cited by 57 · see citing works
Signaling mechanisms regulating synapse formation and function in mental retardation
Boda, B., Dubos, A., & Müller, D. (2010) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2010.03.012 · Cited by 57 · see citing works
Elevated lead levels from e-waste exposure are linked to decreased olfactory memory in children
Zhang, B., Huo, X., Xu, L., Cheng, Z., Cong, X., Lu, X., & Xu, X. (2017) · Environmental Pollution · doi:10.1016/j.envpol.2017.07.015 · Cited by 57 · see citing works
Dietary-induced obesity disrupts trace fear conditioning and decreases hippocampal reelin expression
Reichelt, A. C., Maniam, J., Westbrook, R. F., & Morris, M. J. (2014) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2014.07.005 · Cited by 58 · see citing works
Mild Thyroid Hormone Insufficiency During Development Compromises Activity-Dependent Neuroplasticity in the Hippocampus of Adult Male Rats
Gilbert, M. E., Sánchez-Huerta, K., & Wood, C. R. (2015) · Endocrinology · doi:10.1210/en.2015-1643 · Cited by 55 · see citing works
Targeted delivery of brain-derived neurotrophic factor for the treatment of blindness and deafness
Khalin, I., Kocherga, G., Bakar, M. A., & Alyautdin, R. N. (2015) · International Journal of Nanomedicine · doi:10.2147/ijn.s77480 · Cited by 57 · see citing works
Medial PFC AMPA receptor and BDNF signaling are required for the rapid and sustained antidepressant-like effects of 5-HT1A receptor stimulation
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mTOR signaling in the hippocampus is necessary for memory formation
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Self-citation
Translational Control via the Mammalian Target of Rapamycin Pathway Is Critical for the Formation and Stability of Long-Term Fear Memory in Amygdala Neurons
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mTOR inhibition impairs extinction memory reconsolidationPreprint
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Self-citation
Selective pharmacogenetic inhibition of mammalian target of Rapamycin complex I (mTORC1) blocks long-term synaptic plasticity and memory storage
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A role for BDNF- and NMDAR-induced lysosomal recruitment of mTORC1 in the regulation of neuronal mTORC1 activity
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Authors: Slipczuk, L., Bekinschtein, P., Katche, C., Cammarota, M., Izquierdo, I., & Medina, J. H.
Affiliations: Universidad de Buenos Aires (AR)
Pontifícia Universidade Católica do Rio Grande do Sul (BR)
Corresponding author: Medina, Jorge H.
ORCID: Slipczuk, Leandro
Bekinschtein, Pedro
Katche, Cynthia
Izquierdo, Iván
Medina, Jorge H.
Venue: PLoS ONE
Publisher: Public Library of Science (PLoS)
Published: 2009-06-23
Volume: 4
Issue: 6
Pages: e6007
ISSN: 1932-6203 (ISSN-L)
DOI: 10.1371/journal.pone.0006007
PMC: PMC2695538
OpenAlex: W2035139662
Cited by: 246
References: 90
Citations by year: 2026: 3 · 2025: 3 · 2024: 8 · 2023: 6 · 2022: 13 · 2021: 10 · 2020: 19 · 2019: 1 · 2018: 14 · 2017: 21 · 2016: 19 · 2015: 20 · 2014: 23 · 2013: 19 · 2012: 29
FWCI: 10.85
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (unspecified)
Locations: PLoS ONE (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Greater South Information System
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › PI3K/AKT/mTOR signaling in cancer
Keywords: brain-derived neurotrophic factor, mTOR signaling, GluR1, AMPA receptors, long-term memory consolidation, passive avoidance, fear memory, hippocampus, CA1, p70S6K, antisense oligonucleotides
MeSH terms: Animals, Hippocampus, Male, Memory, Models, Biological, Neuronal Plasticity, Protein Kinases, RNA, Messenger, Synapses, Time Factors, Rats, Wistar, Receptors, AMPA, Brain-Derived Neurotrophic Factor, Rats, TOR Serine-Threonine Kinases

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BDNF activates mTOR to regulate GluR1 expression required for memory formation

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