The DOI matches its Crossref record; 31 of the 31 references it cites were found in a registry or an index.
The endogenous cannabinoid system controls extinction of aversive memories
Abstract
Acquisition and storage of aversive memories is one of the basic principles of central nervous systems throughout the animal kingdom. In the absence of reinforcement, the resulting behavioural response will gradually diminish to be finally extinct. Despite the importance of extinction, its cellular mechanisms are largely unknown. The cannabinoid receptor 1 (CB1) and endocannabinoids are present in memory-related brain areas and modulate memory. Here we show that the endogenous cannabinoid system has a central function in extinction of aversive memories. CB1-deficient mice showed strongly impaired short-term and long-term extinction in auditory fear-conditioning tests, with unaffected memory acquisition and consolidation. Treatment of wild-type mice with the CB1 antagonist SR141716A mimicked the phenotype of CB1-deficient mice, revealing that CB1 is required at the moment of memory extinction. Consistently, tone presentation during extinction trials resulted in elevated levels of endocannabinoids in the basolateral amygdala complex, a region known to control extinction of aversive memories. In the basolateral amygdala, endocannabinoids and CB1 were crucially involved in long-term depression of GABA (gamma-aminobutyric acid)-mediated inhibitory currents. We propose that endocannabinoids facilitate extinction of aversive memories through their selective inhibitory effects on local inhibitory networks in the amygdala.
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“Following their binding to central nervous system receptors (e.g.CB1 receptors), endocannabinoids have been shown, e.g., to reduce anxiety (Marsicano et al., 2002;Lutz et al., 2015) and increase food intake (Di Marzo et al., 2001).”
From Sleep restriction alters plasma endocannabinoids concentrations before but not after exercise in humans (2016) · cites this paper as Marsicano et al., 2002
In the citing paper
“Moreover, there is an emerging body of evidence demonstrating an important role for CB1 receptor-mediated endocannabinoid signaling in the extinction of aversive memories8.”
From Elevated brain cannabinoid CB1 receptor availability in post-traumatic stress disorder: A positron emission tomography study (2013) · cites this paper as [8]
In the citing paper
“As part of this protective role under aversive conditions, elevated EC signaling during stress has been shown to dampen the development of anxiety [12] and to regulate the encoding [13], retrieval [14] and extinction [15] of traumatic memories.”
From Plasma concentrations of endocannabinoids and related primary fatty acid amides in patients with post-traumatic stress disorder (2013) · cites this paper as [15]
In the citing paper
“Additionally, inhibition of FAAH facilitates long-term fear extinction and rescues deficient fear extinction in rodent models by enhancing AEA–CB1 (cannabinoid type 1) receptor signaling and synaptic plasticity in the BLA.”
From Amygdala FAAH and anandamide: mediating protection and recovery from stress (2013) · cites this paper as [86]
In the citing paper
“Marsicano and colleagues reported elevated AEA and 2-AG BLA levels after extinction training in mice [86]”
From Amygdala FAAH and anandamide: mediating protection and recovery from stress (2013) · cites this paper as [86]
In the citing paper
“One notable finding is that a CB1R-dependent form of synaptic plasticity in BLA [51,86], long-term depression of inhibitory GABAergic transmission (LTDi), is enhanced by FAAH KO [51] and by the FAAH inhibitor AM3506 at doses that promote extinction [50].”
From Amygdala FAAH and anandamide: mediating protection and recovery from stress (2013) · cites this paper as [86]
In the citing paper
“and produced impairments in extinction learning (but not fear conditioning) by CB1R KO or systemic antagonist (SR141716A) administration [28,86]”
From Amygdala FAAH and anandamide: mediating protection and recovery from stress (2013) · cites this paper as [86]
In the citing paper
“This suggests a scheme in which AEA released during extinction relieves a tonic inhibitory brake on BLA output neurons [50,51,86] necessary for the encoding of extinction memories [102] (Figure 2).”
From Amygdala FAAH and anandamide: mediating protection and recovery from stress (2013) · cites this paper as [86]
In the citing paper
“The cannabinoid system is part of the complex circuitry that regulates anxiety and stress and is a crucial mediator of emotional learning (Marsicano et al, 2002;Viveros et al, 2005;Patel et al, 2005Patel et al, , 2005a; Laviolette and Grace, 2006;Varvel et al, 2007;Ganon-Elazar and Akirav, 2009;Lutz, 2009;Hill et al, 2009;Abush and Akirav, 2010;Akirav, 2011).”
From Cannabinoids prevent the development of behavioral and endocrine alterations in a rat model of intense stress (2012) · cites this paper as Marsicano et al, 2002
Citations
Cites
LeDoux, J. E. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.155 · Cited by 8,444
Structure of a cannabinoid receptor and functional expression of the cloned cDNA
Matsuda, L. A., Lolait, S. J., Brownstein, M. J., Young, A. C., & Bonner, T. I. (1990) · Nature · doi:10.1038/346561a0 · Cited by 5,011
Genetic enhancement of learning and memory in mice
Tang, Y., Shimizu, E., Dubé, G., Rampon, C., Kerchner, G. A., Zhuo, M., Liu, G., & Tsien, J. Z. (1999) · Nature · doi:10.1038/43432 · Cited by 1,878
SR141716A, a potent and selective antagonist of the brain cannabinoid receptor
Rinaldi, M. L., Barth, F., Héaulme, M., Shire, D. J., Calandra, B., Congy, C., Martinez, S., Maruani, J., Neliat, G., Caput, D., et al. (1994) · FEBS Letters · doi:10.1016/0014-5793(94)00773-x · Cited by 1,762
Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses
Wilson, R. I., & Nicoll, R. A. (2001) · Nature · doi:10.1038/35069076 · Cited by 1,607
The role of ventromedial prefrontal cortex in the recovery of extinguished fear
Quirk, G. J., Russo, G. K., Barron, J. L., & Lebron, K. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-16-06225.2000 · Cited by 957 · cited 1×
“; however, there is increasing evidence that some cellular pathways are specifically involved in extinction, but not in acquisition or consolidation of fear memorie”
BackgroundMarsicano, G., & Lutz, B. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00847.x · Cited by 937
Self-citationExtinction of emotional learning: contribution of medial prefrontal cortex
Morgan, M. A., Romanski, L. M., & LeDoux, J. E. (1993) · Neuroscience Letters · doi:10.1016/0304-3940(93)90241-c · Cited by 897 · cited 1×
“To confirm this assumption, we measured in C57BL/6J mice levels of the two major endocannabinoids, anandamide (AEA) and 2-arachidonoylglycerol (2-AG), in brain punches of the medial prefrontal cortex (mPFC) and the basolateral amygdala complex (BLAC), both of which are thought to have central roles in extinction of av…”
BackgroundOhno‐Shosaku, T., Maejima, T., & Kano, M. (2001) · Neuron · doi:10.1016/s0896-6273(01)00247-1 · Cited by 874
Cannabinoid receptors and pain
Pertwee, R. G. (2001) · Progress in Neurobiology · doi:10.1016/s0301-0082(00)00031-9 · Cited by 741
Research works printed but not linked: 1
- Franklin, K. B. J. & Paxinos, G. The Mouse Brain (Academic, San Diego, 1997)
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The Endocannabinoid System as an Emerging Target of Pharmacotherapy
Pacher, P., Bátkai, S., & Kunos, G. (2006) · Pharmacological Reviews · doi:10.1124/pr.58.3.2 · Cited by 2,077
The molecular logic of endocannabinoid signalling
Piomelli, D. (2003) · Nature Reviews Neuroscience · doi:10.1038/nrn1247 · Cited by 1,957
Neurons in medial prefrontal cortex signal memory for fear extinction
Milad, M. R., & Quirk, G. J. (2002) · Nature · doi:10.1038/nature01138 · Cited by 1,836
Neuronal circuits for fear and anxiety
Tovote, P., Fadok, J. P., & Lüthi, A. (2015) · Nature Reviews Neuroscience · doi:10.1038/nrn3945 · Cited by 1,786
Stress, memory and the amygdala
Roozendaal, B., McEwen, B. S., & Chattarji, S. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2651 · Cited by 1,760
Neural Mechanisms of Extinction Learning and Retrieval
Quirk, G. J., & Mueller, D. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301555 · Cited by 1,645
Taming THC: potential cannabis synergy and phytocannabinoid-terpenoid entourage effects.
Russo, E. B. (2011) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2011.01238.x · Cited by 1,535
Endocannabinoid-Mediated Control of Synaptic Transmission
Kano, M., Ohno‐Shosaku, T., Hashimotodani, Y., Uchigashima, M., & Watanabe, M. (2009) · Physiological Reviews · doi:10.1152/physrev.00019.2008 · Cited by 1,595
Myers, K. M., & Davis, M. (2007) · Molecular Psychiatry · doi:10.1038/sj.mp.4001939 · Cited by 1,277
The ascent of mouse: advances in modelling human depression and anxiety
Cryan, J. F., & Holmes, A. (2005) · Nature Reviews Drug Discovery · doi:10.1038/nrd1825 · Cited by 1,198
A Comprehensive Profile of Brain Enzymes that Hydrolyze the Endocannabinoid 2-Arachidonoylglycerol
Blankman, J. L., Simon, G. M., & Cravatt, B. F. (2007) · Chemistry & Biology · doi:10.1016/j.chembiol.2007.11.006 · Cited by 1,177
Cota, D., Marsicano, G., Tschöp, M. H., Grübler, Y., Flachskamm, C., Schubert, M. I., Auer, D. P., Yassouridis, A., Thöne‐Reineke, C., Ortmann, S., et al. (2003) · Journal of Clinical Investigation · doi:10.1172/jci17725 · Cited by 1,168
Self-citationMemory Reconsolidation and Extinction Have Distinct Temporal and Biochemical Signatures
Suzuki, A., Josselyn, S. A., Frankland, P. W., Masushige, S., Silva, A. J., & Kida, S. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.5491-03.2004 · Cited by 1,127
Endocannabinoid Signaling and Synaptic Function
Castillo, P. E., Younts, T. J., Chávez, A. E., & Hashimotodani, Y. (2012) · Neuron · doi:10.1016/j.neuron.2012.09.020 · Cited by 1,191
Metaplasticity: tuning synapses and networks for plasticity
Abraham, W. C. (2008) · Nature reviews. Neuroscience · doi:10.1038/nrn2356 · Cited by 1,166
The endocannabinoid system and the brain.
Mechoulam, R., & Parker, L. A. (2013) · Annual Review of Psychology · doi:10.1146/annurev-psych-113011-143739 · Cited by 1,090
The endocannabinoid system and its therapeutic exploitation
Marzo, V. D., Bifulco, M., & Petrocellis, L. D. (2004) · Nature Reviews Drug Discovery · doi:10.1038/nrd1495 · Cited by 1,090
CB1 Cannabinoid Receptors and On-Demand Defense Against Excitotoxicity
Marsicano, G., Goodenough, S., Monory, K., Hermann, H., Eder, M., Cannich, A., Azad, S. C., Cascio, M. G., Gutiérrez, S. O., van der Stelt, M., et al. (2003) · Science · doi:10.1126/science.1088208 · Cited by 1,208
Self-citationBisogno, T., Howell, F., Williams, G., Minassi, A., Cascio, M. G., Ligresti, A., Matias, I., Schiano-Moriello, A., Paul, P., Williams, E.-J., et al. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200305129 · Cited by 1,039
Self-citationPape, H.-C., & Pare, D. (2010) · Physiological Reviews · doi:10.1152/physrev.00037.2009 · Cited by 994
The neurobiology and control of anxious states
Millan, M. J. (2003) · Progress in Neurobiology · doi:10.1016/s0301-0082(03)00087-x · Cited by 978
Selective blockade of 2-arachidonoylglycerol hydrolysis produces cannabinoid behavioral effects
Long, J. Z., Li, W., Booker, L., Burston, J. J., Kinsey, S. G., Schlosburg, J. E., Pavón, F. J., Serrano, A., Selley, D. E., Parsons, L. H., et al. (2008) · Nature Chemical Biology · doi:10.1038/nchembio.129 · Cited by 954
Behavioral and Neural Analysis of Extinction
Myers, K. M., & Davis, M. (2002) · Neuron · doi:10.1016/s0896-6273(02)01064-4 · Cited by 918
Amygdala inhibitory circuits and the control of fear memory
Ehrlich, I., Humeau, Y., Grenier, F., Ciocchi, S., Herry, C., & Lüthi, A. (2009) · Neuron · doi:10.1016/j.neuron.2009.05.026 · Cited by 878
The Emerging Role of the Endocannabinoid System in Endocrine Regulation and Energy Balance
Pagotto, U., Marsicano, G., Cota, D., Lutz, B., & Pasquali, R. (2005) · Endocrine Reviews · doi:10.1210/er.2005-0009 · Cited by 891
Self-citationTargeting the endocannabinoid system: to enhance or reduce?
Marzo, V. D. (2008) · Nature Reviews Drug Discovery · doi:10.1038/nrd2553 · Cited by 822
ENDOCANNABINOID-MEDIATED SYNAPTIC PLASTICITY IN THE CNS
Chevaleyre, V., Takahashi, K. A., & Castillo, P. E. (2006) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.29.051605.112834 · Cited by 829
Amygdala Microcircuits Controlling Learned Fear
Duvarci, S., & Pare, D. (2014) · Neuron · doi:10.1016/j.neuron.2014.04.042 · Cited by 751
Distribution of cannabinoid receptors in the central and peripheral nervous system
Mackie, K. (2005) · Handbook of Experimental Pharmacology · doi:10.1007/3-540-26573-2_10 · Cited by 744
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Peters, J., Kalivas, P. W., & Quirk, G. J. (2009) · Learning & Memory · doi:10.1101/lm.1041309 · Cited by 736
The Endocannabinoid System Controls Key Epileptogenic Circuits in the Hippocampus
Monory, K., Massa, F., Egertová, M., Eder, M., Blaudzun, H., Westenbroek, R., Kelsch, W., Jacob, W., Marsch, R., Ekker, M., et al. (2006) · Neuron · doi:10.1016/j.neuron.2006.07.006 · Cited by 706
Self-citationButler, R. K., & Finn, D. P. (2009) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2009.04.003 · Cited by 768
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Morena, M., Patel, S., Bains, J. S., & Hill, M. N. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.166 · Cited by 698
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Chevaleyre, V., & Castillo, P. E. (2003) · Neuron · doi:10.1016/s0896-6273(03)00235-6 · Cited by 647
Multiple Functions of Endocannabinoid Signaling in the Brain
Katona, I., & Freund, T. F. (2012) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062111-150420 · Cited by 630
History of Cannabis and Its Preparations in Saga, Science, and Sobriquet
Russo, E. B. (2007) · Chemistry & Biodiversity · doi:10.1002/cbdv.200790144 · Cited by 630
Neocortical LTD via Coincident Activation of Presynaptic NMDA and Cannabinoid Receptors
Sjöström, P. J., Turrigiano, G. G., & Nelson, S. B. (2003) · Neuron · doi:10.1016/s0896-6273(03)00476-8 · Cited by 629
Cannabinoid physiology and pharmacology: 30 years of progress
Howlett, A. C., Breivogel, C. S., Childers, S. R., Deadwyler, S. A., Hampson, R. E., & Porrino, L. J. (2004) · Neuropharmacology · doi:10.1016/j.neuropharm.2004.07.030 · Cited by 608
Retrograde signaling in the regulation of synaptic transmission: focus on endocannabinoids
Alger, B. E. (2002) · Progress in Neurobiology · doi:10.1016/s0301-0082(02)00080-1 · Cited by 616
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Bénard, G., Massa, F., Puente, N., Lourenço, J., Bellocchio, L., Soria-Gómez, E., Matias, I., Delamarre, A., Metna-Laurent, M., Cannich, A., et al. (2012) · Nature Neuroscience · doi:10.1038/nn.3053 · Cited by 588
Self-citationCannabinoids mediate analgesia largely via peripheral type 1 cannabinoid receptors in nociceptors
Agarwal, N., Pacher, P., Tegeder, I., Amaya, F., Constantin, C. E., Brenner, G. J., Rubino, T., Michalski, C. W., Marsicano, G., Monory, K., et al. (2007) · Nature Neuroscience · doi:10.1038/nn1916 · Cited by 571
Self-citationCrippa, J. A. S., Derenusson, G. N., Ferrari, T. B., Wichert-Ana, L., Duran, F. L., Martin-Santos, R., Simões, M. V., Bhattacharyya, S., Fusar-Poli, P., Atakan, Z., et al. (2011) · Journal of Psychopharmacology · doi:10.1177/0269881110379283 · Cited by 535
The acute effects of cannabinoids on memory in humans: a review
Ranganathan, M., & D’Souza, D. C. (2006) · Psychopharmacology · doi:10.1007/s00213-006-0508-y · Cited by 544
Han, J., Kesner, P., Metna-Laurent, M., Duan, T., Xu, L., Georges, F., Koehl, M., Abrous, D. N., Mendizabal-Zubiaga, J., Grandes, P., et al. (2012) · Cell · doi:10.1016/j.cell.2012.01.037 · Cited by 514
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Mackie, K. (2005) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.46.120604.141254 · Cited by 518
The endocannabinoid system in guarding against fear, anxiety and stress
Lutz, B., Marsicano, G., Maldonado, R., & Hillard, C. J. (2015) · Nature reviews. Neuroscience · doi:10.1038/nrn4036 · Cited by 506
Self-citationBunge, M. (2004) · Philosophy of the Social Sciences · doi:10.1177/0048393103262550 · Cited by 520
Regional Brain Abnormalities Associated With Long-term Heavy Cannabis Use
Yücel, M., Solowij, N., Respondek, C., Whittle, S., Fornito, A., Pantelis, C., & Lubman, D. I. (2008) · Archives of General Psychiatry · doi:10.1001/archpsyc.65.6.694 · Cited by 495
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Herry, C., Ferraguti, F., Singewald, N., Letzkus, J. J., Ehrlich, I., & Lüthi, A. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07101.x · Cited by 484
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VIVEROS, M., MARCO, E., & FILE, S. (2005) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2005.01.029 · Cited by 485
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Heifets, B. D., & Castillo, P. E. (2009) · Annual Review of Physiology · doi:10.1146/annurev.physiol.010908.163149 · Cited by 516
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de Quervain, D., Schwabe, L., & Roozendaal, B. (2017) · Nature Reviews Neuroscience · doi:10.1038/nrn.2016.155 · Cited by 484
Endocannabinoid signalling in reward and addiction
Parsons, L. H., & Hurd, Y. L. (2015) · Nature reviews. Neuroscience · doi:10.1038/nrn4004 · Cited by 488
Patel, S., Roelke, C. T., Rademacher, D. J., Cullinan, W. E., & Hillard, C. J. (2004) · Endocrinology · doi:10.1210/en.2004-0638 · Cited by 475
The Endocannabinoid System and Pain
Guindon, J., & Hohmann, A. (2009) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/187152709789824660 · Cited by 476
Campos, A. C., Moreira, F. A., Gomes, F. V., Del Bel, E. A., & Guimarães, F. S. (2012) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2011.0389 · Cited by 475
Stress Hormone Regulation: Biological Role and Translation into Therapy
Holsboer, F., & Ising, M. (2010) · Annual Review of Psychology · doi:10.1146/annurev.psych.093008.100321 · Cited by 473
Ligresti, A., PETROCELLIS, L. D., & Marzo, V. D. (2016) · Physiological Reviews · doi:10.1152/physrev.00002.2016 · Cited by 505
Fusar-Poli, P., Crippa, J. A., Bhattacharyya, S., Borgwardt, S. J., Allen, P., Martin-Santos, R., Seal, M., Surguladze, S. A., O’Carrol, C., Atakan, Z., et al. (2009) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2008.519 · Cited by 465
The endogenous cannabinoid system protects against colonic inflammation
Massa, F., Marsicano, G., Hermann, H., Cannich, A., Monory, K., Cravatt, B. F., Ferri, G., Sibaev, A., Storr, M., & Lutz, B. (2004) · Journal of Clinical Investigation · doi:10.1172/jci19465 · Cited by 461
Self-citationThe probability of neurotransmitter release: variability and feedback control at single synapses
Branco, T., & Staras, K. (2009) · Nature reviews. Neuroscience · doi:10.1038/nrn2634 · Cited by 467
Inverse agonism and neutral antagonism at cannabinoid CB1 receptors
Pertwee, R. G. (2004) · Life Sciences · doi:10.1016/j.lfs.2004.10.025 · Cited by 444
Pharmacological Profile of the Selective FAAH Inhibitor KDS-4103 (URB597)
Piomelli, D., Tarzia, G., Duranti, A., Tontini, A., Mor, M., Compton, T. R., Dasse, O. A., Monaghan, E. P., Parrott, J. A., & Putman, D. (2006) · CNS Drug Reviews · doi:10.1111/j.1527-3458.2006.00021.x · Cited by 451
How the Neurocircuitry and Genetics of Fear Inhibition May Inform Our Understanding of PTSD
Jovanović, T., & Ressler, K. J. (2010) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2009.09071074 · Cited by 457
A cannabinoid link between mitochondria and memory
Hebert-Chatelain, E., Desprez, T., Serrat, R., Bellocchio, L., Soria-Gomez, E., Busquets-Garcia, A., Pagano Zottola, A. C., Delamarre, A., Cannich, A., Vincent, P., et al. (2016) · Nature · doi:10.1038/nature20127 · Cited by 434
Self-citationSotres-Bayon, F., Cain, C. K., & LeDoux, J. E. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.10.012 · Cited by 433
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
Emotional Perseveration: An Update on Prefrontal-Amygdala Interactions in Fear ExtinctionPreprint
Sotres-Bayón, F., Bush, D. E. A., & LeDoux, J. E. (2004) · Learning & Memory · doi:10.1101/lm.79504 · Cited by 419
50 years of hurdles and hope in anxiolytic drug discovery
Griebel, G., & Holmes, A. (2013) · Nature Reviews Drug Discovery · doi:10.1038/nrd4075 · Cited by 430
THE ENDOCANNABINOID SYSTEM: PHYSIOLOGY AND PHARMACOLOGY
de Fonseca, F. R., del Arco, I., Bermúdez‐Silva, F. J., Bilbao, A., Cippitelli, A., & Navarro, M. (2004) · Alcohol and Alcoholism · doi:10.1093/alcalc/agh110 · Cited by 419
Singewald, N., Schmuckermair, C., Whittle, N., Holmes, A., & Ressler, K. J. (2015) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2014.12.004 · Cited by 390
“…Reference CB1 KO − − ns No drug (Cannich et al., 2004) CB1 KO − ns ns No drug ((Dubreucq et al., 2010); (Kamprath et al., 2006); (Marsicano et al., 2002); (Plendl & Wotjak, 2010)) D1-CB1 KO − ns ns No drug (Terzian et al., 2011) SR141716A CB1 ant ns No effect1 ns sc…”
BackgroundInfluentialThe Study of Fear Extinction: Implications for Anxiety Disorders
Graham, B. M., & Milad, M. R. (2011) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2011.11040557 · Cited by 387
Cannabinoid modulation of hippocampal long-term memory is mediated by mTOR signaling
Puighermanal, E., Marsicano, G., Busquets-García, A., Lutz, B., Maldonado, R. J., & Ozaita, A. (2009) · Nature Neuroscience · doi:10.1038/nn.2369 · Cited by 381
Self-citationTwo Coincidence Detectors for Spike Timing-Dependent Plasticity in Somatosensory Cortex
Bender, V. A., Bender, K. J., Brasier, D. J., & Feldman, D. E. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0176-06.2006 · Cited by 373
Pharmacological treatment of alcohol dependence: Target symptoms and target mechanisms
Heilig, M. A., & Egli, M. (2006) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2006.02.001 · Cited by 382
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Chhatwal, J. P., Davis, M., Maguschak, K. A., & Ressler, K. J. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300655 · Cited by 376
GABAA receptor diversity and pharmacology
Möhler, H. (2006) · Cell and Tissue Research · doi:10.1007/s00441-006-0284-3 · Cited by 368
Neumeister, A., Normandin, M. D., Pietrzak, R. H., Piomelli, D., Zheng, M. Q., Gujarro-Anton, A., Potenza, M. N., Bailey, C. R., Lin, S. F., Najafzadeh, S., et al. (2013) · Molecular Psychiatry · doi:10.1038/mp.2013.61 · Cited by 361
Hill, M. N., Patel, S., Carrier, E. J., Rademacher, D. J., Ormerod, B. K., Hillard, C. J., & Gorzalka, B. B. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300601 · Cited by 363
Kreitzer, A. C., & Malenka, R. C. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2959-05.2005 · Cited by 358
Simon, G. M., & Cravatt, B. F. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m604660200 · Cited by 360
SUGIURA, T., KISHIMOTO, S., OKA, S., & Gokoh, M. (2006) · Progress in Lipid Research · doi:10.1016/j.plipres.2006.03.003 · Cited by 374
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The therapeutic potential of cannabis
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Metadata
- Authors
- Marsicano, G., Wotjak, C. T., Azad, S. C., Bisogno, T., Rammes, G., Cascio, M. G., Hermann, H., Tang, J., Hofmann, C., Zieglgänsberger, W., Di Marzo, V., & Lutz, B.
- Affiliations
- Max Planck Institute of Psychiatry (DE)
- LMU Klinikum (DE)
- Istituto di Chimica Biomolecolare (IT)
- Helmholtz Munich (DE)
- Corresponding author
- Lutz, Beat
- Venue
- Nature
- Published
- 2002-08
- Volume
- 418
- Issue
- 6897
- Pages
- 530-534
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W1982291289
- Cited by
- 1,728
- References
- 30
- Citations by year
- 2026: 22 · 2025: 39 · 2024: 41 · 2023: 48 · 2022: 60 · 2021: 61 · 2020: 60 · 2019: 70 · 2018: 64 · 2017: 77 · 2016: 75 · 2015: 87 · 2014: 90 · 2013: 87 · 2012: 85
- FWCI
- 42.91
- 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)
- Max Planck Institute for Plasma Physics (submittedVersion)
- Topics
- Health Sciences › Medicine › Pharmacology (medical) › Cannabis and Cannabinoid Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- endocannabinoid system, CB1 receptor, CB1 knockout mice, fear extinction, auditory fear conditioning, basolateral amygdala, long-term depression, GABAergic inhibition, SR141716A, memory consolidation, inhibitory neural networks
- MeSH terms
- Rimonabant, Acoustic Stimulation, Amygdala, Animals, Cannabinoids, Conditioning, Classical, Electrophysiology, Extinction, Psychological, Fear, gamma-Aminobutyric Acid, Male, Memory, Mice, Inbred C57BL, Neuronal Plasticity, Neurons, Piperidines, Pyrazoles, Receptors, Drug, Synapses, Gene Deletion, Mice, Knockout, Receptors, Cannabinoid, Mice, Cannabinoid Receptor Modulators, In Vitro Techniques
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