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.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
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?
In the citing paper
“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
Flagged first, then by citations
Research works printed but not linked: 1
- Franklin, K. B. J. & Paxinos, G. The Mouse Brain (Academic, San Diego, 1997)
Cited by
Sorted by citations
Items 301–400 of 1,005
Stress regulates endocannabinoid-CB1 receptor signaling
Hillard, C. J. (2014) · Seminars in Immunology · doi:10.1016/j.smim.2014.04.001 · Cited by 144
Endocannabinoids in Synaptic Plasticity and Neuroprotection
Xu, J., & Chen, C. (2014) · The Neuroscientist · doi:10.1177/1073858414524632 · Cited by 143
Marco, E. M. (2011) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2011.00063 · Cited by 139
Cannabinoid facilitation of fear extinction memory recall in humans
Rabinak, C. A., Angstadt, M., Sripada, C. S., Abelson, J. L., Liberzon, I., Milad, M. R., & Phan, K. L. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.06.063 · Cited by 163
Cabranes, A., Venderová, K., de Lago, E., Fezza, F., Sánchez, A., Mestre, L., Valenti, M., García‐Merino, A., Ramos, J. A., Marzo, V. D., et al. (2005) · Neurobiology of Disease · doi:10.1016/j.nbd.2005.03.002 · Cited by 135
Lafenêtre, P., Chaouloff, F., & Marsicano, G. (2007) · Pharmacological Research · doi:10.1016/j.phrs.2007.09.006 · Cited by 143
Self-citationEndocannabinoids in nervous system health and disease: the big picture in a nutshell
Skaper, S. D., & Marzo, V. D. (2012) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2012.0313 · Cited by 141
Reinforcement Learning With Modulated Spike Timing–Dependent Synaptic Plasticity
Farries, M. A., & Fairhall, A. L. (2007) · Journal of Neurophysiology · doi:10.1152/jn.00364.2007 · Cited by 135
Jung, K., Astarita, G., Yaşar, S., Vasilevko, V., Cribbs, D. H., Head, E., Cotman, C. W., & Piomelli, D. (2011) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2011.03.012 · Cited by 136
Ruehle, S., Remmers, F., Romo-Parra, H., Massa, F., Wickert, M., Wortge, S., Haring, M., Kaiser, N., Marsicano, G., Pape, H.-C., et al. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.4171-12.2013 · Cited by 132
Self-citationFatty Acid Amide Hydrolase Controls Mouse Intestinal Motility In Vivo
Capasso, R., Matias, I., Lutz, B., Borrelli, F., Capasso, F., Marsicano, G., Mascolo, N., Petrosino, S., Monory, K., Valenti, M., et al. (2005) · Gastroenterology · doi:10.1053/j.gastro.2005.06.018 · Cited by 136
Self-citationLópez‐Moreno, J. A., González‐Cuevas, G., Moreno, G., & Navarro, M. A. (2008) · Addiction Biology · doi:10.1111/j.1369-1600.2008.00105.x · Cited by 132
Disruption of CB1 receptor signaling impairs extinction of spatial memory in mice
Varvel, S. A., Anum, E. A., & Lichtman, A. H. (2004) · Psychopharmacology · doi:10.1007/s00213-004-2121-2 · Cited by 136
Cannich, A., Wotjak, C. T., Kamprath, K., Hermann, H., Lutz, B., & Marsicano, G. (2004) · Learning & Memory · doi:10.1101/lm.77904 · Cited by 130
Self-citationInteractions of the opioid and cannabinoid systems in reward: Insights from knockout studies
Befort, K. (2015) · Frontiers in Pharmacology · doi:10.3389/fphar.2015.00006 · Cited by 139
Mendizabal‐Zubiaga, J., Melser, S., Bénard, G., Ramos, A., Reguero, L., Arrabal, S., Elezgarai, I., Gerrikagoitia, I., Suárez, J., de Fonseca, F. R., et al. (2016) · Frontiers in Physiology · doi:10.3389/fphys.2016.00476 · Cited by 137
Self-citationKraft, B., Frickey, N., Kaufmann, R. M., Reif, M., Frey, R., Gustorff, B., & Kress, H. G. (2008) · Anesthesiology · doi:10.1097/aln.0b013e31817881e1 · Cited by 129
Sex differences in fear extinction
Velasco, E. R., Florido, A., Milad, M. R., & Andero, R. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.05.020 · Cited by 132
Habenular CB1 Receptors Control the Expression of Aversive Memories
Gómez, E. S., Busquets-García, A., Hu, F., Mehidi, A., Cannich, A., Roux, L., Louit, I., Alonso, L., Wiesner, T., Georges, F. E., et al. (2015) · Neuron · doi:10.1016/j.neuron.2015.08.035 · Cited by 127
Self-citationTerzian, A. L. B., Drago, F., Wotjak, C. T., & Micale, V. (2011) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2011.00049 · Cited by 127
Self-citationHill, M. N., Hillard, C. J., & McEwen, B. S. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq280 · Cited by 136
Takahashi, R. N., Pamplona, F. A., & Fernandes, M. S. (2005) · Neuroscience Letters · doi:10.1016/j.neulet.2005.01.049 · Cited by 127
Walter, L. M., Dinh, T. P., & Stella, N. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.2419-04.2004 · Cited by 131
Kishimoto, Y., & Kano, M. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.1236-06.2006 · Cited by 127
Cannabinoid modulation of executive functions
Pattij, T., Wiskerke, J., & Schoffelmeer, A. N. M. (2008) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2008.02.099 · Cited by 129
Zhu, P., & Lovinger, D. M. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1148-05.2005 · Cited by 131
Short- and long-term effects of cannabinoids on the extinction of contextual fear memory in rats
Pamplona, F. A., Bitencourt, R. M., & Takahashi, R. N. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.04.003 · Cited by 123
The learning of fear extinction
Furini, C., Myskiw, J., & Izquierdo, I. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.10.016 · Cited by 124
Endocannabinoid signals in the control of emotion
Lutz, B. (2009) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2008.12.001 · Cited by 128
Self-citationImpaired cannabinoid receptor type 1 signaling interferes with stress-coping behavior in mice
Steiner, M. A., Wanisch, K., Monory, K., Marsicano, G., Borroni, E., Bächli, H., Holsboer, F., Lutz, B., & Wotjak, C. T. (2007) · The Pharmacogenomics Journal · doi:10.1038/sj.tpj.6500466 · Cited by 130
Self-citationBiosynthesis, degradation and pharmacological importance of the fatty acid amides
Farrell, E. K., & Merkler, D. J. (2008) · Drug Discovery Today · doi:10.1016/j.drudis.2008.02.006 · Cited by 129
The Endocannabinoid System and Extinction Learning
Lutz, B. (2007) · Molecular Neurobiology · doi:10.1007/s12035-007-8004-x · Cited by 124
Self-citationNiehaus, J. L., Liu, Y., Wallis, K. T., Egertová, M., Bhartur, S. G., Mukhopadhyay, S., Shi, S., He, H., Selley, D. E., Howlett, A. C., et al. (2007) · Molecular Pharmacology · doi:10.1124/mol.107.039263 · Cited by 121
The role of prefrontal cortex CB1 receptors in the modulation of fear memory
Lin, H.-C., Mao, S.-C., Su, C.-L., & Gean, P.-W. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhn075 · Cited by 119
Ganon-Elazar, E., & Akirav, I. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2011.204 · Cited by 120
Di, S., Itoga, C. A., Fisher, M. O., Solomonow, J., Roltsch, E. A., Gilpin, N. W., & Tasker, J. G. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.2279-15.2016 · Cited by 127
Protective role of palmitoylethanolamide in contact allergic dermatitis
Petrosino, S., Cristino, L., Karsak, M., Gaffal, E., Ueda, N., Tüting, T., Bisogno, T., Filippis, D. D., D’Amico, A., Saturnino, C., et al. (2009) · Allergy · doi:10.1111/j.1398-9995.2009.02254.x · Cited by 120
Self-citationChung, S. C., Hammarsten, P., Josefsson, A., Stattin, P. E., Granfors, T., Egevad, L., Mancini, G., Lutz, B., Bergh, A. R. J., & Fowler, C. J. (2008) · European Journal of Cancer · doi:10.1016/j.ejca.2008.10.010 · Cited by 120
Self-citationGutiérrez‐Rodrίguez, A., Río, I. B., Puente, N., Gómez‐Urquijo, S., Fontaine, C. J., Huguet, J. E., Elezgarai, I., Ruehle, S., Lutz, B., Robin, L. M., et al. (2018) · Glia · doi:10.1002/glia.23314 · Cited by 127
Self-citationCasarotto, P. C., Terzian, A. L. B., Aguiar, D. C., Zangrossi, H., Guimarães, F. S., Wotjak, C. T., & Moreira, F. A. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2011.207 · Cited by 117
Self-citationGorzalka, B. B., & Hill, M. N. (2010) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2010.11.021 · Cited by 120
Brain sites involved in fear memory reconsolidation and extinction of rodents
Baldi, E., & Bucherelli, C. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.04.003 · Cited by 123
Jiang, B., Huang, S., Pasquale, R. D., Millman, D. J., Song, L., Lee, H., Tsumoto, T., & Kirkwood, A. (2010) · Neuron · doi:10.1016/j.neuron.2010.03.021 · Cited by 123
Bellocchio, L., Gómez, E. S., Quarta, C., Metna‐Laurent, M., Cardinal, P., Binder, E., Cannich, A., Delamarre, A., Häring, M., Martín‐Fontecha, M., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1218573110 · Cited by 118
Self-citationLötsch, J., Weyer-Menkhoff, I., & Tegeder, I. (2017) · European Journal of Pain · doi:10.1002/ejp.1148 · Cited by 123
Passie, T., Emrich, H. M., Karst, M., Brandt, S. D., & Halpern, J. H. (2012) · Drug Testing and Analysis · doi:10.1002/dta.1377 · Cited by 117
Modulation of the serotonin system by endocannabinoid signaling
Haj‐Dahmane, S., & Shen, R. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.02.016 · Cited by 126
Proteolysis of proBDNF Is a Key Regulator in the Formation of Memory
Barnes, P., & Thomas, K. L. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003248 · Cited by 121
Endocannabinoids and neurodegenerative diseases
Micale, V., Mazzola, C., & Drago, F. (2007) · Pharmacological Research · doi:10.1016/j.phrs.2007.09.008 · Cited by 119
Social Stress and Psychosis Risk: Common Neurochemical Substrates?
Mizrahi, R. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.274 · Cited by 122
Marzo, V. D., Bisogno, T., & PETROCELLIS, L. D. (2007) · Chemistry & Biology · doi:10.1016/j.chembiol.2007.05.014 · Cited by 118
Self-citationYoshida, T., Uchigashima, M., Yamasaki, M., Katona, I., Yamazaki, M., Sakimura, K., Kano, M., Yoshioka, M., & Watanabe, M. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1012875108 · Cited by 117
Role of the endocannabinoid system in drug addiction
Manzanares, J., Cabañero, D., Puente, N., García‐Gutiérrez, M. S., Grandes, P., & Maldonado, R. J. (2018) · Biochemical Pharmacology · doi:10.1016/j.bcp.2018.09.013 · Cited by 118
Pistis, M., Perra, S., Pillolla, G., Melis, M., Gessa, G., & Muntoni, A. (2004) · Neuropharmacology · doi:10.1016/j.neuropharm.2003.08.003 · Cited by 124
Hugues, S., Chessel, A., Léna, I., Marsault, R., & Garcia, R. (2006) · Synapse · doi:10.1002/syn.20291 · Cited by 114
Basavarajappa, B. S. (2007) · Current Neuropharmacology · doi:10.2174/157015907780866910 · Cited by 115
Neuropsychiatric Adverse Effects of Centrally Acting Antiobesity Drugs
Nathan, P. J., O’Neill, B. V., Napolitano, A., & Bullmore, E. T. (2010) · CNS Neuroscience & Therapeutics · doi:10.1111/j.1755-5949.2010.00172.x · Cited by 115
PTSD and stress sensitisation: A tale of brain and body Part 2: Animal models
Stam, R. (2007) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2007.01.001 · Cited by 117
Cannabinoid CB1 Receptor Calibrates Excitatory Synaptic Balance in the Mouse Hippocampus
Monory, K., Polack, M., Remus, A., Lutz, B., & Körte, M. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.3167-14.2015 · Cited by 116
Self-citationHill, M. N., & Patel, S. (2013) · Biology of Mood & Anxiety Disorders · doi:10.1186/2045-5380-3-19 · Cited by 120
Moreira, F. A., de Aguiar, D. C., Terzian, A. L. B., Guimarães, F. S., & Wotjak, C. T. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.08.046 · Cited by 113
Self-citationSignaling via CNS cannabinoid receptors
Mackie, K. (2008) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2008.01.022 · Cited by 112
Retrograde Signalling by Endocannabinoids
Vaughan, C. W., & Christie, M. J. (2005) · Springer eBooks · doi:10.1007/3-540-26573-2_12 · Cited by 113
Myers, K. M., & Carlezon, W. A. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.01.011 · Cited by 113
Huestis, M. A., Mazzoni, I. E., & Rabin, O. (2011) · Sports Medicine · doi:10.2165/11591430-000000000-00000 · Cited by 110
Cannabis: A Toxin-Producing Plant with Potential Therapeutic Uses
Breijyeh, Z., Jubeh, B., Bufo, S. A., Karaman, R., & Scrano, L. (2021) · Toxins · doi:10.3390/toxins13020117 · Cited by 126
Niyuhire, F., Varvel, S. A., Thorpe, A. J., Stokes, R. J., Wiley, J. L., & Lichtman, A. H. (2007) · Psychopharmacology · doi:10.1007/s00213-006-0650-6 · Cited by 110
Galante, M., & Diana, M. A. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.0403-04.2004 · Cited by 110
Galve‐Roperh, I., Palazuelos, J., Aguado, T., & Guzmán, M. (2009) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-009-0028-y · Cited by 113
The use of cognitive enhancers in animal models of fear extinction
Kaplan, G. B., & Moore, K. A. (2011) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2011.01.009 · Cited by 113
Naydenov, A. V., Horne, E. A., Cheah, C. S., Swinney, K., Hsu, K., Cao, J. K., Marrs, W., Blankman, J. L., Tu, S., Cherry, A. E., et al. (2014) · Neuron · doi:10.1016/j.neuron.2014.06.030 · Cited by 111
The Shared Neuroanatomy and Neurobiology of Comorbid Chronic Pain and PTSD
Scioli, E. R., Forman, D. E., Otis, J. D., Gregor, K. L., Valovski, I. T., & Rasmusson, A. M. (2014) · Clinical Journal of Pain · doi:10.1097/ajp.0000000000000115 · Cited by 122
Köfalvi, A. (2007) · Springer eBooks · doi:10.1007/978-0-387-74349-3 · Cited by 110
Increased endocannabinoid levels reduce the development of precancerous lesions in the mouse colon
Izzo, A. A., Aviello, G., Petrosino, S., Orlando, P., Marsicano, G., Lutz, B., Borrelli, F., Capasso, R., Nigam, S., Capasso, F., et al. (2007) · Journal of Molecular Medicine · doi:10.1007/s00109-007-0248-4 · Cited by 109
Self-citationLin, H.-C., Mao, S.-C., & Gean, P.-W. (2006) · Learning & Memory · doi:10.1101/lm.217006 · Cited by 107
Panlilio, L. V., Justinová, Z., & Goldberg, S. R. (2013) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2013.01.003 · Cited by 106
Lever, I. J., & Rice, A. S. C. (2007) · Springer eBooks · doi:10.1007/978-3-540-33823-9_10 · Cited by 108
DEOLIVEIRAALVARES, L., De-Oliveira, L. M., de Almeida, C. C. S., Diehl, F., Genro, B. P., Lanziotti, V. M. N. B., & Quillfeldt, J. A. (2004) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2004.10.002 · Cited by 108
A therapeutic role for cannabinoid CB1 receptor antagonists in major depressive disorders
Witkin, J. M., Tzavara, E. T., Davis, R. J., Li, X., & Nomikos, G. G. (2005) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2005.10.006 · Cited by 110
Functional mapping of GABAA receptor subtypes in the amygdala
Marowsky, A., Fritschy, J., & Vogt, K. E. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03574.x · Cited by 107
Llorente‐Berzal, A., Terzian, A. L. B., Marzo, V. D., Micale, V., Viveros, M., & Wotjak, C. T. (2015) · Psychopharmacology · doi:10.1007/s00213-015-3917-y · Cited by 112
Self-citationNicotine and cannabinoids: parallels, contrasts and interactions
VIVEROS, M., MARCO, E., & FILE, S. (2006) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2006.08.002 · Cited by 106
Mouse models of genetic effects on cognition: Relevance to schizophrenia
Papaleo, F., Lipska, B. K., & Weinberger, D. R. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.04.025 · Cited by 107
Qin, Z., Zhou, X. C., Pandey, N. R., Vecchiarelli, H. A., Stewart, C. A., Zhang, X., Lagace, D. C., Brunel, J. M., Béïque, J.-C., Stewart, A. F. R., et al. (2015) · Neuron · doi:10.1016/j.neuron.2015.02.015 · Cited by 106
Kamprath, K., Plendl, W., Marsicano, G., Deussing, J. M., Wurst, W., Lutz, B., & Wotjak, C. T. (2008) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2008.00463.x · Cited by 104
Self-citationHeterosynaptic Long-Term Potentiation of Inhibitory Interneurons in the Lateral Amygdala
Bauer, E. P., & LeDoux, J. E. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.3567-04.2004 · Cited by 105
Alterations in the Hippocampal Endocannabinoid System in Diet-Induced Obese Mice
Massa, F., Mancini, G., Schmidt, H., Steindel, F., Mackie, K., Angioni, C., Oliet, S. H. R., Geißlinger, G., & Lutz, B. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.2648-09.2010 · Cited by 105
Self-citationKruk-Słomka, M., Dzik, A., Budzyńska, B., & Biała, G. (2016) · Molecular Neurobiology · doi:10.1007/s12035-016-0313-5 · Cited by 117
Bimodal Control of Fear-Coping Strategies by CB 1 Cannabinoid Receptors
Metna‐Laurent, M., Gómez, E. S., Verrier, D., Conforzi, M., Jégo, P., Lafenêtre, P., & Marsicano, G. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.1054-12.2012 · Cited by 111
Self-citationSuplita, R. L., Farthing, J. N., Gutierrez, T., & Hohmann, A. G. (2005) · Neuropharmacology · doi:10.1016/j.neuropharm.2005.07.007 · Cited by 104
FROM THE NEUROBIOLOGY OF EXTINCTION TO IMPROVED CLINICAL TREATMENTS
Morrison, F. G., & Ressler, K. J. (2013) · Depression and Anxiety · doi:10.1002/da.22214 · Cited by 107
Wenzel, J. M., Oleson, E. B., Gove, W. N., Cole, A. B., Gyawali, U., Dantrassy, H. M., Bluett, R. J., Dryanovski, D. I., Stuber, G. D., Deisseroth, K. A., et al. (2018) · Current Biology · doi:10.1016/j.cub.2018.03.037 · Cited by 102
Anandamide hydrolysis: a new target for anti-anxiety drugs?
Gaetani, S., Cuomo, V., & Piomelli, D. (2003) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2003.09.005 · Cited by 104
SR141716A, a cannabinoid CB1 receptor antagonist, improves memory in a delayed radial maze task
Wolff, M. C., & Leander, J. D. (2003) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2003.08.025 · Cited by 103
Dubreucq, S., Koehl, M., Abrous, D. N., Marsicano, G., & Chaouloff, F. (2010) · Experimental Neurology · doi:10.1016/j.expneurol.2010.01.017 · Cited by 103
Self-citationCannabinoid signaling in health and disease
Lu, Y., & Anderson, H. D. (2017) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/cjpp-2016-0346 · Cited by 105
Cellular and intracellular mechanisms involved in the cognitive impairment of cannabinoids
Puighermanal, E., Busquets-García, A., Maldonado, R. J., & Ozaita, A. (2012) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2011.0384 · Cited by 104
Empirical support for an involvement of the mesostriatal dopamine system in human fear extinction
Raczka, K. A., Mechias, M.-L., Gartmann, N., Reif, A., Deckert, J., Pessiglione, M., & Kalisch, R. (2011) · Translational Psychiatry · doi:10.1038/tp.2011.10 · Cited by 102
Cannabinoid Regulation of Fear and Anxiety: an Update
Papagianni, E. P., & Stevenson, C. W. (2019) · Current Psychiatry Reports · doi:10.1007/s11920-019-1026-z · Cited by 108
Dissecting the cannabinergic control of behavior: The where matters
Busquets-García, A., Desprez, T., Metna‐Laurent, M., Bellocchio, L., Marsicano, G., & Gómez, E. S. (2015) · BioEssays · doi:10.1002/bies.201500046 · Cited by 111
Self-citation
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
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
