Posttraining activation of CB1 cannabinoid receptors in the CA1 region of the dorsal hippocampus impairs object recognition long-term memory
Abstract
Evidence indicates that brain endocannabinoids are involved in memory processing. However, the participation of CB1 and CB2 cannabinoid receptors in recognition memory has not been yet conclusively determined. Therefore, we evaluated the effect of the posttraining activation of hippocampal cannabinoid receptors on the consolidation of object recognition memory. Rats with infusion cannulae stereotaxically aimed to the CA1 region of the dorsal hippocampus were trained in an object recognition learning task involving exposure to two different stimulus objects. Memory retention was assessed at different times after training. In the test sessions, one of the objects presented during training was replaced by a novel one. When infused in the CA1 region immediately after training, the non-selective cannabinoid receptor agonist WIN-55,212-2 and the endocannabinoid membrane transporter inhibitor VDM-11 blocked long-term memory retention in a dose-dependent manner without affecting short-term memory, exploratory behavior, anxiety state or the functionality of the hippocampus. The amnesic effect of WIN-55,212-2 and VDM-11 was not due to state-dependency and was completely reversed by co-infusion of the CB1 receptor antagonist AM-251 and mimicked by the CB1 receptor agonist ACEA but not by the CB2 receptor agonists JWH-015 and palmitoylethanolamide. Our data indicate that activation of hippocampal CB1 receptors early after training hampers consolidation of object recognition memory.
Integrity signals
Registry
Cites
Statistics
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?
Post-sample infusions of WIN 55,212-2 or VDM-11, an endocannabinoid membrane transporter inhibitor, into the hippocampal CA1 region impaired long-term but not short-term NOP memory in a dose-dependent manner.
“Post-sample infusions of WIN 55,212–2 or VDM-11, an endocannabinoid membrane transporter inhibitor, into the hippocampal CA1 region impaired long-term, but not short-term, NOP memory in a dose-dependent manner”
From The medial prefrontal cortex - hippocampus circuit that integrates information of object, place and time to construct episodic memory in rodents: Behavioral, anatomical and neurochemical properties (2020) · cites this paper as Clarke et al., 2008
CA1 infusion of the cannabinoid 1-R agonist ACEA, but not the cannabinoid 2-R agonist JWH-015 or palmitoylethanolamide, had similar effects, suggesting a role of hippocampal cannabinoid 1-R in NOP consolidation.
“Similar effects were found by the CA1 infusion of the cannabinoid 1-R agonist ACEA, but not the cannabinoid 2-R agonist JWH-015 or palmitoylethanolamide, an endogenous fatty acid amide with affinity to cannabinoid-R GPR55 and GPR119, suggesting a role of hippocampal cannabinoid 1-R in NOP consolidation”
From The medial prefrontal cortex - hippocampus circuit that integrates information of object, place and time to construct episodic memory in rodents: Behavioral, anatomical and neurochemical properties (2020) · cites this paper as Clarke et al., 2008
Cites
The rat brain in stereotaxic coordinates
Palkovits, M. (1983) · Neuropeptides · doi:10.1016/0143-4179(83)90049-5 · Cited by 28,959 · see citing works
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat
Pellow, S., Chopin, P., File, S. E., & Briley, M. (1985) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(85)90031-7 · Cited by 5,822 · see citing works
Molecular characterization of a peripheral receptor for cannabinoids
Munro, S., Thomas, K. L., & Abu-Shaar, M. (1993) · Nature · doi:10.1038/365061a0 · Cited by 5,092 · see citing works
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 · see citing works
A new one-trial test for neurobiological studies of memory in rats. 1: behavioral data
Ennaceur, A., & Delacour, J. (1988) · Behavioural Brain Research · doi:10.1016/0166-4328(88)90157-x · Cited by 3,223 · see citing works
Cannabinoid receptor localization in brain.
Herkenham, M., Lynn, A. B., Little, M. D., Johnson, M. R., Melvin, L. S., de Costa, B. R., & Rice, K. C. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.5.1932 · Cited by 2,321 · see citing works
The endogenous cannabinoid system controls extinction of aversive memories
Marsicano, G., Wotjak, C. T., Azad, S. C., Bisogno, T., Rammes, G., Cascio, M. G., Hermann, H., Tang, J., Hofmann, C., Zieglgänsberger, W., et al. (2002) · Nature · doi:10.1038/nature00839 · Cited by 1,728 · see citing works
Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses
Wilson, R. I., & Nicoll, R. A. (2001) · Nature · doi:10.1038/35069076 · Cited by 1,607 · see citing works
A second endogenous cannabinoid that modulates long-term potentiation
Stella, N., Schweitzer, P., & Piomelli, D. (1997) · Nature · doi:10.1038/42015 · Cited by 1,496 · see citing works
Effects of rimonabant on metabolic risk factors in overweight patients with dyslipidemia
Després, J.-P., Golay, A., & Sjöström, L. (2005) · New England Journal of Medicine · doi:10.1056/nejmoa044537 · Cited by 1,392 · see citing works
Logothetis, N. K., & Sheinberg, D. L. (1996) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.19.030196.003045 · Cited by 1,360 · see citing works
Katona, I., Sperlágh, B., Sı́k, A., Käfalvi, A., Vizi, E. S., Mackie, K., & Freund, T. F. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-11-04544.1999 · Cited by 1,218 · see citing works
Impaired Recognition Memory in Rats after Damage to the Hippocampus
Clark, R. E., Zola, S. M., & Squire, L. R. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-23-08853.2000 · Cited by 740 · see citing works
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 · see citing works
Pharmacological Actions of Cannabinoids
Pertwee, R. G. (2005) · Springer eBooks · doi:10.1007/3-540-26573-2_1 · Cited by 600 · see citing works
Showalter, V. M., Compton, D. M., Martin, B. R., & Abood, M. E. (1996) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)20744-3 · Cited by 572 · see citing works
Discovery of the Presence and Functional Expression of Cannabinoid CB2 Receptors in Brain
Onaivi, E. S., Ishiguro, H., GONG, J., Sejal, P., Perchuk, A., Meozzi, P. A., MYERS, L., Mora, Z., Tagliaferro, P. A., Gardner, E., et al. (2006) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1369.052 · Cited by 546 · see citing works
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 517 · see citing works
Molecular Composition of the Endocannabinoid System at Glutamatergic Synapses
Katona, I., Urbán, G. M., Wallace, M., Ledent, C., Jung, K.-M., Piomelli, D., Mackie, K., & Freund, T. F. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.0309-06.2006 · Cited by 511 · see citing works
Involvement of CB1 cannabinoid receptors in emotional behaviour
Martín, M., Ledent, C. A., Parmentier, M., Maldonado, R. J., & Valverde, O. (2002) · Psychopharmacology · doi:10.1007/s00213-001-0946-5 · Cited by 507 · see citing works
Kruman, I. I., Guo, Q., & Mattson, M. P. (1998) · Journal of Neuroscience Research · doi:10.1002/(sici)1097-4547(19980201)51:3 · Cited by 377 · see citing works
Hillard, C. J., Manna, S., Greenberg, M. J., DiCamelli, R. F., Ross, R. A., Stevenson, L., Murphy, V. L., Pertwee, R. G., & Campbell, W. B. (1999) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)38289-8 · Cited by 373 · see citing works
Neural mechanisms of object recognition
Riesenhuber, M., & Poggio, T. (2002) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(02)00304-5 · Cited by 373 · see citing works
Tsou, K., Mackie, K., Sañudo-Peña, M. C., & Walker, J. M. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00086-x · Cited by 343 · see citing works
Endocannabinoids facilitate the induction of LTP in the hippocampus
Carlson, G. C., Wang, Y., & Alger, B. E. (2002) · Nature Neuroscience · doi:10.1038/nn879 · Cited by 336 · see citing works
Mechanism of Cannabinoid Effects on Long-Term Potentiation and Depression in Hippocampal CA1 Neurons
Misner, D., & Sullivan, J. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-16-06795.1999 · Cited by 287 · see citing works
Improvement of memory in rodents by the selective CB1 cannabinoid receptor antagonist, SR 141716
Terranova, J.-P., Storme, J.-J., Lafon, N., Perio, A., Rinaldi, M. L., Fur, G. L., & Soubrié, P. (1996) · Psychopharmacology · doi:10.1007/bf02246352 · Cited by 283 · see citing works
Rossato, J. I., Bevilaqua, L. R. M., Myskiw, J. C., Medina, J. H., Izquierdo, I., & Cammarota, M. (2007) · Learning & Memory · doi:10.1101/lm.422607 · Cited by 282 · see citing works
Adverse effects of cannabis on health: an update of the literature since 1996
Kalant, H. (2004) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2004.05.027 · Cited by 264 · see citing works
Gatley, S. J., Gifford, A. N., Volkow, N. D., Lan, R., & Makriyannis, A. (1996) · European Journal of Pharmacology · doi:10.1016/0014-2999(96)00279-8 · Cited by 252 · see citing works
Evaluation of CB1 Receptor Knockout Mice in the Morris Water Maze
Varvel, S. A., & Lichtman, A. H. (2002) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.301.3.915 · Cited by 245 · see citing works
Domenici, M. R., Azad, S. C., Marsicano, G., Schierloh, A., Wotjak, C. T., Dodt, H.-U., Zieglgänsberger, W., Lutz, B., & Rammes, G. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.0372-06.2006 · Cited by 224 · see citing works
D’Argenio, G., Valenti, M., Scaglione, G., Cosenza, V., Sorrentini, I., & Marzo, V. D. (2006) · The FASEB Journal · doi:10.1096/fj.05-4943fje · Cited by 223 · see citing works
Cannabinoids, hippocampal function and memory
Hampson, R. E., & Deadwyler, S. A. (1999) · Life Sciences · doi:10.1016/s0024-3205(99)00294-5 · Cited by 221 · see citing works
Cannabinoid Function in Learning, Memory and Plasticity
Riedel, G., & Davies, S. N. (2005) · Springer eBooks · doi:10.1007/3-540-26573-2_15 · Cited by 219 · see citing works
Terranova, J.-P., Michaud, J.-C., Fur, G. L., & Soubrié, P. (1995) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/bf00169393 · Cited by 206 · see citing works
Enhancement of memory in cannabinoid CB1 receptor knock-out mice
Reibaud, M., Obinu, M. C., Ledent, C. A., Parmentier, M., Böhme, G. A., & Impérato, A. (1999) · European Journal of Pharmacology · doi:10.1016/s0014-2999(99)00496-3 · Cited by 189 · see citing works
Hashimotodani, Y., Ohno‐Shosaku, T., & Kano, M. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.4159-06.2007 · Cited by 186 · see citing works
Functions of cannabinoid receptors in the hippocampus
Davies, S. N., Pertwee, R. G., & Riedel, G. (2002) · Neuropharmacology · doi:10.1016/s0028-3908(02)00060-6 · Cited by 182 · see citing works
Sullivan, J. (2000) · Learning & Memory · doi:10.1101/lm.7.3.132 · Cited by 173 · see citing works
Sullivan, J. (1999) · Journal of Neurophysiology · doi:10.1152/jn.1999.82.3.1286 · Cited by 173 · see citing works
SR 141716A enhances spatial memory as assessed in a radial-arm maze task in rats
Lichtman, A. H. (2000) · European Journal of Pharmacology · doi:10.1016/s0014-2999(00)00615-4 · Cited by 171 · see citing works
Early age-related cognitive impairment in mice lacking cannabinoid CB1 receptors
Bilkei‐Gorzó, A., Rácz, I., Valverde, O., Otto, M., Michel, K., Sarstre, M., & Zimmer, A. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504640102 · Cited by 166 · see citing works
Differential effects of Δ 9 -THC on spatial reference and working memory in mice
Varvel, S. A., Hamm, R. L., Martin, B. R., & Lichtman, A. H. (2001) · Psychopharmacology · doi:10.1007/s002130100780 · Cited by 160 · see citing works
Maccarrone, M., Valverde, O., Barbaccia, M. L., Castañé, A., Maldonado, R. J., Ledent, C. A., Parmentier, M., & Finazzi‐Agrò, A. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.01957.x · Cited by 151 · see citing works
Enhanced long-term potentiation in mice lacking cannabinoid CB1 receptors
Böhme, G. A., Laville, M., Ledent, C. A., Parmentier, M., & Impérato, A. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00483-2 · Cited by 149 · see citing works
Cannich, A., Wotjak, C. T., Kamprath, K., Hermann, H., Lutz, B., & Marsicano, G. (2004) · Learning & Memory · doi:10.1101/lm.77904 · Cited by 130 · see citing works
Hohmann, A. G., Tsou, K., & Walker, J. M. (1999) · Journal of Neurophysiology · doi:10.1152/jn.1999.81.2.575 · Cited by 126 · see citing works
On the participation of mTOR in recognition memory.
Myskiw, J., Rossato, J., Bevilaqua, L., Medina, J., Izquierdo, I., & Cammarota, M. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2007.10.002 · Cited by 118 · see citing works
Risk factors for schizophrenia — All roads lead to dopamine
Forti, M. D., Lappin, J., & Murray, R. M. (2007) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2007.02.005 · Cited by 113 · see citing works
Lambert, D. M., DiPaolo, F. G., Sonveaux, P., Kanyonyo, M. R., Govaerts, S. J., Hermans, E., Bueb, J., Delzenne, N. M., & Tschirhart, E. J. (1999) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/s1388-1981(99)00132-8 · Cited by 113 · see citing works
Learning Impairment Produced in Rats by the Cannabinoid Agonist HU 210 in a Water-Maze Task
Ferrari, F., Ottani, A., Vivoli, R., & Giuliani, D. (1999) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(99)00106-9 · Cited by 111 · see citing works
Silva, G. E. D., & Takahashi, R. N. (2002) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/s0278-5846(01)00275-5 · Cited by 110 · see citing works
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 · see citing works
In vivo pharmacological actions of two novel inhibitors of anandamide cellular uptake
de Lago, E., Ligresti, A., Ortar, G., Morera, E., Cabranes, A., Pryce, G., Bifulco, M., Baker, D., Fernández‐Ruíz, J., & Marzo, V. D. (2003) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2003.11.027 · Cited by 98 · see citing works
Nowicky, A. V., Teyler, T. J., & Vardaris, R. M. (1987) · Brain Research Bulletin · doi:10.1016/0361-9230(87)90052-9 · Cited by 96 · see citing works
Alvares, L. D. O., Genro, B. P., Breda, R. V., Pedroso, M. F., da Costa, J. C., & Quillfeldt, J. A. (2006) · Brain Research · doi:10.1016/j.brainres.2005.11.101 · Cited by 95 · see citing works
Collins, D. R., Pertwee, R. G., & Davies, S. N. (1995) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.1995.tb15889.x · Cited by 92 · see citing works
Endocannabinoids restrict hippocampal long-term potentiation via CB1
Slanina, K. A., Roberto, M., & Schweitzer, P. (2005) · Neuropharmacology · doi:10.1016/j.neuropharm.2005.04.021 · Cited by 89 · see citing works
CB1 Receptor Antagonism Increases Hippocampal Acetylcholine Release: Site and Mechanism of Action
Degroot, A., Köfalvi, A., Wade, M. R., Davis, R. J., Rodrigues, R. J., Rebola, N., Cunha, R. A., & Nomikos, G. G. (2006) · Molecular Pharmacology · doi:10.1124/mol.106.024661 · Cited by 82 · see citing works
The Search for Selective Ligands for the CB2 Receptor
Huffman, J. (2000) · Current Pharmaceutical Design · doi:10.2174/1381612003399347 · Cited by 75 · see citing works
Input-specific plasticity at excitatory synapses mediated by endocannabinoids in the dentate gyrus
Chiu, C. Q., & Castillo, P. E. (2007) · Neuropharmacology · doi:10.1016/j.neuropharm.2007.06.026 · Cited by 73 · see citing works
da Silva, W. C. F. N., Bonini, J. S., Bevilaqua, L. R., Medina, J. H., Izquierdo, I., & Cammarota, M. (2007) · Hippocampus · doi:10.1002/hipo.20362 · Cited by 68 · see citing works
Jaggar, S., Sellaturay, S., & Rice, A. S. C. (1998) · Neuroscience Letters · doi:10.1016/s0304-3940(98)00621-1 · Cited by 60 · see citing works
Hill, M. N., Froc, D. J., Fox, C. J., Gorzalka, B. B., & Christie, B. R. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03522.x · Cited by 59 · see citing works
Paton, G., Pertwee, R. G., & Davies, S. N. (1998) · Neuropharmacology · doi:10.1016/s0028-3908(98)00096-3 · Cited by 59 · see citing works
Robinson, L., Goonawardena, A. V., Pertwee, R. G., Hampson, R. E., & Riedel, G. (2007) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0707273 · Cited by 59 · see citing works
Role of cortical cannabinoid CB1 receptor in conditioned taste aversion memory
Kobilo, T., Hazvi, S., & Dudai, Y. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05561.x · Cited by 58 · see citing works
Izquierdo, L. A., Barros, D. M., da Costa, J. C., Furini, C. R. G., Zinn, C. G., Cammarota, M., Bevilaqua, L. R., & Izquierdo, I. (2007) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2007.04.014 · Cited by 52 · see citing works
Cannabinoids, endogenous ligands and synthetic analogs
Pop, E. (1999) · Current Opinion in Chemical Biology · doi:10.1016/s1367-5931(99)80062-3 · Cited by 45 · see citing works
BEVILAQUA, L., DASILVA, W., MEDINA, J., IZQUIERDO, I., & CAMMAROTA, M. (2005) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2005.03.005 · Cited by 35 · see citing works
Endocannabinoid Liberation from Neurons in Transsynaptic Signaling
Lovinger, D. M. (2007) · Journal of Molecular Neuroscience · doi:10.1007/s12031-007-0043-2 · Cited by 23 · see citing works
Bura, S. A., Castañé, A., Ledent, C. A., Valverde, O., & Maldonado, R. J. (2007) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0707152 · Cited by 21 · see citing works
Thiemann, G., Fletcher, B. C., Ledent, C. A., Molleman, A., & Hasenöhrl, R. U. (2007) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2007.07.013 · Cited by 11 · see citing works
Flagged first, then by citations
1 of the 76 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
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 · see citing works
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 · see citing works
Campolongo, P., Roozendaal, B., Trezza, V., Hauer, D., Schelling, G., McGaugh, J. L., & Cuomo, V. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0900835106 · Cited by 294 · see citing works
Plastic modifications induced by object recognition memory processing
Clarke, J. R., Cammarota, M., Gruart, A., Izquierdo, I., & Delgado-García, J. M. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0915059107 · Cited by 273 · see citing works
Martín-Moreno, A. M., Brera, B., Spuch, C., Carro, E., García‐García, L., Delgado, M., Pozo, M. A., Innamorato, N. G., Cuadrado, A., & CEBALLOS, M. L. D. (2012) · Journal of Neuroinflammation · doi:10.1186/1742-2094-9-8 · Cited by 246 · see citing works
Endocannabinoid system and mood disorders: Priming a target for new therapies
Micale, V., Marzo, V. D., Šulcová, A., Wotjak, C. T., & Drago, F. (2012) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2012.12.002 · Cited by 222 · see citing works
Cannabinoid Control of Learning and Memory through HCN Channels
Maroso, M., Szabo, G. G., Kim, H. K., Alexander, A., Bui, A. D., Lee, S.-H., Lutz, B., & Soltész, I. (2016) · Neuron · doi:10.1016/j.neuron.2016.01.023 · Cited by 186 · see citing works
Chao, O. Y., de Souza Silva, M. A., Yang, Y.-M., & Huston, J. P. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.04.007 · Cited by 158 · see citing works
The endocannabinoid system: An emotional buffer in the modulation of memory function
Morena, M., & Campolongo, P. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.12.010 · Cited by 143 · see citing works
Roles of the Endocannabinoid System in Learning and Memory
Marsicano, G., & Lafenêtre, P. (2009) · Current topics in behavioral neurosciences · doi:10.1007/978-3-540-88955-7_8 · Cited by 140 · see citing works
Basavarajappa, B. S., Nagre, N. N., Xie, S., & Subbanna, S. (2014) · Hippocampus · doi:10.1002/hipo.22272 · Cited by 109 · see citing works
Lyon, L., Saksida, L. M., & Bussey, T. J. (2011) · Psychopharmacology · doi:10.1007/s00213-011-2536-5 · Cited by 105 · see citing works
Kruk-Słomka, M., Dzik, A., Budzyńska, B., & Biała, G. (2016) · Molecular Neurobiology · doi:10.1007/s12035-016-0313-5 · Cited by 107 · see citing works
Potential and Limits of Cannabinoids in Alzheimer’s Disease Therapy
Abate, G., Uberti, D. L., & Tambaro, S. (2021) · Biology · doi:10.3390/biology10060542 · Cited by 101 · see citing works
Stern, C. A. J., da Silva, T. R., Raymundi, A. M., de Souza, C. P., Sato, V., Kato, L., Guimarães, F. S., Andreatini, R., Takahashi, R. N., & Bertoglio, L. J. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.07.024 · Cited by 96 · see citing works
Brown, M. W., Barker, G. R. I., Aggleton, J. P., & Warburton, E. C. (2012) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2012.07.034 · Cited by 84 · see citing works
Brain CB2 Receptors: Implications for Neuropsychiatric Disorders
Roche, M., & Finn, D. P. (2010) · Pharmaceuticals · doi:10.3390/ph3082517 · Cited by 87 · see citing works
Kuhnert, S., Meyer, C., & Koch, M. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.05.002 · Cited by 67 · see citing works
Campolongo, P., Morena, M., Scaccianoce, S., Trezza, V., Chiarotti, F., Schelling, G., Cuomo, V., & Roozendaal, B. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.26 · Cited by 68 · see citing works
Neurodevelopmental impairment following neonatal hyperoxia in the mouse
Ramani, M., van Groen, T., Kadish, I., Bulger, A., & Ambalavanan, N. (2012) · Neurobiology of Disease · doi:10.1016/j.nbd.2012.10.005 · Cited by 62 · see citing works
Sy, H., Wu, S., Wang, W., Chen, C.-H., Huang, Y.-T., Liou, Y., Chiou, C., Pawlak, C. R., & Ho, Y. (2010) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2009.12.020 · Cited by 61 · see citing works
Azami, N., Piri, M., Oryan, S., Jahanshahi, M., Babapour, V., & Zarrindast, M. (2010) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2010.01.003 · Cited by 61 · see citing works
Aso, E., Fernández‐Dueñas, V., López‐Cano, M., Taura, J. J., Watanabe, M., Ferrer, I., Luján, R., & Ciruela, F. (2019) · Molecular Neurobiology · doi:10.1007/s12035-018-1456-3 · Cited by 57 · see citing works
The Endocannabinoid System and Anxiety
Lisboa, S. F. D. S., Gomes, F. V., Terzian, A. L. B., de Aguiar, D. C., Moreira, F. A., Resstel, L. B. M., & Guimarães, F. S. (2016) · Vitamins and hormones · doi:10.1016/bs.vh.2016.09.006 · Cited by 56 · see citing works
MPTP lesion causes neuroinflammation and deficits in object recognition in Wistar rats.
Wang, W., Wu, S., Liou, Y., Wang, A., Pawlak, C. R., & Ho, Y. (2009) · Behavioral Neuroscience · doi:10.1037/a0017401 · Cited by 54 · see citing works
Harte, L. C., & Dow-Edwards, D. (2010) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2010.05.001 · Cited by 51 · see citing works
López-Rodríguez, A. B., Llorente‐Berzal, A., García‐Segura, L. M., & Viveros, M. (2013) · British Journal of Pharmacology · doi:10.1111/bph.12519 · Cited by 52 · see citing works
Lima, R. H., Rossato, J. I., Furini, C. R., Bevilaqua, L. R., Izquierdo, I., & Cammarota, M. (2009) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.12.009 · Cited by 49 · see citing works
Yu, L., Wang, X., Zhao, M., Liu, Y., Li, Y., Li, F.-Q., Wang, X., Xue, Y.-X., & Lü, L. (2009) · Psychopharmacology · doi:10.1007/s00213-008-1450-y · Cited by 48 · see citing works
McReynolds, J. R., Anderson, K. M., Donowho, K. M., & McIntyre, C. K. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.08.016 · Cited by 46 · see citing works
Campolongo, P., Ratano, P., Manduca, A., Scattoni, M. L., Palmery, M., Trezza, V., & Cuomo, V. (2012) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2012.00011 · Cited by 48 · see citing works
Nasehi, M. M., Piri, M., Jamali-Raeufy, N., & Zarrindast, M. (2010) · Physiology & Behavior · doi:10.1016/j.physbeh.2010.02.025 · Cited by 44 · see citing works
Inhibition and enhancement of contextual fear memory destabilization
Lee, J. L. C., & Flavell, C. R. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00144 · Cited by 42 · see citing works
Mouro, F. M., Batalha, V. L., Ferreira, D. G., Coelho, J. E., Baqi, Y., Müller, C. E., Lopes, L. V., Ribeiro, J. A., & Sebastião, A. M. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.02.021 · Cited by 43 · see citing works
Ratano, P., Palmery, M., Trezza, V., & Campolongo, P. (2017) · Frontiers in Pharmacology · doi:10.3389/fphar.2017.00200 · Cited by 41 · see citing works
Segev, A., & Akirav, I. (2011) · Learning & Memory · doi:10.1101/lm.2110511 · Cited by 41 · see citing works
Mouro, F. M., Ribeiro, J. A., Sebastião, A. M., & Dawson, N. (2018) · Journal of Neurochemistry · doi:10.1111/jnc.14549 · Cited by 39 · see citing works
Raymundi, A. M., da Silva, T. R., Zampronio, A. R., Guimarães, F. S., Bertoglio, L. J., & Stern, C. A. J. (2019) · British Journal of Pharmacology · doi:10.1111/bph.14895 · Cited by 39 · see citing works
Burokas, A., Martín‐García, E., Cuesta, J., Rojas, S., Herance, J. R., Gispert, J. D., Serra, M., & Maldonado, R. J. (2014) · Journal of Neurochemistry · doi:10.1111/jnc.12716 · Cited by 38 · see citing works
Kruk-Słomka, M., & Biała, G. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.12.023 · Cited by 37 · see citing works
Kruk-Słomka, M., Boguszewska‐Czubara, A., Słomka, T., Budzyńska, B., & Biała, G. (2015) · Neural Plasticity · doi:10.1155/2016/9815092 · Cited by 37 · see citing works
Cross state-dependency of learning between WIN55, 212-2 and scopolamine in rat dorsal hippocampus
Jamali-Raeufy, N., Nasehi, M., Ebrahimi-Ghiri, M., & Zarrindast, M. (2011) · Neuroscience Letters · doi:10.1016/j.neulet.2011.01.056 · Cited by 35 · see citing works
Zarrindast, M., Dorrani, M., Lachinani, R., & Rezayof, A. (2010) · Neuroscience Research · doi:10.1016/j.neures.2010.02.001 · Cited by 34 · see citing works
Postsynaptic integrative properties of dorsal CA1 pyramidal neuron subpopulations
Masurkar, A. V., Tian, C., Warren, R., Reyes, I., Lowes, D. C., Brann, D. H., & Siegelbaum, S. A. (2020) · Journal of Neurophysiology · doi:10.1152/jn.00397.2019 · Cited by 34 · see citing works
Pennucci, R., Talpo, F., Astro, V., Montinaro, V., Morè, L., Cursi, M., Castoldi, V., Chiaretti, S., Bianchi, V., Marenna, S., et al. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhv274 · Cited by 32 · see citing works
Mouro, F. M., Köfalvi, A., André, L., Baqi, Y., Müller, C. E., Ribeiro, J. A., & Sebastião, A. M. (2019) · Neuropharmacology · doi:10.1016/j.neuropharm.2019.05.003 · Cited by 31 · see citing works
Navia‐Paldanius, D., Aaltonen, N., Lehtonen, M., Savinainen, J. R., Taschler, U., Radner, F. P. W., Zimmermann, R., & Laitinen, J. T. (2015) · European Journal of Pharmaceutical Sciences · doi:10.1016/j.ejps.2015.06.005 · Cited by 30 · see citing works
Niloy, N., Hediyal, T. A., Vichitra, C., Sharma, S., Chidambaram, S. B., Gorantla, V. R., & Mahalakshmi, A. M. (2023) · Biomolecules · doi:10.3390/biom13010162 · Cited by 28 · see citing works
Galanopoulos, A., Polissidis, A., Γεωργιάδου, Γ., Papadopoulou‐Daifoti, Z., Nomikos, G. G., Pitsikas, N., & Antoniou, K. (2014) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2014.05.014 · Cited by 28 · see citing works
Moshfegh, A., Babaei, P., Oryan, S., Tehrani, B. S., & Zarrindast, M. (2010) · Neuroscience Letters · doi:10.1016/j.neulet.2010.07.079 · Cited by 27 · see citing works
Ballard, M. E., Gallo, D. A., & de Wit, H. (2013) · Psychopharmacology · doi:10.1007/s00213-012-2924-5 · Cited by 32 · see citing works
Chronic pain in Alzheimer's disease: Endocannabinoid system
Blanton, H. L., Reddy, P. H., & Benamar, K. (2022) · Experimental Neurology · doi:10.1016/j.expneurol.2022.114287 · Cited by 26 · see citing works
Zenko, M., Zhu, Y.-Y., Dremencov, E., Ren, W., Xu, L., & Zhang, X. (2011) · Journal of Neuroscience Research · doi:10.1002/jnr.22580 · Cited by 25 · see citing works
Novel object recognition memory in REM sleep-deprived rats: Role of the cannabinoid CB1 receptor
Shahveisi, K., Farnia, V., Khazaie, H., Ghazvini, H., Nozari, M., & Khodamoradi, M. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.112311 · Cited by 24 · see citing works
Murillo‐Rodríguez, E., Palomero‐Rivero, M., Millán‐Aldaco, D., & Marzo, V. D. (2012) · Physiology & Behavior · doi:10.1016/j.physbeh.2012.11.007 · Cited by 23 · see citing works
Tanqueiro, S. R., Mouro, F. M., Ferreira, C. B., Freitas, C. F., Fonseca‐Gomes, J., do Couto, F. S., Sebastião, A. M., Dawson, N., & Diógenes, M. J. (2021) · Journal of Psychopharmacology · doi:10.1177/02698811211008560 · Cited by 22 · see citing works
Modulation of food consumption and sleep–wake cycle in mice by the neutral CB1 antagonist ABD459
Goonawardena, A. V., Plano, A., Robinson, L., Ross, R. A., Greig, I. R., Pertwee, R. G., Hampson, R. E., Platt, B., & Riedel, G. (2014) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000108 · Cited by 22 · see citing works
Behavioral Neurobiology of the Endocannabinoid System
Kendall, D., & Alexander, S. (2009) · Current topics in behavioral neurosciences · doi:10.1007/978-3-540-88955-7 · Cited by 22 · see citing works
Endocannabinoid regulation of hippocampus-dependent memory
Figueiredo, A. M. P. D., & Cheer, J. F. (2023) · Experimental Neurology · doi:10.1016/j.expneurol.2023.114384 · Cited by 20 · see citing works
Rasekhi, K., Oryan, S., Nasehi, M., & Zarrindast, M. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.04.006 · Cited by 20 · see citing works
Khodamoradi, M., Tirgar, F., Ghazvini, H., Rafaiee, R., Tamijani, S. M. S., Karimi, N., Yadegari, A., Siahposht-Khachaki, A., & Akhtari, J. (2022) · Neuroscience Letters · doi:10.1016/j.neulet.2022.136634 · Cited by 20 · see citing works
Alijanpour, S., & Rezayof, A. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.04.030 · Cited by 21 · see citing works
Stanciu, G. D., Ababei, D. C., Solcan, C., Bild, V., Ciobîcă, A., Chiriac, S. I. B., Ciobanu, L., & Tamba, B.-I. (2023) · Pharmaceuticals · doi:10.3390/ph16111620 · Cited by 20 · see citing works
Neurocognitive effects of cannabis: Lessons learned from human experimental studies
Colizzi, M., & Bhattacharyya, S. (2018) · Progress in brain research · doi:10.1016/bs.pbr.2018.08.010 · Cited by 18 · see citing works
Rezayof, A., Habibi, P., & Zarrindast, M. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2010.12.006 · Cited by 20 · see citing works
Interplay between serotonin and cannabinoid function in the amygdala in fear conditioning
Nasehi, M., Davoudi, K., Ebrahimi-Ghiri, M., & Zarrindast, M. (2016) · Brain Research · doi:10.1016/j.brainres.2016.01.034 · Cited by 17 · see citing works
Yadav-Samudrala, B. J., Gorman, B. L., Dodson, H., Ramineni, S., Wallace, E. D., Peace, M. R., Poklis, J. L., Jiang, W., & Fitting, S. (2023) · Brain Research · doi:10.1016/j.brainres.2023.148638 · Cited by 15 · see citing works
Piri, M., & Zarrindast, M. (2011) · PubMed · Cited by 15 · see citing works
Marion, M., Hamilton, J., Richardson, B., Roeder, N. M., Figueiredo, A. M. P. D., Nubelo, A., Hetelekides, E. M., Penman, S. L., Owada, Y., Kagawa, Y., et al. (2022) · Behavioural Brain Research · doi:10.1016/j.bbr.2022.113814 · Cited by 14 · see citing works
Guzman, A. S., Avalos, M. P., Giovanni, L. N. D., Euliarte, P. V., Sanchez, M. A., Mongi‐Bragato, B., Rigoni, D., Bollati, F. A., Virgolini, M. B., & Cancela, L. M. (2021) · Scientific Reports · doi:10.1038/s41598-021-92389-4 · Cited by 13 · see citing works
Schurman, L. D., Sticht, M. A., Mitchnick, K. A., Limebeer, C. L., Parker, L. A., & Winters, B. D. (2014) · Neuroscience Letters · doi:10.1016/j.neulet.2014.06.056 · Cited by 11 · see citing works
Is there sufficient evidence that cannabis use is a risk factor for psychosis?
Colizzi, M., & Bhattacharyya, S. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-813201-2.00016-8 · Cited by 11 · see citing works
Jafari‐Sabet, M., & Karimi, A.-M. (2017) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2017.10.005 · Cited by 8 · see citing works
On the effect of hippocampal c-Jun N-terminal kinase inhibition on object recognition memory
Rossato, J. I., Radiske, A., González, M. C., Bevilaqua, L. R., & Cammarota, M. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.1052124 · Cited by 6 · see citing works
Aliczki, M., & Haller, J. (2015) · Springer eBooks · doi:10.1007/978-1-4939-2294-9_4 · Cited by 5 · see citing works
Ren, Y., Xu, Y.-J., & Tan, Z.-M. (2011) · Medical Hypotheses · doi:10.1016/j.mehy.2011.04.022 · Cited by 3 · see citing works
Gold, P. E. (2022) · Neuroscience · doi:10.1016/j.neuroscience.2022.05.037 · Cited by 3 · see citing works
Acute Glucocorticoids Interact with Arousal State in Regulating Long‐term Memory Formation
Campolongo, P., & Roozendaal, B. (2011) · doi:10.1002/9781118083222.ch9 · Cited by 2 · see citing works
Obesogenic diet impairs memory consolidation via the hippocampal endocannabinoid system
Ducourneau, E., Janthakhin, Y., da Cruz, J. F. O., Artinian, J., Alfos, S., Helbling, J., Matias, I., Bakoyiannis, I., N’diaye, M., Bosch‐Bouju, C., et al. (2025) · Current Biology · doi:10.1016/j.cub.2025.10.049 · Cited by 2 · see citing works
Rasekhi, K., Oryan, S., Nasehi, M., & Zarrindast, M. (2015) · Nova Biologica Reperta · doi:10.21859/acadpub.nbr.2.2.113 · Cited by 1 · see citing works
Protective Effects of Cannabis in Neuroinflammation-Mediated Alzheimer's Disease
Kashif, M., Waseem, M., Vijendra, P. D., & Pandurangan, A. K. (2023) · Advances in medical diagnosis, treatment, and care (AMDTC) book series · doi:10.4018/978-1-6684-5652-1.ch002 · Cited by 2 · see citing works
(Endo)Cannabinoids and Cognitive Functions in Animals: Healthy and Pathological BrainPreprint
Kitchigina, V. F. (2023) · Preprints.org · doi:10.20944/preprints202304.0224.v1
Assini, F. L. (2011) · LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas)
Cross state-dependency of learning between morphine and WIN55, 212-2 in mouse dorsal hippocampus
(2014) · International Journal of Biosciences (IJB) · doi:10.12692/ijb/5.3.140-152
Endocannabinoid Function in Hippocampal Synaptic Plasticity and Spatial Working Memory
Blaskovits, F. (2013) · uO Research (University of Ottawa) · doi:10.20381/ruor-3206
Kamino, D. (2012) · uO Research (University of Ottawa) · doi:10.20381/ruor-5930
Long-Term Outcomes Resulting from Exposure to Stress and Fluoxetine During Development
Kiryanova, V. (2017) · Libraries and Cultural Resources (University of Calgary) · doi:10.11575/prism/26786
Milewski, T., & Orr, P. T. (2018) · Behavioral Neuroscience · doi:10.1037/bne0000262
Changes in the Endocannabinoid system in the Brain Following Bilateral Vestibular Damage
Baek, J. (2011) · Otago University Research Archive (University of Otago)
Mohammadkhani, M., Jarah, M., Gholami, D., Riazi, G. H., & Mirabzadeh, Y. (2022) · Research Square · doi:10.21203/rs.3.rs-1759887/v1
Raymundi, A. M., & Stern, C. A. J. (2023) · Elsevier eBooks · doi:10.1016/b978-0-323-90877-1.00037-1
Mohammadkhani, M., Jarah, M., Gholami, D., Riazi, G., & Rezazadeh, H. (2025) · BMC Neuroscience · doi:10.1186/s12868-025-00957-5
Holliday, E. D., Chowdhury, K. U., Chen, K., Saleem, B., Yenduri, A., & Suppiramaniam, V. D. (2025) · Psychoactives · doi:10.3390/psychoactives4030029
The endocannabinoid system in intellectual disability
Vázquez-Oliver, A., Reyes‐Ramírez, L. D. L., Galera-López, L., & Ozaita, A. (2025) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-443-13908-6.00022-0
Upstream CB1R Regulation of β‐Adrenergic Memory Consolidation
Rossato, J. I., Ribeiro, L., Lima‐Silva, T., Araújo, R. B. D. A., Orvate, R., Azevedo, A. L., Cammarota, N. B., Baracho, A. L., Carneiro, L. M., & Cammarota, M. (2026) · Hippocampus · doi:10.1002/hipo.70084
- Authors
- Clarke, J. R., Rossato, J. I., Monteiro, S., Bevilaqua, L. R. M., Izquierdo, I., & Cammarota, M.
- Affiliations
- Pontifícia Universidade Católica do Rio Grande do Sul (BR)
- Centro Universitário Metodista IPA (BR)
- Venue
- Neurobiology of Learning and Memory
- Publisher
- Elsevier BV
- Published
- 2008-09
- Volume
- 90
- Issue
- 2
- Pages
- 374-381
- ISSN
- 1074-7427 (ISSN-L)
- OpenAlex
- W2087674179
- Cited by
- 97
- References
- 76
- Citations by year
- 2026: 1 · 2025: 4 · 2023: 7 · 2022: 6 · 2021: 3 · 2020: 3 · 2019: 4 · 2018: 3 · 2017: 5 · 2016: 4 · 2015: 6 · 2014: 12 · 2013: 5 · 2012: 9
- FWCI
- 5.85
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- Locations
- Neurobiology of Learning and Memory (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Universidade Federal do Rio Grande do Sul
- Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
- Conselho Nacional de Desenvolvimento Científico e Tecnológico
- Topics
- Health Sciences › Medicine › Pharmacology › Cannabis and Cannabinoid Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Keywords
- CB1 receptor, CB2 receptor, object recognition memory, long-term memory consolidation, dorsal hippocampus, CA1 region, WIN 55,212-2, AM251, ACEA, JWH-015, palmitoylethanolamide, endocannabinoids, memory impairment
- MeSH terms
- Animals, Arachidonic Acids, Avoidance Learning, Dominance, Cerebral, Dose-Response Relationship, Drug, Electroshock, Escape Reaction, Exploratory Behavior, Fear, Hippocampus, Male, Memory, Short-Term, Morpholines, Motor Activity, Naphthalenes, Pattern Recognition, Visual, Retention, Psychology, Rats, Wistar, Maze Learning, Receptor, Cannabinoid, CB1, Benzoxazines, Rats
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