Endocannabinoid system and stress and anxiety responses
Abstract
Cannabinoid agonists induce complex and often contradictory effects on anxiety in humans and experimental animals. The data from animal tests provide evidence of dose-dependent bidirectional modulation of anxiety by the cannabinoid system and the importance of environmental context. The mechanisms mediating the effects of cannabinoids on anxiety-related responses appear to involve CB1 and non-CB1 cannabinoid receptors. In addition, the CRH, GABA(A), cholecystokinin, opioid and serotonergic systems have also been implicated. Brain regions such as the amygdala, hippocampus and cortex, directly involved in the regulation of emotional behavior, contain high densities of CB1 receptors. Mutant mice lacking CB1 receptors show anxiogenic-like and depressive-like phenotypes in several tests, as well as profound alterations in their adrenocortical activity. Pharmacological blockade of CB1 receptors induces anxiety in rats, and inhibition of anandamide metabolism produces anxiolytic-like effects. Thus, the endocannabinoid system appears to play a pivotal role in the regulation of emotional states and may constitute a novel pharmacological target for anti-anxiety therapy.
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?
Low doses of CB1 agonists tend to be anxiolytic and high doses tend to increase aversion and anxiety-related behaviors.
“Given that low doses of CB1 agonists tend to be anxiolytic and high doses tend to increase aversion and anxiety-related behaviors (Ganon-Elazar and Akirav, 2012; also reviewed in Viveros et al., 2005)”
From Sleep restriction alters plasma endocannabinoids concentrations before but not after exercise in humans (2016) · cites this paper as Viveros et al., 2005
The cannabinoid system is part of the complex circuitry that regulates anxiety and stress and is a crucial mediator of emotional learning.
“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 Viveros et al, 2005
Cites
International Union of Pharmacology: Approaches to the Nomenclature of Voltage-Gated Ion Channels
Catterall, W. A., Chandy, K. G., Clapham, D. E., Gutman, G. A., Hofmann, F., Harmar, A. J., Abernethy, D. R., & Spedding, M. (2003) · Pharmacological Reviews · doi:10.1124/pr.55.4.5 · Cited by 7,126 · see citing works
Ledent, C. A., Valverde, O., Cossu, G., Petitet, F., Aubert, J.-F., Beslot, F., Böhme, G. A., Impérato, A., Pedrazzini, T., Roques, B. P., et al. (1999) · Science · doi:10.1126/science.283.5400.401 · Cited by 3,612 · see citing works
A review of central 5-HT receptors and their function
Barnes, N. M., & Sharp, T. (1999) · Neuropharmacology · doi:10.1016/s0028-3908(99)00010-6 · Cited by 3,150 · see citing works
International Union of Pharmacology. XXVII. Classification of Cannabinoid Receptors
Howlett, A. C., Barth, F., Bonner, T. I., Cabral, G., Casellas, P., Devane, W. A., Felder, C. C., Herkenham, M., Mackie, K., Martin, B. R., et al. (2002) · Pharmacological Reviews · doi:10.1124/pr.54.2.161 · Cited by 2,819 · 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
Herkenham, M., Lynn, A., Johnson, M., Melvin, L., de Costa, B., & Rice, K. (1991) · The Journal of Neuroscience · doi:10.1523/jneurosci.11-02-00563.1991 · Cited by 2,159 · 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
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
Increased mortality, hypoactivity, and hypoalgesia in cannabinoid CB1 receptor knockout mice
Zimmer, A., Zimmer, A. M., Hohmann, A. G., Herkenham, M. A., & Bonner, T. I. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.10.5780 · Cited by 1,065 · see citing works
Glass, M., Faull, R. L. M., & Dragunow, M. (1997) · Neuroscience · doi:10.1016/s0306-4522(96)00428-9 · Cited by 1,052 · see citing works
Cannabis use and mental health in young people: cohort study.
Patton, G. C., Coffey, C., Carlin, J. B., Degenhardt, L., Lynskey, M., & Hall, W. (2002) · BMJ · doi:10.1136/bmj.325.7374.1195 · Cited by 997 · see citing works
The neurobiology and control of anxious states
Millan, M. J. (2003) · Progress in Neurobiology · doi:10.1016/s0301-0082(03)00087-x · Cited by 963 · see citing works
Marsicano, G., & Lutz, B. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00847.x · Cited by 937 · see citing works
Pharmacology and effects of cannabis: A brief review
Ashton, C. (2001) · British Journal of Psychiatry · doi:10.1192/bjp.178.2.101 · Cited by 868 · see citing works
Di, S., Malcher‐Lopes, R., Halmos, K. C., & Tasker, J. G. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-12-04850.2003 · Cited by 801 · see citing works
Hall, W., & Solowij, N. (1998) · The Lancet · doi:10.1016/s0140-6736(98)05021-1 · Cited by 778 · see citing works
Galve‐Roperh, I., Sánchez, C., Cortés, M. L., del Pulgar, T. G., Izquierdo, M., & Guzmán, M. (2000) · Nature Medicine · doi:10.1038/73171 · Cited by 684 · see citing works
Katona, I., Rancz, E. A., Acsády, L., Ledent, C., Mackie, K., Hájos, N., & Freund, T. F. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-23-09506.2001 · Cited by 668 · see citing works
Action of cannabidiol on the anxiety and other effects produced by ?9-THC in normal subjects
Zuardi, A. W., Shirakawa, I., Finkelfarb, E., & Karniol, I. G. (1982) · Psychopharmacology · doi:10.1007/bf00432554 · Cited by 608 · see citing works
Járai, Z., Wagner, J. A., Varga, K., Lake, K. D., Compton, D. M., Martin, B. R., Zimmer, A. M., Bonner, T. I., Buckley, N. E., Mezey, É., et al. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.24.14136 · Cited by 598 · see citing works
Arnone, M., Maruani, J., Chaperon, F., Thiébot, M.-H., Poncelet, M., Soubrié, P., & Fur, G. L. (1997) · Psychopharmacology · doi:10.1007/s002130050326 · Cited by 593 · see citing works
Evidence for a New G Protein-Coupled Cannabinoid Receptor in Mouse Brain
Breivogel, C. S., Griffin, G., Marzo, V. D., & Martin, B. R. (2001) · Molecular Pharmacology · doi:10.1124/mol.60.1.155 · Cited by 537 · 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
Hollister, L. E. (1987) · Journal of Ethnopharmacology · doi:10.1016/0378-8741(87)90030-4 · Cited by 500 · see citing works
Griebel, G. (1995) · Pharmacology & Therapeutics · doi:10.1016/0163-7258(95)98597-j · Cited by 487 · see citing works
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 · see citing works
Müller, M. B., Zimmermann, S., Sillaber, I., Hagemeyer, T. P., Deussing, J. M., Timpl, P., Kormann, M., Droste, S. K., Kühn, R., Reul, J. M. H. M., et al. (2003) · Nature Neuroscience · doi:10.1038/nn1123 · Cited by 446 · see citing works
Hájos, N., Ledent, C. A., & Freund, T. F. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00287-1 · Cited by 420 · see citing works
Cohen, C., Perrault, G., Voltz, C., Steinberg, R., & Soubrié, P. (2002) · Behavioural Pharmacology · doi:10.1097/00008877-200209000-00018 · Cited by 396 · see citing works
Pharmacological and biochemical interactions between opioids and cannabinoids
Manzanares, J., Corchero, J., Romero, J., Fernández‐Ruíz, J., Ramos, J. A., & Fuentes, J. (1999) · Trends in Pharmacological Sciences · doi:10.1016/s0165-6147(99)01339-5 · Cited by 391 · see citing works
Marzo, V. D., Breivogel, C. S., Tao, Q., Bridgen, D. T., Razdan, R. K., Zimmer, A. M., Zimmer, A., & Martin, B. R. (2000) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2000.0752434.x · Cited by 389 · see citing works
Antianxiety effect of cannabidiol in the elevated plus-maze
Guimarães, F. S., Chiaretti, T. M., Graeff, F. G., & Zuardi, A. W. (1990) · Psychopharmacology · doi:10.1007/bf02244012 · Cited by 379 · see citing works
Experimental Approaches to Anxiety and Depression
Elliott, J. M., Heal, D. J., & Mardens, C. A. (1993) · Behavioural Pharmacology · doi:10.1097/00008877-199310000-00012 · Cited by 363 · see citing works
The effects of genetic and pharmacological blockade of the CB1 cannabinoid receptor on anxiety
Haller, J., Bakos, N., Szirmay, M., Ledent, C., & Freund, T. F. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.02192.x · Cited by 354 · see citing works
Ecstasy use in Australia: patterns of use and associated harm
Topp, L., Hando, J., Dillon, P., ROCHE, A. M., & Solowij, N. (1999) · Drug and Alcohol Dependence · doi:10.1016/s0376-8716(99)00002-2 · Cited by 353 · 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
Behavioural and biochemical evidence for interactions between Δ9‐tetrahydrocannabinol and nicotine
Valjent, E., Mitchell, J., Besson, M., Caboche, J., & Maldonado, R. J. (2002) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0704479 · Cited by 321 · see citing works
Pharmacological characterization of cannabinoids in the elevated plus maze.
Onaivi, E. S., Green, M. R., & Martin, B. R. (1990) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)13195-9 · Cited by 312 · see citing works
Behavioral Effects of Cannabinoid Agents in Animals
Chaperon, F., & Thiébot, M.-H. (1999) · Critical Reviews in Neurobiology · doi:10.1615/critrevneurobiol.v13.i3.20 · Cited by 311 · see citing works
Effects of cannabidiol (CBD) on regional cerebral blood flow
Crippa, J. A. D. S., Zuardi, A. W., Garrido, G. E. J., Wichert-Ana, L., Guarnieri, R., Ferrari, L., Azevedo-Marques, P. M., Hallak, J. E. C., McGuire, P. K., & Busatto, G. F. (2004) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300340 · Cited by 307 · see citing works
Navarro, M., Hernández, E., Muñoz, R. M., del Arco, I., Villanúa, M. Á., Carrera, M. R. A., & de Fonseca, F. R. (1997) · Neuroreport · doi:10.1097/00001756-199701200-00023 · Cited by 306 · see citing works
Haller, J., Varga, B., Ledent, C., Barna, I., & Freund, T. F. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03293.x · Cited by 284 · see citing works
Cannabinoids in Clinical Practice
Williamson, E. M., & Evans, F. J. (2000) · Drugs · doi:10.2165/00003495-200060060-00005 · Cited by 283 · see citing works
González, S. R., Cascio, M. G., Fernández‐Ruíz, J., Fezza, F., Marzo, V. D., & Ramos, J. A. (2002) · Brain Research · doi:10.1016/s0006-8993(02)03344-9 · Cited by 278 · see citing works
WINSTOCK, A. R., Griffiths, P., & Stewart, D. (2001) · Drug and Alcohol Dependence · doi:10.1016/s0376-8716(00)00215-5 · Cited by 276 · see citing works
Antitumor Effects of Cannabidiol, a Nonpsychoactive Cannabinoid, on Human Glioma Cell Lines
Massi, P., Vaccani, A., Ceruti, S., Colombo, A., Abbracchio, M. P., & Parolaro, D. (2004) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.103.061002 · Cited by 272 · see citing works
Therapeutic aspects of cannabis and cannabinoids
Robson, P. (2001) · The British Journal of Psychiatry · doi:10.1192/bjp.178.2.107 · Cited by 265 · see citing works
Motivational Effects of Cannabinoids Are Mediated by μ-Opioid and κ-Opioid Receptors
Ghozland, S. G., Matthes, H. W. D., Simonin, F., Filliol, D., Kieffer, B. L., & Maldonado, R. J. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-03-01146.2002 · Cited by 263 · see citing works
Biphasic Effects of Anandamide
Sulcova, E. (1998) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(97)00422-x · Cited by 256 · see citing works
de Kloet, E. R. (2003) · PubMed · Cited by 255 · see citing works
Castañé, A., Valjent, E., Ledent, C. A., Parmentier, M., Maldonado, R. J., & Valverde, O. (2002) · Neuropharmacology · doi:10.1016/s0028-3908(02)00118-1 · Cited by 240 · see citing works
Therapeutic Potential of Cannabinoids in CNS Disease
Croxford, J. L. (2003) · CNS Drugs · doi:10.2165/00023210-200317030-00004 · Cited by 240 · see citing works
Lepore, M., Vorel, S. R., Lowinson, J. H., & Gardner, E. L. (1995) · Life Sciences · doi:10.1016/0024-3205(95)00191-8 · Cited by 237 · see citing works
File, S. E., Gonzalez, L. E., & Andrews, N. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-15-04810.1996 · Cited by 230 · see citing works
Self-citationThe endocannabinoid nervous system
Porter, A. C., & Felder, C. C. (2001) · Pharmacology & Therapeutics · doi:10.1016/s0163-7258(01)00130-9 · Cited by 226 · see citing works
Involvement of the opioid system in the anxiolytic-like effects induced by Δ9-tetrahydrocannabinol
Berrendero, F., & Maldonado, R. J. (2002) · Psychopharmacology · doi:10.1007/s00213-002-1144-9 · Cited by 221 · see citing works
The HPA axis and cocaine reinforcement
Goeders, N. E. (2002) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(01)00034-8 · Cited by 220 · see citing works
Impaired action of anxiolytic drugs in mice deficient in cannabinoid CB1 receptors
Urigüen, L., Pérez-Rial, S., Ledent, C., Palomo, T., & Manzanares, J. (2004) · Neuropharmacology · doi:10.1016/j.neuropharm.2004.01.003 · Cited by 218 · see citing works
A behavioural model to reveal place preference to Δ9-tetrahydrocannabinol in mice
Valjent, E., & Maldonado, R. J. (2000) · Psychopharmacology · doi:10.1007/s002130050013 · Cited by 214 · see citing works
Gonzalez, L. E., Andrews, N., & File, S. E. (1996) · Brain Research · doi:10.1016/0006-8993(96)00517-3 · Cited by 204 · see citing works
Self-citationTargeted gene mutation approaches to the study of anxiety-like behavior in mice
Holmes, A. (2001) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(01)00012-4 · Cited by 198 · see citing works
File, S. E., Mabbutt, P. S., & Hitchcott, P. K. (1990) · Psychopharmacology · doi:10.1007/bf02245751 · Cited by 197 · see citing works
Self-citationRodgers, R. J., Perrault, G., Sanger, D. J., & Griebel, G. (1997) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(96)00402-9 · Cited by 190 · see citing works
The involvement of serotonin in regulation of pituitary-adrenocortical function.
Rw, F. (1992) · PubMed · Cited by 181 · see citing works
Weidenfeld, J., Feldman, S., & Mechoulam, R. (2008) · Neuroendocrinology · doi:10.1159/000126646 · Cited by 179 · see citing works
Cannabinoid effects on anxiety-related behaviours and hypothalamic neurotransmitters
Arévalo, C., de Miguel, R., & Hernández‐Tristán, R. (2001) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(01)00578-0 · Cited by 175 · see citing works
Cannabinoid receptor gene (CNR1): association with IV drug use
Comings, D. E., Muhleman, D. R., Gade, R., Johnson, P., Verde, R., Saucier, G., & MacMurray, J. P. (1997) · Molecular Psychiatry · doi:10.1038/sj.mp.4000247 · Cited by 175 · see citing works
de Fonseca, F. R., Rubio, P., Menzaghi, F., Merlo‐Pich, E., Rivier, J., Koob, G. F., & Navarro, M. A. (1996) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)12276-3 · Cited by 175 · see citing works
Valverde, O., Noble, F., Beslot, F., Daugé, V., Fournié‐Zaluski, M., & Roques, B. P. (2001) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01558.x · Cited by 172 · see citing works
Synergistic interactions of endogenous opioids and cannabinoid systems
Welch, S. P., & Eads, M. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01908-3 · Cited by 169 · see citing works
Aversive effects of the synthetic cannabinoid CP 55,940 in rats
McGregor, I. S., Issakidis, C. N., & Prior, G. (1996) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(95)02066-7 · Cited by 168 · see citing works
A neuroendocrine role in cocaine reinforcement
Goeders, N. E. (1997) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(97)00027-9 · Cited by 168 · see citing works
Manzanares, J., Corchero, J., & Fuentes, J. A. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01756-4 · Cited by 152 · see citing works
Braida, D., Pozzi, M., Cavallini, R., & Sala, M. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00210-x · Cited by 152 · see citing works
Tzavara, E. T., Wade, M. R., & Nomikos, G. G. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-28-09374.2003 · Cited by 151 · 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
Absence of Δ-9-Tetrahydrocannabinol Dysphoric Effects in Dynorphin-Deficient Mice
Zimmer, A., Valjent, E., König, M., Zimmer, A. M., Robledo, P., Hahn, H., Valverde, O., & Maldonado, R. J. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-23-09499.2001 · Cited by 140 · see citing works
The psychobiology of anxiolytic drugs
Sandford, J. J., Argyropoulos, S. V., & Nutt, D. (2000) · Pharmacology & Therapeutics · doi:10.1016/s0163-7258(00)00082-6 · Cited by 137 · see citing works
Marco, E. M., rez-Alvarez, L. P., Borcel, É., Rubio, M., Guaza, C., Ambrosio, E., File, S. E., & Viveros, M. (2004) · Behavioural Pharmacology · doi:10.1097/00008877-200402000-00003 · Cited by 133 · see citing works
Self-citationPistis, M., Perra, S., Pillolla, G., Melis, M., Gessa, G., & Muntoni, A. (2004) · Neuropharmacology · doi:10.1016/j.neuropharm.2003.08.003 · Cited by 124 · see citing works
Mascia, M. S., Obinu, M. C., Ledent, C. A., Parmentier, M., Böhme, G. A., Impérato, A., & Fratta, W. (1999) · European Journal of Pharmacology · doi:10.1016/s0014-2999(99)00656-1 · Cited by 123 · see citing works
Distinct cannabinoid sensitive receptors regulate hippocampal excitation and inhibition
Hájos, N., & Freund, T. F. (2002) · Chemistry and Physics of Lipids · doi:10.1016/s0009-3084(02)00149-4 · Cited by 122 · see citing works
Rotzinger, S., & Vaccarino, F. J. (2003) · Journal of Psychiatry and Neuroscience · doi:10.1139/jpn.0322 · Cited by 120 · see citing works
Hill, M. N., & Gorzalka, B. B. (2004) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2004.06.069 · Cited by 114 · see citing works
Valverde, O., Ledent, C. A., Beslot, F., Parmentier, M., & Roques, B. P. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.00929.x · Cited by 111 · see citing works
Cannabis use and anxiety in daily life: a naturalistic investigation in a non-clinical population
Tournier, M., Sorbara, F., Gindre, C., Swendsen, J. D., & Verdoux, H. (2003) · Psychiatry Research · doi:10.1016/s0165-1781(03)00052-0 · Cited by 107 · see citing works
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 102 · see citing works
Polydrug use at raves by a Western Australian sample
Boys, A., Lenton, S. R., & Norcross, K. (1997) · Drug and Alcohol Review · doi:10.1080/09595239800187411 · Cited by 97 · see citing works
Genn, R. F., Tucci, S. A., Marco, E. M., Viveros, M., & File, S. E. (2004) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2003.12.019 · Cited by 92 · see citing works
Self-citationVicentic, A., Li, Q., Battaglia, G., & de Kar, L. D. V. (1998) · European Journal of Pharmacology · doi:10.1016/s0014-2999(97)01607-5 · Cited by 89 · see citing works
Anxiolytic effect of cannabidiol derivatives in the elevated plus-maze
Guimarães, F. S., Aguiar, J. C. D., Mechoulam, R., & Breuer, A. (1994) · General Pharmacology The Vascular System · doi:10.1016/0306-3623(94)90027-2 · Cited by 89 · see citing works
Rodgers, R. J., Haller, J., Halász, J., & Mikics, É. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02548.x · Cited by 88 · see citing works
Cheeta, S., Kenny, P. J., & File, S. E. (2000) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/s0278-5846(00)00129-9 · Cited by 88 · see citing works
Self-citationCannabinoid modulation of rat pup ultrasonic vocalizations
McGregor, I. S., Dastur, F. N., McLellan, R. A., & Brown, R. E. (1996) · European Journal of Pharmacology · doi:10.1016/0014-2999(96)00511-0 · Cited by 88 · see citing works
Beinfeld, M. C., & Connolly, K. (2001) · Neuroscience Letters · doi:10.1016/s0304-3940(01)01591-9 · Cited by 86 · see citing works
Wenger, T., Jamali, K. A., Juanéda, C., Léonardelli, J., & Tramu, G. (1997) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1997.7222 · Cited by 85 · see citing works
Cheeta, S. (2001) · Neuropsychopharmacology · doi:10.1016/s0893-133x(01)00258-5 · Cited by 84 · see citing works
Griebel, G., Rodgers, R. J., Perrault, G., et al. (2000) · Neuropharmacology · doi:10.1016/s0028-3908(00)00074-5 · Cited by 82 · see citing works
Antinociceptive, behavioural and neuroendocrine effects of CP 55,940 in young rats
Romero, E., Martín‐Fernández, B., Sagredo, O., Gomez, N., Urigüen, L., Guaza, C., de Miguel, R., Ramos, J. A., & Viveros, M. (2002) · Developmental Brain Research · doi:10.1016/s0165-3806(02)00306-1 · Cited by 81 · see citing works
Self-citationPugh, G., Mason, D. J., Combs, V., & Welch, S. P. (1997) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)36640-6 · Cited by 81 · see citing works
File, S. E., Fluck, E., & Leahy, A. (2001) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145701002577 · Cited by 81 · see citing works
Self-citationInvolvement of the κ-opioid receptor in the anxiogenic-like effect of CP 55,940 in male rats
Marı́n, S., Marco, E. M., Biscaia, M., Fernández, B., Rubio, M., Guaza, C., Schmidhammer, H., & Viveros, M. (2003) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(02)01041-9 · Cited by 78 · see citing works
Self-citationArnold, J. C., Topple, A. N., Mallet, P. E., Hunt, G. E., & McGregor, I. S. (2001) · Brain Research · doi:10.1016/s0006-8993(01)03127-4 · Cited by 77 · see citing works
Gonzalez, L. E., Ouagazzal, A., & File, S. E. (1998) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1998.00375.x · Cited by 75 · see citing works
Self-citationMartı́n-Calderón, J. L., Muñoz, R. M., Villanúa, M. Á., del Arco, I., Moreno, J. L., de Fonseca, F. R., & Navarro, M. A. (1998) · European Journal of Pharmacology · doi:10.1016/s0014-2999(97)01560-4 · Cited by 74 · see citing works
Houser, S. J., Eads, M., Embrey, J. P., & Welch, S. P. (2000) · Brain Research · doi:10.1016/s0006-8993(00)01981-8 · Cited by 73 · see citing works
DeVries, A. C., & Pert, A. (1998) · Psychopharmacology · doi:10.1007/s002130050627 · Cited by 71 · see citing works
THE CANNABINOID AGONIST HU 210 MODIFIES RAT BEHAVIOURAL RESPONSES TO NOVELTY AND STRESS
Giuliani, D., FERRARI, F., & Ottani, A. (2000) · Pharmacological Research · doi:10.1006/phrs.1999.0560 · Cited by 67 · see citing works
Comorbid cannabis use and panic disorder: short term and long term follow‐up study
Dannon, P. N., Lowengrub, K., Amiaz, R., Grunhaus, L. J., & Kotler, M. (2004) · Human Psychopharmacology Clinical and Experimental · doi:10.1002/hup.560 · Cited by 66 · see citing works
Sante, A. B., Nobre, M. J., & Brandão, M. L. (2000) · Behavioural Pharmacology · doi:10.1097/00008877-200011000-00005 · Cited by 60 · see citing works
Morley, K. C., Li, K. M., Hunt, G. E., Mallet, P. E., & McGregor, I. S. (2004) · Neuropharmacology · doi:10.1016/j.neuropharm.2004.01.002 · Cited by 59 · see citing works
ARE ANANDAMIDE AND CANNABINOID RECEPTORS INVOLVED IN ETHANOL TOLERANCE? A REVIEW OF THE EVIDENCE
Hungund, B. L. (2000) · Alcohol and Alcoholism · doi:10.1093/alcalc/35.2.126 · Cited by 58 · see citing works
The endocannabinoid system: function in survival of the embryo, the newborn and the neuron
Fride, E., & Shohami, E. (2002) · Neuroreport · doi:10.1097/00001756-200210280-00001 · Cited by 44 · see citing works
Role of Cannabinoid Receptor in the Brain as It Relates to Drug Reward
Yamamoto, T., & Takada, K. (2000) · The Japanese Journal of Pharmacology · doi:10.1254/jjp.84.229 · Cited by 41 · see citing works
Malone, D. T., & TAYLOR, D. A. H. B. (2001) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(01)00567-6 · Cited by 38 · see citing works
Tucci, S., Cheeta, S., Seth, P., & File, S. E. (2003) · Psychopharmacology · doi:10.1007/s00213-003-1403-4 · Cited by 38 · see citing works
Self-citationNobre, M. J., Santos, N. R., Aguiar, M. S., & Brandão, M. L. (2000) · European Journal of Pharmacology · doi:10.1016/s0014-2999(00)00589-6 · Cited by 36 · see citing works
Patterns of drug use among young men in Piedmont (Italy)
Siliquini, R., Faggiano, F., Geninatti, S., et al. (2001) · Drug and Alcohol Dependence · doi:10.1016/s0376-8716(01)00138-7 · Cited by 32 · see citing works
Mood differences between male and female light smokers and nonsmokers
File, S. E., Dinnis, A. K., Heard, J. E., & Irvine, E. E. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(02)00733-5 · Cited by 27 · see citing works
Self-citationGenn, R. F., Tucci, S. A., Parikh, S., & File, S. E. (2004) · Psychopharmacology · doi:10.1007/s00213-004-1932-5 · Cited by 26 · see citing works
Self-citationConditioned anxiety to nicotine
File, S. E., Cheeta, S., Irvine, E. E., Tucci, S. A., & Akthar, M. (2002) · Psychopharmacology · doi:10.1007/s00213-002-1219-7 · Cited by 21 · see citing works
Self-citationBorcel, É., Pérez-Álvarez, L., CEBALLOS, M. L. D., Ramírez, B. G., Marco, E. M., Fernández, B., Rubio, M., Guaza, C., & Viveros, M. (2004) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2004.02.020 · Cited by 16 · see citing works
Self-citationDeRossett, S. E., & Holtzman, S. G. (1985) · Psychopharmacology · doi:10.1007/bf00427896 · Cited by 15 · see citing works
Anxiety conditioned to nicotine in the elevated plus-maze is time dependent
Tucci, S. A., Cheeta, S., Genn, R. F., Seth, P., & File, S. E. (2002) · Behavioural Pharmacology · doi:10.1097/00008877-200212000-00002 · Cited by 15 · see citing works
Self-citationSakaue, M., Ago, Y., Sowa, C., et al. (2002) · European Journal of Pharmacology · doi:10.1016/s0014-2999(02)02786-3 · Cited by 13 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
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 · see citing works
Crippa, 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 · see citing works
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 · see citing works
The dark side of emotion: the addiction perspective
Koob, G. F. (2015) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2014.11.044 · Cited by 433 · see citing works
Zanelati, T., Biojone, C., Moreira, F., Guimarães, F., & Joca, S. (2010) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2009.00521.x · Cited by 366 · see citing works
Marsch, R., Foeller, E., Rammes, G., Bunck, M., Kössl, M., Holsboer, F., Zieglgänsberger, W., Landgraf, R., Lutz, B., & Wotjak, C. T. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.3303-06.2007 · Cited by 359 · see citing works
Bambico, F. R., Katz, N., Debonnel, G., & Gobbi, G. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.1636-07.2007 · Cited by 325 · see citing works
The neurobiology of individual differences in complex behavioral traits
Hariri, A. R. (2009) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.051508.135335 · Cited by 273 · see citing works
Cannabinoid Modulation of Amygdala Reactivity to Social Signals of Threat in Humans
Phan, K. L., Angstadt, M., Golden, J., Onyewuenyi, I., Popovska, A., & de Wit, H. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.5603-07.2008 · Cited by 251 · see citing works
Reich, C. G., Taylor, M. E., & McCarthy, M. M. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.05.013 · Cited by 244 · see citing works
Cannabis and psychiatric disorders: it is not only addiction
Leweke, F. M., & Koethe, D. (2008) · Addiction Biology · doi:10.1111/j.1369-1600.2008.00106.x · Cited by 213 · see citing works
Anxiolytic-like effect of cannabidiol in the rat Vogel conflict test
Moreira, F. A., Aguiar, D. C., & Guimarães, F. S. (2006) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2006.06.004 · Cited by 207 · see citing works
Clinical applications of hallucinogens: a review
Garcia-Romeu, A., Kersgaard, B., & Addy, P. H. (2016) · Experimental and Clinical Psychopharmacology · doi:10.1037/pha0000084 · Cited by 201 · see citing works
Evaluation of fatty acid amide hydrolase inhibition in murine models of emotionality
Naidu, P. S., Varvel, S. A., Ahn, K., Cravatt, B. F., Martin, B. R., & Lichtman, A. H. (2007) · Psychopharmacology · doi:10.1007/s00213-006-0689-4 · Cited by 184 · see citing works
Resstel, L. B. M., Joca, S. R. L., Moreira, F. A., Corrêa, F. M. A., & Guimarães, F. S. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.05.016 · Cited by 182 · see citing works
Moreira, F. A., & Wotjak, C. T. (2009) · Current topics in behavioral neurosciences · doi:10.1007/7854_2009_16 · Cited by 177 · see citing works
Ganon-Elazar, E., & Akirav, I. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.1223-09.2009 · Cited by 173 · see citing works
Campos, A. C., & Guimarães, F. S. (2009) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2009.08.017 · Cited by 172 · see citing works
Haller, J., Barna, I., Barsvari, B., Gyimesi Pelczer, K., Yasar, S., Panlilio, L. V., & Goldberg, S. (2009) · Psychopharmacology · doi:10.1007/s00213-009-1494-7 · Cited by 159 · see citing works
Shonesy, B. C., Bluett, R. J., Ramikie, T. S., Báldi, R., Hermanson, D. J., Kingsley, P. J., Marnett, L. J., Winder, D. G., Colbran, R. J., & Patel, S. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.11.001 · Cited by 155 · see citing works
Patel, S., Kingsley, P. J., Mackie, K., Marnett, L. J., & Winder, D. G. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2009.101 · Cited by 153 · see citing works
Lemos, J. I., Resstel, L. B., & Guimarães, F. S. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.09.045 · Cited by 146 · see citing works
Campos, A. C., Ferreira, F. R., & Guimarães, F. S. (2012) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2012.08.012 · Cited by 139 · see citing works
Sumislawski, J. J., Ramikie, T. S., & Patel, S. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.166 · Cited by 124 · see citing works
Ganon-Elazar, E., & Akirav, I. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2011.204 · Cited by 120 · see citing works
Nicotine 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 · see citing works
Self-citationEndocannabinoid-mediated synaptic plasticity and addiction-related behavior
Sidhpura, N., & Parsons, L. H. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.05.034 · Cited by 92 · see citing works
Bailey, C. R., Cordell, E., Sobin, S. M., & Neumeister, A. (2013) · CNS Drugs · doi:10.1007/s40263-013-0051-4 · Cited by 89 · see citing works
Kamprath, K., Romo-Parra, H., Häring, M., Gaburro, S., Doengi, M., Lutz, B., & Pape, H.-C. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.196 · Cited by 86 · see citing works
Chapter 5 The Endocannabinoid System as A Target for Novel Anxiolytic and Antidepressant Drugs
Gaetani, S., Dipasquale, P., Romano, A., Righetti, L., Cassano, T., Piomelli, D., & Cuomo, V. (2009) · International Review of Neurobiology · doi:10.1016/s0074-7742(09)85005-8 · Cited by 83 · see citing works
Testing the effects of Δ9-THC and D-cycloserine on extinction of conditioned fear in humans
Klumpers, F., Denys, D., Kenemans, J. L., Grillon, C., van der Aart, J., & Baas, J. M. (2012) · Journal of Psychopharmacology · doi:10.1177/0269881111431624 · Cited by 72 · see citing works
Cedernaes, J., Fanelli, F., Fazzini, A., Pagotto, U., Broman, J.-E., Vogel, H., Dickson, S. L., Schiöth, H. B., & Benedict, C. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.09.014 · Cited by 59 · see citing works
Klugmann, M., Goepfrich, A., Friemel, C. M., & Schneider, M. (2011) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2011.00037 · Cited by 49 · see citing works
Almeida-Santos, A. F., Gobira, P. H., Rosa, L. C., Guimaraes, F. S., Moreira, F. A., & Aguiar, D. C. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.05.027 · Cited by 41 · see citing works
Klugmann, M., Klippenstein, V., Leweke, F. M., Spanagel, R., & Schneider, M. (2011) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145710001562 · Cited by 38 · see citing works
Emerging Therapeutic Role of PPAR–α in Cognition and Emotions
Nisbett, K. E., & Pinna, G. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.00998 · Cited by 37 · see citing works
- Authors
- VIVEROS, M., MARCO, E., & FILE, S.
- Affiliations
- Universidad Complutense de Madrid (ES)
- King's College London (GB)
- Corresponding author
- VIVEROS, M
- ORCID
- Venue
- Pharmacology Biochemistry and Behavior
- Publisher
- Elsevier BV
- Published
- 2005-06
- Volume
- 81
- Issue
- 2
- Pages
- 331-342
- ISSN
- 0091-3057 (ISSN-L)
- OpenAlex
- W2056891327
- Cited by
- 485
- References
- 125
- Citations by year
- 2026: 8 · 2025: 18 · 2024: 11 · 2023: 10 · 2022: 13 · 2021: 17 · 2020: 26 · 2019: 23 · 2018: 20 · 2017: 18 · 2016: 23 · 2015: 33 · 2014: 24 · 2013: 27 · 2012: 34
- FWCI
- 17.82
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Pharmacology Biochemistry and Behavior (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Pharmacology › Cannabis and Cannabinoid Research
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Health Sciences › Medicine › Complementary and alternative medicine › Medicinal Plant Extracts Effects
- Keywords
- endocannabinoid system, anxiety, stress response, CB1 receptor, corticotropin-releasing factor, GABAA receptor, cholecystokinin, opioid system, serotonergic system, amygdala, hippocampus, adrenocortical function, CB1 receptor knockout mice
- MeSH terms
- Animals, Anxiety, Cannabinoids, Drug Interactions, Humans, Stress, Psychological, Substance-Related Disorders, Cannabinoid Receptor Modulators, Endocannabinoids
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