Activation of Corticotropin-Releasing Factor in the Limbic System During Cannabinoid Withdrawal
Abstract
Corticotropin-releasing factor (CRF) has been implicated in the mediation of the stress-like and negative affective consequences of withdrawal from drugs of abuse, such as alcohol, cocaine, and opiates. This study sought to determine whether brain CRF systems also have a role in cannabinoid dependence. Rats were treated daily for 2 weeks with the potent synthetic cannabinoid HU-210. Withdrawal, induced by the cannabinoid antagonist SR 141716A, was accompanied by a marked elevation in extracellular CRF concentration and a distinct pattern of Fos activation in the central nucleus of the amygdala. Maximal increases in CRF corresponded to the time when behavioral signs resulting from cannabinoid withdrawal were at a maximum. These data suggest that long-term cannabinoid administration alters CRF function in the limbic system of the brain, in a manner similar to that observed with other drugs of abuse, and also induces neuroadaptive processes that may result in future vulnerability to drug dependence.
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?
CRF production and release from the amygdala are greatly potentiated during withdrawal from various drugs and during chronic stress.
“CRF production in, and release from, the amygdala is greatly potentiated during withdrawal from a variety of drugs of abuse, as well as during chronic stress (Merlo Pich et al 1995; Rodriguez de Fonseca et al 1997; Richter and Weiss 1999; Stout et al 2000; Zorrilla et al 2001; Olive et al 2002; Funk et al 2006; George et al 2007).”
From The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction (2012) · cites this paper as Rodriguez de Fonseca et al 1997
Cites
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
Vale, W., Spiess, J., Rivier, C., & Rivier, J. (1981) · Science · doi:10.1126/science.6267699 · Cited by 3,965 · see citing works
Vale, W., Spiess, J., RIVIER, C. L., & Rivier, J. (1982) · Obstetrical & Gynecological Survey · doi:10.1097/00006254-198205000-00013 · Cited by 3,904 · see citing works
Morgan, J., & Curran, T. (1991) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.14.030191.002225 · Cited by 2,689 · see citing works
Determination and characterization of a cannabinoid receptor in rat brain
Devane, W. A., Dysarz, F. A., Johnson, M. R., Melvin, L. S., & Howlett, A. C. (1988) · Molecular Pharmacology · doi:10.1016/s0026-895x(25)09876-1 · Cited by 2,443 · 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
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 1,751 · see citing works
Anthony, J. C., Warner, L. A., & Kessler, R. C. (1994) · Experimental and Clinical Psychopharmacology · doi:10.1037/1064-1297.2.3.244 · Cited by 1,341 · see citing works
Bullitt, E. (1990) · Journal of Comparative Neurology · doi:10.1002/cne.902960402 · Cited by 1,059 · 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
Pich, E., Lorang, M., Yeganeh, M., Rodriguez de Fonseca, F., Raber, J., Koob, G., & Weiss, F. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-08-05439.1995 · Cited by 565 · see citing works
Self-citationExpression of c-Fos immunoreactivity in transmitter-characterized neurons after stress.
Ceccatelli, S., Villar, M. J., Goldstein, M., & Hökfelt, T. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.23.9569 · Cited by 536 · see citing works
Hollister, L. E. (1987) · Journal of Ethnopharmacology · doi:10.1016/0378-8741(87)90030-4 · Cited by 499 · see citing works
The residual cognitive effects of heavy marijuana use in college students
Pope, H. G. (1996) · JAMA · doi:10.1001/jama.275.7.521 · Cited by 469 · see citing works
Nuclear Receptor/AP-1 Interaction*
Pfahl, M. (1993) · Endocrine Reviews · doi:10.1210/edrv-14-5-651 · Cited by 445 · see citing works
Rassnick, S., Heinrichs, S. C., Britton, K. T., & Koob, G. F. (1993) · Brain Research · doi:10.1016/0006-8993(93)91352-s · Cited by 407 · see citing works
Self-citationThe Residual Cognitive Effects of Heavy Marijuana Use in College Students
Pope, H. G. (1996) · JAMA · doi:10.1001/jama.1996.03530310027028 · Cited by 354 · see citing works
Drug Addiction: The Yin and Yang of Hedonic Homeostasis
Koob, G. F. (1996) · Neuron · doi:10.1016/s0896-6273(00)80109-9 · Cited by 347 · see citing works
Self-citationNavarro, 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
Self-citationCorticotropin-releasing factor and behavior.
Koob, G. F., & Bloom, F. E. (1985) · PubMed · Cited by 292 · see citing works
Self-citation[38] Assay of corticotropin releasing factor
Vale, W., Vaughan, J. M., Yamamoto, G., BRUHN, T. O., Douglas, C., Dalton, D., RIVIER, C. L., & Rivier, J. (1983) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(83)03040-2 · Cited by 246 · see citing works
Corticotropin-releasing factor modulates defensive-withdrawal and exploratory behavior in rats.
Takahashi, L. K., Kalin, N. H., Burgt, J. A. V., & Sherman, J. E. (1989) · Behavioral Neuroscience · doi:10.1037//0735-7044.103.3.648 · Cited by 203 · see citing works
Hayward, M. D., Duman, R. S., & Nestler, E. J. (1990) · Brain Research · doi:10.1016/0006-8993(90)90872-9 · Cited by 181 · 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
Self-citationCorticotropin-releasing factor modulates defensive-withdrawal and exploratory behavior in rats.
Takahashi, L. K., Kalin, N. H., Burgt, J. A. V., et al. (1989) · Behavioral Neuroscience · doi:10.1037/0735-7044.103.3.648 · Cited by 175 · see citing works
Tsou, K., Patrick, S. L., & Walker, J. M. (1995) · European Journal of Pharmacology · doi:10.1016/0014-2999(95)00360-w · Cited by 173 · see citing works
Santucci, V., Storme, J.-J., Soubrié, P., & Fur, G. L. (1996) · Life Sciences · doi:10.1016/0024-3205(95)02319-4 · Cited by 165 · see citing works
Arnold, F. J. L., de Lucas Bueno, M., Shiers, H., Hancock, D. C., Evan, G. I., & Herbert, J. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90322-s · Cited by 155 · see citing works
Larsen, P., & Mikkelsen, J. D. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-04-02609.1995 · Cited by 142 · see citing works
An evaluation of the history of a marijuana withdrawal syndrome in a large population
Wiesbeck, G. A., Schuckit, M. A., Kalmijn, J. A., TIPP, J. E., Bucholz, K. K., & Smith, T. L. (1996) · Addiction · doi:10.1046/j.1360-0443.1996.911014696.x · Cited by 141 · see citing works
Corticotropin releasing factor, stress and behavior
Koob, G. F., Heinrichs, S. C., Menzaghi, F., Pich, E. M., & Britton, K. T. (1994) · Seminars in Neuroscience · doi:10.1006/smns.1994.1029 · Cited by 141 · see citing works
Self-citationCHARACTERISTICS OF TETRAHYDROCANNABINOL TOLERANCE*
McMillan, D. E., Dewey, W. L., & Harris, L. S. (1971) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1971.tb13990.x · Cited by 134 · see citing works
Alcohol selectively attenuates stress-induced c-fos expression in rat hippocampus
Ryabinin, A. E., Melia, K. R., Cole, M., Bloom, F. E., & Wilson, M. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-01-00721.1995 · Cited by 99 · see citing works
Corticosterone elevation mediated centrally by Δ1-tetrahydrocannabinol in rats
Kubena, R. K., Perhach, J. L., & Barry, H. (1971) · European Journal of Pharmacology · doi:10.1016/0014-2999(71)90128-2 · Cited by 91 · see citing works
Opponent process and drug dependence: Neurobiological mechanisms
Koob, G. F., Markou, A., Weiss, F., & Schulteis, G. (1993) · Seminars in Neuroscience · doi:10.1016/s1044-5765(05)80043-0 · Cited by 90 · see citing works
Self-citationHonkaniemi, J. (1992) · Brain Research · doi:10.1016/0006-8993(92)90173-7 · Cited by 64 · see citing works
Marijuana withdrawal syndrome in a woman
Mendelson, J. H., Mello, N. K., Lex, B. W., & Bavli, S. Z. (1984) · American Journal of Psychiatry · doi:10.1176/ajp.141.10.1289 · Cited by 57 · see citing works
Pich, E. M., Koob, G. F., Heilig, M. A., Menzaghi, F., Vale, W., & Weiss, F. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90435-i · Cited by 55 · see citing works
Self-citationImmediate early gene expression during morphine withdrawal
Beckmann, A. M., Matsumoto, I., & Wilce, P. A. (1995) · Neuropharmacology · doi:10.1016/0028-3908(95)00089-o · Cited by 46 · see citing works
A Longitudinal Study of Marijuana Effects
Halikas, J. A., Weller, R. A., Morse, C. L., & Hoffmann, R. G. (1985) · International Journal of the Addictions · doi:10.3109/10826088509044290 · Cited by 41 · see citing works
Imaki, T., Shibasaki, T., Wang, X.-Q., & Demura, H. (2008) · Neuroendocrinology · doi:10.1159/000126867 · Cited by 37 · see citing works
Menzaghi, F., Heinrichs, S. C., Merlo‐Pich, E., Tilders, F. J. H., & Koob, G. F. (1994) · Neuroscience Letters · doi:10.1016/0304-3940(94)90435-9 · Cited by 37 · see citing works
Self-citationThe effects of lesions of the posterior piriform cortex on amygdala kindling in the rat
Wahnschaffe, U., Ebert, U., & Löscher, W. (1993) · Brain Research · doi:10.1016/0006-8993(93)90041-k · Cited by 35 · see citing works
de Fonseca, F. R., Villanúa, M. Á., Muñoz, R. M., San-Martín-Clark, O., & Navarro, M. (2008) · Neuroendocrinology · doi:10.1159/000126899 · Cited by 34 · see citing works
Self-citationVARGAS, M. A., Bissette, G., Owens, M. J., Ehlers, C. L., & Nemeroff, C. B. (1992) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1992.tb25963.x · Cited by 14 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
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
Drug Addiction, Dysregulation of Reward, and Allostasis
Koob, G. (2001) · Neuropsychopharmacology · doi:10.1016/s0893-133x(00)00195-0 · Cited by 2,953 · see citing works
Self-citationDrug abuse: hedonic homeostatic dysregulation
Koob, G. F., & Moal, M. L. (1997) · Science · doi:10.1126/science.278.5335.52 · Cited by 2,535 · see citing works
Self-citationThe 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
Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system
Tsou, K., Brown, S., Sañudo-Peña, M. C., Mackie, K., & Walker, J. M. (1998) · Neuroscience · doi:10.1016/s0306-4522(97)00436-3 · Cited by 1,586 · see citing works
Modulation of anxiety through blockade of anandamide hydrolysis
Kathuria, S., Gaetani, S., Fegley, D., Valiño, F., Duranti, A., Tontini, A., Mor, M., Tarzia, G., Rana, G. L., Calignano, A., et al. (2003) · Nature Medicine · doi:10.1038/nm803 · Cited by 1,293 · see citing works
A Role for Brain Stress Systems in Addiction
Koob, G. F. (2008) · Neuron · doi:10.1016/j.neuron.2008.06.012 · Cited by 1,056 · see citing works
Self-citationKoob, G. F., Sanna, P. P., & Bloom, F. E. (1998) · Neuron · doi:10.1016/s0896-6273(00)80557-7 · Cited by 1,026 · see citing works
Self-citationThe 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
The effects of cannabinoids on the brain
Ameri, A. (1999) · Progress in Neurobiology · doi:10.1016/s0301-0082(98)00087-2 · Cited by 805 · see citing works
Alcoholism: Allostasis and Beyond
Koob, G. F. (2003) · Alcoholism Clinical and Experimental Research · doi:10.1097/01.alc.0000057122.36127.c2 · Cited by 737 · see citing works
Self-citationIversen, L. L. (2003) · Brain · doi:10.1093/brain/awg143 · Cited by 735 · see citing works
Tsuang, M. T., Lyons, M. J., Meyer, J. M., Doyle, T., Eisen, S. A., Goldberg, J., True, W., Lin, N., Toomey, R., & Eaves, L. (1998) · Archives of General Psychiatry · doi:10.1001/archpsyc.55.11.967 · Cited by 710 · see citing works
Drug dependence: stress and dysregulation of brain reward pathways
Kreek, M. J., & Koob, G. F. (1998) · Drug and Alcohol Dependence · doi:10.1016/s0376-8716(98)00064-7 · Cited by 696 · see citing works
Self-citationKatona, 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
Holsboer, F. (1999) · Journal of Psychiatric Research · doi:10.1016/s0022-3956(98)90056-5 · Cited by 654 · see citing works
Corticotropin-releasing factor, norepinephrine, and stress
Koob, G. F. (1999) · Biological Psychiatry · doi:10.1016/s0006-3223(99)00164-x · Cited by 629 · see citing works
Self-citationA role for corticotropin releasing factor and urocortin in behavioral responses to stressors
Koob, G. F., & Heinrichs, S. C. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01991-5 · Cited by 530 · see citing works
Self-citationReview of the Validity and Significance of Cannabis Withdrawal Syndrome
Budney, A. J., Hughes, J. R., Moore, B. A., & Vandrey, R. G. (2004) · American Journal of Psychiatry · doi:10.1176/appi.ajp.161.11.1967 · Cited by 521 · see citing works
A Peripheral Mechanism for CB1 Cannabinoid Receptor-Dependent Modulation of Feeding
Gómez, R., Navarro, M., Ferrer, B., Trigo, J. M., Bilbao, A., del Arco, I., Cippitelli, A., Nava, F. A., Piomelli, D., & de Fonseca, F. R. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-21-09612.2002 · Cited by 486 · see citing works
Self-citationRole of Corticotropin-Releasing Factor in Drug Addiction
Logrip, M. L., Koob, G. F., & Zorrilla, E. P. (2011) · CNS Drugs · doi:10.2165/11587790-000000000-00000 · Cited by 476 · see citing works
Self-citationCannabinoids and Neuroprotection in Global and Focal Cerebral Ischemia and in Neuronal Cultures
Nagayama, T., Sinor, A. D., Simon, R. P., Chen, J., Graham, S. H., Jin, K., & Greenberg, D. A. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-08-02987.1999 · Cited by 468 · see citing works
Neurobiological substrates for the dark side of compulsivity in addiction
Koob, G. F. (2008) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.07.043 · Cited by 458 · see citing works
Self-citationCompulsive Drug‐Seeking Behavior and Relapse: Neuroadaptation, Stress, and Conditioning Factors
WEISS, F., CICCOCIOPPO, R., PARSONS, L. H., KATNER, S., LIU, X., ZORRILLA, E. P., VALDEZ, G. R., BEN‐SHAHAR, O., ANGELETTI, S., & RICHTER, R. R. (2001) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2001.tb03556.x · Cited by 430 · see citing works
Self-citationNeural mechanisms underlying nicotine addiction: acute positive reinforcement and withdrawal
S. Watkins, G. F. K. (2000) · Nicotine & Tobacco Research · doi:10.1080/14622200050011277 · Cited by 424 · see citing works
Schulkin, J., W. Gold, P., & S. McEwen, B. (1998) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(97)00099-1 · Cited by 423 · see citing works
Dietrich, A., & McDaniel, W. F. (2004) · British Journal of Sports Medicine · doi:10.1136/bjsm.2004.011718 · Cited by 410 · see citing works
THE ENDOCANNABINOID SYSTEM: PHYSIOLOGY AND PHARMACOLOGY
de Fonseca, F. R., del Arco, I., Bermúdez‐Silva, F. J., Bilbao, A., Cippitelli, A., & Navarro, M. (2004) · Alcohol and Alcoholism · doi:10.1093/alcalc/agh110 · Cited by 409 · see citing works
Self-citationKeep off the grass? Cannabis, cognition and addiction
Curran, H. V., Freeman, T. P., Mokrysz, C., Lewis, D. A., Morgan, C. J. A., & Parsons, L. H. (2016) · Nature reviews. Neuroscience · doi:10.1038/nrn.2016.28 · Cited by 381 · see citing works
Brain stress systems in the amygdala and addiction
Koob, G. F. (2009) · Brain Research · doi:10.1016/j.brainres.2009.03.038 · Cited by 388 · see citing works
Self-citationEndocannabinoid signaling system and brain reward: emphasis on dopamine
GARDNER, E. (2005) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2005.01.032 · Cited by 387 · see citing works
The Role of Corticotropin-Releasing Factor in Drug Addiction
Sarnyai, Z., Shaham, Y., & Heinrichs, S. C. (2001) · Pharmacological Reviews · doi:10.1016/s0031-6997(24)01492-3 · Cited by 381 · see citing works
Functional interaction between opioid and cannabinoid receptors in drug self-administration.
Navarro, M., Carrera, M. R. A., Fratta, W., Valverde, O., Cossu, G., Fattore, L., Chowen, J. A., Gómez, R., del Arco, I., Villanúa, M. A., et al. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-14-05344.2001 · Cited by 378 · see citing works
Self-citationReverse gateways? Frequent cannabis use as a predictor of tobacco initiation and nicotine dependence
Patton, G. C., Coffey, C., Carlin, J. B., Sawyer, S. M., & Lynskey, M. T. (2005) · Addiction · doi:10.1111/j.1360-0443.2005.01220.x · Cited by 356 · see citing works
A missense mutation in human fatty acid amide hydrolase associated with problem drug use
Sipe, J. C., Chiang, K. P., Gerber, A. L., Beutler, E., & Cravatt, B. F. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.082235799 · Cited by 354 · see citing works
The cannabis withdrawal syndrome
Budney, A. J., & Hughes, J. R. (2006) · Current Opinion in Psychiatry · doi:10.1097/01.yco.0000218592.00689.e5 · Cited by 351 · see citing works
Stress-related factors in cannabis use and misuse: Implications for prevention and treatment
Hyman, S. M., & Sinha, R. (2009) · Journal of Substance Abuse Treatment · doi:10.1016/j.jsat.2008.08.005 · Cited by 344 · see citing works
Corticotropin-releasing hormone receptor subtypes and emotion
Steckler, T., & Holsboer, F. (1999) · Biological Psychiatry · doi:10.1016/s0006-3223(99)00170-5 · Cited by 323 · see citing works
The Role of the Striatopallidal and Extended Amygdala Systems in Drug Addiction
Koob, G. F. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb09282.x · Cited by 322 · see citing works
Self-citationShepard, J. D., Barron, K. W., & Myers, D. A. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02019-9 · Cited by 321 · 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
Sex differences in the neural mechanisms mediating addiction: a new synthesis and hypothesis
Becker, J. B., Perry, A. N., & Westenbroek, C. (2012) · Biology of Sex Differences · doi:10.1186/2042-6410-3-14 · Cited by 315 · see citing works
Neurobiology of Addiction: Toward the Development of New Therapies
Koob, G. F. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb06682.x · Cited by 314 · see citing works
Self-citationPuberty as a highly vulnerable developmental period for the consequences of cannabis exposure
Schneider, M. (2008) · Addiction Biology · doi:10.1111/j.1369-1600.2008.00110.x · Cited by 330 · see citing works
Neurobiology of the nicotine withdrawal syndrome
Kenny, P. J., & Markou, A. (2001) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(01)00651-7 · Cited by 310 · see citing works
Burkett, J. P., & Young, L. J. (2012) · Psychopharmacology · doi:10.1007/s00213-012-2794-x · Cited by 307 · see citing works
Relapse to drug-seeking: neural and molecular mechanisms
Self, D. W., & Nestler, E. J. (1998) · Drug and Alcohol Dependence · doi:10.1016/s0376-8716(98)00065-9 · Cited by 296 · see citing works
van der Stelt, M., & Marzo, V. D. (2003) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2003.08.101 · Cited by 286 · see citing works
The role of CRF and CRF-related peptides in the dark side of addiction
Koob, G. F. (2009) · Brain Research · doi:10.1016/j.brainres.2009.11.008 · Cited by 290 · see citing works
Self-citationGonzález, 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
Tanda, G., & Goldberg, S. R. (2003) · Psychopharmacology · doi:10.1007/s00213-003-1485-z · Cited by 280 · see citing works
Rosenberg, E. C., Tsien, R. W., Whalley, B. J., & Devinsky, O. (2015) · Neurotherapeutics · doi:10.1007/s13311-015-0375-5 · Cited by 282 · see citing works
Cortisol secretion patterns in addiction and addiction risk
Lovallo, W. R. (2006) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2005.10.007 · Cited by 269 · see citing works
Merali, Z., McIntosh, J. F., Kent, P., Michaud, D. S., & Anisman, H. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-12-04758.1998 · Cited by 268 · see citing works
Cannabis Use, Abuse, and Dependence in a Population-Based Sample of Female Twins
Kendler, K. S., & Prescott, C. A. (1998) · American Journal of Psychiatry · doi:10.1176/ajp.155.8.1016 · Cited by 265 · see citing works
Hall, W., & Lynskey, M. T. (2005) · Drug and Alcohol Review · doi:10.1080/09595230500126698 · Cited by 265 · see citing works
Sex differences in the neurobiology of drug addiction
Bobzean, S. A. M., Nobrega, A. K. D., & Perrotti, L. I. (2014) · Experimental Neurology · doi:10.1016/j.expneurol.2014.01.022 · Cited by 261 · see citing works
Abstinence symptoms following oral THC administration to humans
Haney, M., Ward, A. S., Comer, S. D., Foltin, R. W., & Fischman, M. W. (1999) · Psychopharmacology · doi:10.1007/s002130050848 · Cited by 261 · see citing works
Cannabinoid tolerance and dependence: A review of studies in laboratory animals
González, S. R., Cebeira, M., & Fernández‐Ruíz, J. (2005) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2005.01.028 · Cited by 258 · see citing works
The dark side of food addiction
Parylak, S. L., Koob, G. F., & Zorrilla, E. P. (2011) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.04.063 · Cited by 257 · see citing works
Self-citationCorticotropin releasing factor: A key role in the neurobiology of addiction
Zorrilla, E. P., Logrip, M. L., & Koob, G. F. (2014) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2014.01.001 · Cited by 255 · see citing works
Self-citationCannabis Addiction and the Brain: a Review
Zehra, A., Burns, J. A., Liu, C. K., Manza, P., Wiers, C. E., Volkow, N. D., & Wang, G. (2018) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-018-9782-9 · Cited by 258 · 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
Cannabinoid Transmission and Reward-Related Events
Gardner, E. L., & Vorel, S. R. (1998) · Neurobiology of Disease · doi:10.1006/nbdi.1998.0219 · Cited by 247 · see citing works
Mason, B. J., Crean, R., Goodell, V., Light, J. M., Quello, S., Shadan, F., Buffkins, K., Kyle, M., Adusumalli, M., Begovic, A., et al. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2012.14 · Cited by 242 · see citing works
Uhl, G. R., Koob, G. F., & Cable, J. (2019) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.13989 · Cited by 259 · see citing works
Self-citationOlive, M. F., Koenig, H. N., Nannini, M. A., & Hodge, C. W. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(01)00748-1 · Cited by 237 · see citing works
Martín, M., Ledent, C. A., Parmentier, M., Maldonado, R. J., & Valverde, O. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.00287.x · Cited by 237 · see citing works
Stress, Corticotropin‐releasing Factor, and Drug Addiction
Koob, G. F. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb07876.x · Cited by 231 · see citing works
Self-citationCrowley, T. J., Macdonald, M. J., Whitmore, E. A., & Mikulich, S. K. (1998) · Drug and Alcohol Dependence · doi:10.1016/s0376-8716(98)00003-9 · Cited by 231 · see citing works
The 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
Marijuana Abstinence Effects in Marijuana Smokers Maintained in Their Home Environment
Budney, A. J., Hughes, J. R., Moore, B. A., & Novy, P. L. (2001) · Archives of General Psychiatry · doi:10.1001/archpsyc.58.10.917 · Cited by 223 · see citing works
Leshner, A. I., & Koob, G. F. (1999) · Proceedings of the Association of American Physicians · doi:10.1046/j.1525-1381.1999.09218.x · Cited by 220 · see citing works
Self-citationThe endocannabinoid system: emotion, learning and addiction
Moreira, F. A., & Lutz, B. (2008) · Addiction Biology · doi:10.1111/j.1369-1600.2008.00104.x · Cited by 222 · 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
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
Adverse effects of cannabis and cannabinoids
Ashton, C. H. (1999) · British Journal of Anaesthesia · doi:10.1093/bja/83.4.637 · Cited by 213 · see citing works
Iversen, L. L. (2007) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195328240.001.0001 · Cited by 230 · see citing works
Smith, R. J., & Aston-Jones, G. (2008) · Brain Structure and Function · doi:10.1007/s00429-008-0191-3 · Cited by 206 · see citing works
Frerking, M., & Wilson, M. (1999) · Synapse · doi:10.1002/(sici)1098-2396(19990615)32:4 · Cited by 2 · see citing works
Self-citationCannabis use in young people: The risk for schizophrenia
Casadio, P., Fernandes, C., Murray, R. M., & Forti, M. D. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.04.007 · Cited by 207 · see citing works
Cannabinoid Addiction: Behavioral Models and Neural Correlates
Maldonado, R. J., & de Fonseca, F. R. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-09-03326.2002 · Cited by 205 · see citing works
Self-administration of the cannabinoid receptor agonist WIN 55,212-2 in drug-naive mice
Martellotta, M. C., Cossu, G., Fattore, L., Gessa, G. L., & Fratta, W. (1998) · Neuroscience · doi:10.1016/s0306-4522(98)00052-9 · Cited by 202 · see citing works
Glucocorticoids, chronic stress, and obesity
Dallman, M. F., Pecoraro, N. C., La Fleur, S. E., Warne, J. P., Ginsberg, A. B., Akana, S. F., Laugero, K. C., Houshyar, H., Strack, A. M., Bhatnagar, S., et al. (2006) · Progress in Brain Research · doi:10.1016/s0079-6123(06)53004-3 · Cited by 198 · see citing works
The Functional Neuroanatomy of Brain Cannabinoid Receptors
Breivogel, C. S., & Childers, S. R. (1998) · Neurobiology of Disease · doi:10.1006/nbdi.1998.0229 · Cited by 195 · see citing works
Hutcheson, D. M., Tzavara, E. T., Smadja, C., Valjent, E., Roques, B. P., Hanoune, J., & Maldonado, R. J. (1998) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0702228 · Cited by 192 · see citing works
Mesolimbic dopaminergic decline after cannabinoid withdrawal
Diana, M., Melis, M., Muntoni, A. L., & Gessa, G. L. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.17.10269 · Cited by 192 · see citing works
Basso, A. M., Spina, M. G., Rivier, J., Vale, W., & Koob, G. F. (1999) · Psychopharmacology · doi:10.1007/s002130051028 · Cited by 190 · see citing works
Self-citationDecreases in Dietary Preference Produce Increased Emotionality and Risk for Dietary Relapse
Teegarden, S. L., & Bale, T. L. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.09.032 · Cited by 188 · see citing works
Oral delta-9-tetrahydrocannabinol suppresses cannabis withdrawal symptoms
Budney, A. J., Vandrey, R. G., Hughes, J. R., Moore, B. A., & Bahrenburg, B. (2007) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2006.04.014 · Cited by 180 · see citing works
Tobacco addiction and the dysregulation of brain stress systems
Bruijnzeel, A. W. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.02.015 · Cited by 172 · 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
McGregor, I. S., Callaghan, P. D., & Hunt, G. E. (2008) · British Journal of Pharmacology · doi:10.1038/bjp.2008.132 · Cited by 171 · 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
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
Role of the endocannabinoid system in regulation of the hypothalamic-pituitary-adrenocortical axis
Steiner, M. S., & Wotjak, C. T. (2008) · Progress in brain research · doi:10.1016/s0079-6123(08)00433-0 · Cited by 167 · see citing works
Valjent, E., Pagès, C., Rogard, M., Besson, M., Maldonado, R. J., & Caboche, J. (2001) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01652.x · Cited by 168 · see citing works
Läck, A. K., Diaz, M. R., Chappell, A. M., DuBois, D. W., & McCool, B. A. (2007) · Journal of Neurophysiology · doi:10.1152/jn.00189.2007 · Cited by 167 · see citing works
Role of the Endogenous Cannabinoid System in the Regulation of Motor Activity
de Fonseca, F. R., del Arco, I., Martı́n-Calderón, J. L., Gorriti, M. Á., & Navarro, M. (1998) · Neurobiology of Disease · doi:10.1006/nbdi.1998.0217 · Cited by 166 · see citing works
Self-citation
- Authors
- Rodrı́guez de Fonseca, F., Carrera, M. R. A., Navarro, M., Koob, G. F., & Weiss, F.
- Affiliations
- F. Rodrı́guez de Fonseca and M. Navarro, Instituto Complutense de Drogodependencias, Departamento de Psicobiologı́a, Facultad de Psicologı́a, Universidad Complutense de Madrid, 28223 Madrid, Spain.
- Universidad Complutense de Madrid (ES)
- Corresponding author
- Navarro, Miguel
- Venue
- Science
- Published
- 1997-06-27
- Volume
- 276
- Issue
- 5321
- Pages
- 2050-2054
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W2124997151
- Cited by
- 499
- References
- 45
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 3 · 2023: 4 · 2022: 3 · 2021: 8 · 2020: 3 · 2019: 11 · 2018: 19 · 2017: 7 · 2016: 7 · 2015: 7 · 2014: 8 · 2013: 12 · 2012: 21
- FWCI
- 27.34
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r03da008426-02)
- National Institute on Drug Abuse (DA 08426)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK 26741, P01DK026741)
- Topics
- Health Sciences › Medicine › Pharmacology › Cannabis and Cannabinoid Research
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Keywords
- corticotropin-releasing factor, cannabinoid withdrawal, HU-210, SR141716A, Fos activation, central amygdala, limbic system, neural adaptation, drug addiction, stress response
- MeSH terms
- Rimonabant, Amygdala, Animals, Anxiety, Behavior, Animal, Brain, Corticosterone, Corticotropin-Releasing Hormone, Male, Piperidines, Pyrazoles, Receptors, Drug, Substance Withdrawal Syndrome, Dronabinol, Proto-Oncogene Proteins c-fos, Rats, Wistar, Microdialysis, Receptors, Cannabinoid, 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
