Chronic THC during adolescence increases the vulnerability to stress-induced relapse to heroin seeking in adult rats

European Neuropsychopharmacology

Volumn 24, Issue 7, 2014, Pages 1037-1045

  Stopponi, Serena ^a   Soverchia, Laura ^a   Ubaldi, Massimo ^a   Cippitelli, Andrea ^a   Serpelloni, Giovanni ^b   Ciccocioppo, Roberto ^a  

^a UNIVERSITY OF CAMERINO   (Italy)

^b Presidenza del Cons dei Ministri   (Italy)

Author keywords

Addiction; Adolescence; Anxiety; Rat; Self administration; THC

Indexed keywords

DIAMORPHINE; DRONABINOL; YOHIMBINE;

ADOLESCENCE; ADOLESCENT; ADULT; ADULTHOOD; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; BODY WEIGHT; CANNABIS USE; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; DISEASE PREDISPOSITION; DRUG EXPOSURE; DRUG SEEKING BEHAVIOR; FOOD INTAKE; HEROIN DEPENDENCE; INTOXICATION; LONG TERM EXPOSURE; MALE; MAZE TEST; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; RAT; RELAPSE; SELF ADMINISTRATION TEST; STRESS; ADDICTION; ANIMAL; ANIMAL BEHAVIOR; DRUG EFFECTS; DRUG SELF ADMINISTRATION; INSTRUMENTAL CONDITIONING; MENTAL STRESS; PHYSIOLOGICAL STRESS; REINFORCEMENT; WISTAR RAT;

ANIMALS; BEHAVIOR, ADDICTIVE; BEHAVIOR, ANIMAL; CONDITIONING, OPERANT; DRONABINOL; DRUG-SEEKING BEHAVIOR; EXTINCTION, PSYCHOLOGICAL; HEROIN; RATS; RATS, WISTAR; SELF ADMINISTRATION; STRESS, PHYSIOLOGICAL; STRESS, PSYCHOLOGICAL;

EID: 84902323976     PISSN: 0924977X     EISSN: 18737862     Source Type: Journal    
DOI: 10.1016/j.euroneuro.2013.12.012     Document Type: Article

References (80)

1. Abercrombie E.D., Keller R.W., Zigmond M.J. Characterization of hippocampal norepinephrine release as measured by microdialysis perfusion: pharmacological and behavioral studies. Neuroscience 1988, 27:897-904.
2. Aghajanian G.K., VanderMaelen C.P. Alpha 2-adrenoceptor-mediated hyperpolarization of locus coeruleus neurons: intracellular studies in vivo. Science 1982, 215:1394-1396.
3. Banna K.M., Back S.E., Do P., See R.E. Yohimbine stress potentiates conditioned cue-induced reinstatement of heroin-seeking in rats. Behav. Brain Res. 2010, 208:144-148.
4. Belue R.C., Howlett A.C., Westlake T.M., Hutchings D.E. The ontogeny of cannabinoid receptors in the brain of postnatal and aging rats. Neurotoxicol. Teratol. 1995, 17:25-30.
5. Biscaia M., Marin S., Fernandez B., Marco E.M., Rubio M., Guaza C., Ambrosio E., Viveros M.P. Chronic treatment with CP 55,940 during the peri-adolescent period differentially affects the behavioural responses of male and female rats in adulthood. Psychopharmacology (Berl) 2003, 170:301-308.
6. Cadoni C., Simola N., Espa E., Fenu S., Di Chiara G. Strain dependence of adolescent Cannabis influence on heroin reward and mesolimbic dopamine transmission in adult Lewis and Fischer 344 rats. Addict. Biol 2013.
7. Cheer J.F., Kendall D.A., Marsden C.A. Cannabinoid receptors and reward in the rat: a conditioned place preference study. Psychopharmacology (Berl) 2000, 151:25-30.
8. Cheung J.T., Mann R.E., Ialomiteanu A., Stoduto G., Chan V., Ala-Leppilampi K., Rehm J. Anxiety and mood disorders and cannabis use. Am. J. Drug Alcohol Abuse 2010, 36:118-122.
9. Ciccocioppo R., Antonelli L., Biondini M., Perfumi M., Pompei P., Massi M. Memory impairment following combined exposure to delta (9)-tetrahydrocannabinol and ethanol in rats. Eur. J. Pharmacol. 2002, 449:245-252.
10. Cossu G., Ledent C., Fattore L., Imperato A., Bohme G.A., Parmentier M., Fratta W. Cannabinoid CB1 receptor knockout mice fail to self-administer morphine but not other drugs of abuse. Behav. Brain Res. 2001, 118:61-65.
11. Croft R.J., Mackay A.J., Mills A.T., Gruzelier J.G. The relative contributions of ecstasy and cannabis to cognitive impairment. Psychopharmacology (Berl) 2001, 153:373-379.
12. Cruz A.P., Frei F., Graeff F.G. Ethopharmacological analysis of rat behavior on the elevated plus-maze. Pharmacol. Biochem. Behav. 1994, 49:171-176.
13. D'Souza D.C., Sewell R.A., Ranganathan M. Cannabis and psychosis/schizophrenia: human studies. Eur. Arch. Psychiatry. Clin. Neurosci. 2009, 259:413-431.
14. Dannon P.N., Lowengrub K., Amiaz R., Grunhaus L., Kotler M. Comorbid cannabis use and panic disorder: short term and long term follow-up study. Hum. Psychopharmacol. 2004, 19:97-101.
15. Dow-Edwards D., Izenwasser S. Pretreatment with delta 9-tetrahydrocannabinol (THC) increases cocaine-stimulated activity in adolescent but not adult male rats. Pharmacol. Biochem. Behav. 2012, 100:587-591.
16. Economidou D., Mattioli L., Ubaldi M., Lourdusamy A., Soverchia L., Hardiman G., Campolongo P., Cuomo V., Ciccocioppo R. Role of cannabinoidergic mechanisms in ethanol self-administration and ethanol seeking in rat adult offspring following perinatal exposure to Delta9-tetrahydrocannabinol. Toxicol. Appl. Pharmacol. 2007, 223:73-85.
17. Ellgren M., Artmann A., Tkalych O., Gupta A., Hansen H.S., Hansen S.H., Devi L.A., Hurd Y.L. Dynamic changes of the endogenous cannabinoid and opioid mesocorticolimbic systems during adolescence: THC effects. Eur. Neuropsychopharmacol. 2008, 18:826-834.
18. Ellgren M., Spano S.M., Hurd Y.L. Adolescent cannabis exposure alters opiate intake and opioid limbic neuronal populations in adult rats. Neuropsychopharmacology 2007, 32:607-615.
19. Evins A.E., Green A.I., Kane J.M., Murray R.M. The effect of marijuana use on the risk for schizophrenia. J. Clin. Psychiatry 2012, 73:1463-1468.
20. Ferdinand R.F., Sondeijker F., van der Ende J., Selten J.P., Huizink A., Verhulst F.C. Cannabis use predicts future psychotic symptoms, and vice versa. Addiction 2005, 100:612-618.
21. Fergusson D.M., Horwood L.J., Swain-Campbell N. Cannabis use and psychosocial adjustment in adolescence and young adulthood. Addiction 2002, 97:1123-1135.
22. Fergusson D.M., Horwood L.J., Swain-Campbell N.R. Cannabis dependence and psychotic symptoms in young people. Psychol. Med. 2003, 33:15-21.
23. Fernandez-Espejo E., Viveros M.P., Nunez L., Ellenbroek B.A., Rodriguez de Fonseca F. Role of cannabis and endocannabinoids in the genesis of schizophrenia. Psychopharmacology (Berl) 2009, 206:531-549.
24. Gonzalez R. Acute and non-acute effects of cannabis on brain functioning and neuropsychological performance. Neuropsychol. Rev. 2007, 17:347-361.
25. Hall W.D., Lynskey M. Is cannabis a gateway drug? Testing hypotheses about the relationship between cannabis use and the use of other illicit drugs. Drug Alcohol Rev. 2005, 24:39-48.
26. Herkenham M., Lynn A.B., Johnson M.R., Melvin L.S., de Costa B.R., Rice K.C. Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J. Neurosci. 1991, 11:563-583.
27. Hill M.N., Gorzalka B.B. Enhancement of anxiety-like responsiveness to the cannabinoid CB(1) receptor agonist HU-210 following chronic stress. Eur. J. Pharmacol. 2004, 499:291-295.
28. Hill M.N., Gorzalka B.B. Increased sensitivity to restraint stress and novelty-induced emotionality following long-term, high dose cannabinoid exposure. Psychoneuroendocrinology 2006, 31:526-536.
29. Hurd Y.L., Michaelides M., Miller M.L., Jutras-Aswad D. Trajectory of adolescent cannabis use on addiction vulnerability. Neuropharmacology 2013.
30. Kirkham T.C., Williams C.M., Fezza F., Di Marzo V. Endocannabinoid levels in rat limbic forebrain and hypothalamus in relation to fasting, feeding and satiation: stimulation of eating by 2-arachidonoyl glycerol. Br. J. Pharmacol. 2002, 136:550-557.
31. Kubena R.K., Perhach J.L., Barry H. Corticosterone elevation mediated centrally by delta 1-tetrahydrocannabinol in rats. Eur. J. Pharmacol. 1971, 14:89-92.
32. Le A.D., Harding S., Juzytsch W., Funk D., Shaham Y. Role of alpha-2 adrenoceptors in stress-induced reinstatement of alcohol seeking and alcohol self-administration in rats. Psychopharmacology (Berl) 2005, 179:366-373.
33. Ledent C., Valverde O., Cossu G., Petitet F., Aubert J.F., Beslot F., Bohme G.A., Imperato A., Pedrazzini T., Roques B.P., Vassart G., Fratta W., Parmentier M. Unresponsiveness to cannabinoids and reduced addictive effects of opiates in CB1 receptor knockout mice. Science 1999, 283:401-404.
34. Mallet P.E., Beninger R.J. Delta9-tetrahydrocannabinol, but not the endogenous cannabinoid receptor ligand anandamide, produces conditioned place avoidance. Life Sci. 1998, 62:2431-2439.
35. Malone D.T., Hill M.N., Rubino T. Adolescent cannabis use and psychosis: epidemiology and neurodevelopmental models. Br. J. Pharmacol. 2010, 160:511-522.
36. Marco E.M., Perez-Alvarez L., Borcel E., Rubio M., Guaza C., Ambrosio E., File S.E., Viveros M.P. Involvement of 5-HT1A receptors in behavioural effects of the cannabinoid receptor agonist CP 55,940 in male rats. Behav. Pharmacol. 2004, 15:21-27.
37. Marinelli P.W., Funk D., Juzytsch W., Harding S., Rice K.C., Shaham Y., Le A.D. The CRF1 receptor antagonist antalarmin attenuates yohimbine-induced increases in operant alcohol self-administration and reinstatement of alcohol seeking in rats. Psychopharmacology (Berl) 2007, 195:345-355.
38. McLaughlin C.R., Martin B.R., Compton D.R., Abood M.E. Cannabinoid receptors in developing rats: detection of mRNA and receptor binding. Drug Alcohol Depend. 1994, 36:27-31.
39. Murray J.E., Bevins R.A. Cannabinoid conditioned reward and aversion: behavioral and neural processes. ACS Chem. Neurosci. 2010, 1:265-278.
40. O'Shea M., McGregor I.S., Mallet P.E. Repeated cannabinoid exposure during perinatal, adolescent or early adult ages produces similar longlasting deficits in object recognition and reduced social interaction in rats. J. Psychopharmacol. 2006, 20:611-621.
41. O'Shea M., Singh M.E., McGregor I.S., Mallet P.E. Chronic cannabinoid exposure produces lasting memory impairment and increased anxiety in adolescent but not adult rats. J. Psychopharmacol. 2004, 18:502-508.
42. Panlilio L.V., Solinas M., Matthews S.A., Goldberg S.R. Previous exposure to THC alters the reinforcing efficacy and anxiety-related effects of cocaine in rats. Neuropsychopharmacology 2007, 32:646-657.
43. Parker L.A., Gillies T. THC-induced place and taste aversions in Lewis and Sprague-Dawley rats. Behav. Neurosci. 1995, 109:71-78.
44. Patel S., Roelke C.T., Rademacher D.J., Cullinan W.E., Hillard C.J. Endocannabinoid signaling negatively modulates stress-induced activation of the hypothalamic-pituitary-adrenal axis. Endocrinology 2004, 145:5431-5438.
45. Patton G.C., Coffey C., Carlin J.B., Degenhardt L., Lynskey M., Hall W. Cannabis use and mental health in young people: cohort study. BMJ 2002, 325:1195-1198.
46. Pellow S., File S.E. Evidence that the beta-carboline, ZK 91296, can reduce anxiety in animals at doses well below those causing sedation. Brain Res. 1986, 363:174-177.
47. Pistis M., Perra S., Pillolla G., Melis M., Muntoni A.L., Gessa G.L. Adolescent exposure to cannabinoids induces long-lasting changes in the response to drugs of abuse of rat midbrain dopamine neurons. Biol. Psychiatry 2004, 56:86-94.
48. Poddar M.K., Dewey W.L. Effects of cannabinoids on catecholamine uptake and release in hypothalamic and striatal synaptosomes. J. Pharmacol. Exp. Ther. 1980, 214:63-67.
49. Quinn H.R., Matsumoto I., Callaghan P.D., Long L.E., Arnold J.C., Gunasekaran N., Thompson M.R., Dawson B., Mallet P.E., Kashem M.A., Matsuda-Matsumoto H., Iwazaki T., McGregor I.S. Adolescent rats find repeated Delta(9)-THC less aversive than adult rats but display greater residual cognitive deficits and changes in hippocampal protein expression following exposure. Neuropsychopharmacology 2008, 33:1113-1126.
50. Renard J., Krebs M.O., Jay T.M., Le Pen G. Long-term cognitive impairments induced by chronic cannabinoid exposure during adolescence in rats: a strain comparison. Psychopharmacology (Berl) 2013, 225:781-790.
51. Rey A.A., Purrio M., Viveros M.P., Lutz B. Biphasic effects of cannabinoids in anxiety responses: CB1 and GABA(B) receptors in the balance of GABAergic and glutamatergic neurotransmission. Neuropsychopharmacology 2012, 37:2624-2634.
52. Robinson L., Hinder L., Pertwee R.G., Riedel G. Effects of delta9-THC and WIN-55,212-2 on place preference in the water maze in rats. Psychopharmacology (Berl) 2003, 166:40-50.
53. Rodriguez de Fonseca F., Carrera M.R., Navarro M., Koob G.F., Weiss F. Activation of corticotropin-releasing factor in the limbic system during cannabinoid withdrawal. Science 1997, 276:2050-2054.
54. Rodriguez de Fonseca F., Ramos J.A., Bonnin A., Fernandez-Ruiz J.J. Presence of cannabinoid binding sites in the brain from early postnatal ages. Neuroreport 1993, 4:135-138.
55. Rodriguez de Fonseca F., Rubio P., Menzaghi F., Merlo-Pich E., Rivier J., Koob G.F., Navarro M. Corticotropin-releasing factor (CRF) antagonist [D-Phe12,Nle21,38,C alpha MeLeu37]CRF attenuates the acute actions of the highly potent cannabinoid receptor agonist HU-210 on defensive-withdrawal behavior in rats. J. Pharmacol. Exp. Ther. 1996, 276:56-64.
56. Rubino T., Parolaro D. Long lasting consequences of cannabis exposure in adolescence. Mol. Cell. Endocrinol. 2008, 286:S108-113.
57. Rubino T., Parolaro D. Cannabis abuse in adolescence and the risk of psychosis: a brief review of the preclinical evidence. Prog. Neuropsychopharmacol. Biol. Psychiatry 2013, http://dx.doi.org/10.1016/j.pnpbp.2013.07.020.
58. Rubino T., Vigano D., Realini N., Guidali C., Braida D., Capurro V., Castiglioni C., Cherubino F., Romualdi P., Candeletti S., Sala M., Parolaro D. Chronic delta 9-tetrahydrocannabinol during adolescence provokes sex-dependent changes in the emotional profile in adult rats: behavioral and biochemical correlates. Neuropsychopharmacology 2008, 33:2760-2771.
59. Sano K., Koushi E., Irie K., Higuchi S., Tsuchihashi R., Kinjo J., Egashira N., Oishi R., Uchida N., Nagai H., Nishimura R., Tanaka H., Morimoto S., Mishima K., Iwasaki K., Fujiwara M. Delta(9)-tetrahydrocannabinol enhances an increase of plasma corticosterone levels induced by forced swim-stress. Biol. Pharm. Bull. 2009, 32:2065-2067.
60. Sanudo-Pena M.C., Romero J., Seale G.E., Fernandez-Ruiz J.J., Walker J.M. Activational role of cannabinoids on movement. Eur. J. Pharmacol. 2000, 391:269-274.
61. Sanudo-Pena M.C., Tsou K., Delay E.R., Hohman A.G., Force M., Walker J.M. Endogenous cannabinoids as an aversive or counter-rewarding system in the rat. Neurosci. Lett. 1997, 223:125-128.
62. Schneider M., Drews E., Koch M. Behavioral effects in adult rats of chronic prepubertal treatment with the cannabinoid receptor agonist WIN 55,212-2. Behav. Pharmacol. 2005, 16:447-454.
63. Schneider M., Koch M. Chronic pubertal, but not adult chronic cannabinoid treatment impairs sensorimotor gating, recognition memory, and the performance in a progressive ratio task in adult rats. Neuropsychopharmacology 2003, 28:1760-1769.
64. Schramm-Sapyta N.L., Cha Y.M., Chaudhry S., Wilson W.A., Swartzwelder H.S., Kuhn C.M. Differential anxiogenic, aversive, and locomotor effects of THC in adolescent and adult rats. Psychopharmacology (Berl) 2007, 191:867-877.
65. Solinas M., Panlilio L.V., Goldberg S.R. Exposure to delta-9-tetrahydrocannabinol (THC) increases subsequent heroin taking but not heroin's reinforcing efficacy: a self-administration study in rats. Neuropsychopharmacology 2004, 29:1301-1311.
66. Solinas M., Panlilio L.V., Tanda G., Makriyannis A., Matthews S.A., Goldberg S.R. Cannabinoid agonists but not inhibitors of endogenous cannabinoid transport or metabolism enhance the reinforcing efficacy of heroin in rats. Neuropsychopharmacology 2005, 30:2046-2057.
67. Stine S.M., Southwick S.M., Petrakis I.L., Kosten T.R., Charney D.S., Krystal J.H. Yohimbine-induced withdrawal and anxiety symptoms in opioid-dependent patients. Biol. Psychiatry 2002, 51:642-651.
68. Szabo B., Siemes S., Wallmichrath I. Inhibition of GABAergic neurotransmission in the ventral tegmental area by cannabinoids. Eur. J. Neurosci. 2002, 15:2057-2061.
69. Tomasiewicz H.C., Jacobs M.M., Wilkinson M.B., Wilson S.P., Nestler E.J., Hurd Y.L. Proenkephalin mediates the enduring effects of adolescent cannabis exposure associated with adult opiate vulnerability. Biol. Psychiatry 2012, 72:803-810.
70. Tournier M., Sorbara F., Gindre C., Swendsen J.D., Verdoux H. Cannabis use and anxiety in daily life: a naturalistic investigation in a non-clinical population. Psychiatry Res. 2003, 118:1-8.
71. Tzavara E.T., Wade M., Nomikos G.G. Biphasic effects of cannabinoids on acetylcholine release in the hippocampus: site and mechanism of action. J. Neurosci. 2003, 23:9374-9384.
72. Umhau J.C., Schwandt M.L., Usala J., Geyer C., Singley E., George D.T., Heilig M. Pharmacologically induced alcohol craving in treatment seeking alcoholics correlates with alcoholism severity, but is insensitive to acamprosate. Neuropsychopharmacology 2011, 36:1178-1186.
73. Veen N.D., Selten J.P., van der Tweel I., Feller W.G., Hoek H.W., Kahn R.S. Cannabis use and age at onset of schizophrenia. Am. J. Psychiatry 2004, 161:501-506.
74. Verdurand M., Nguyen V., Stark D., Zahra D., Gregoire M.C., Greguric I., Zavitsanou K. Comparison of cannabinoid CB(1) receptor binding in adolescent and adult rats: a positron emission tomography study using [F]MK-9470. Int. J. Mol. Imaging 2011, 2011:548123.
75. Viveros M.P., Llorente R., Suarez J., Llorente-Berzal A., Lopez-Gallardo M., de Fonseca F.R. The endocannabinoid system in critical neurodevelopmental periods: sex differences and neuropsychiatric implications. J. Psychopharmacol. 2012, 26:164-176.
76. Viveros M.P., Marco E.M., File S.E. Endocannabinoid system and stress and anxiety responses. Pharmacol. Biochem. Behav. 2005, 81:331-342.
77. Weinstein A., Brickner O., Lerman H., Greemland M., Bloch M., Lester H., Chisin R., Sarne Y., Mechoulam R., Bar-Hamburger R., Freedman N., Even-Sapir E. A study investigating the acute dose-response effects of 13mg and 17mg Delta 9- tetrahydrocannabinol on cognitive-motor skills, subjective and autonomic measures in regular users of marijuana. J. Psychopharmacol. 2008, 22:441-451.
78. Wiley J.L., Evans R.L., Grainger D.B., Nicholson K.L. Age-dependent differences in sensitivity and sensitization to cannabinoids and 'club drugs' in male adolescent and adult rats. Addict. Biol. 2008, 13:277-286.
79. Williams C.M., Kirkham T.C. Observational analysis of feeding induced by Delta9-THC and anandamide. Physiol. Behav. 2002, 76:241-250.
80. Wu X., French E.D. Effects of chronic delta9-tetrahydrocannabinol on rat midbrain dopamine neurons: an electrophysiological assessment. Neuropharmacology 2000, 39:391-398.