Trajectory of adolescent cannabis use on addiction vulnerability

Neuropharmacology

Volumn 76, Issue PART B, 2014, Pages 416-424

  Hurd, Yasmin L ^a,b   Michaelides, Michael ^a   Miller, Michael L ^a   Jutras Aswad, Didier ^c,d  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b Geriatric Research Education and Clinical Care Center   (United States)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

^d CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Cannabinoid; Marijuana; Nucleus accumbens; Opioid neuropeptide; Prefrontal cortex

Indexed keywords

ENDOCANNABINOID;

ADOLESCENT; ADOLESCENT BEHAVIOR; BRAIN; CANNABIS ADDICTION; DRUG EXPOSURE; GENETIC TRAIT; GENETICS; HUMAN; LEGAL ASPECT; PERCEPTION; PERSONALITY; POLICY; PRIORITY JOURNAL; REVIEW; VULNERABLE POPULATION;

CANNABINOID; MARIJUANA; NUCLEUS ACCUMBENS; OPIOID NEUROPEPTIDE; PREFRONTAL CORTEX;

ADOLESCENT; BRAIN; CANNABINOIDS; HUMANS; MARIJUANA ABUSE;

EID: 84887077990     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2013.07.028     Document Type: Review

References (123)

1. A. Agrawal, and M.T. Lynskey Candidate genes for cannabis use disorders: Findings, challenges and directions Addiction 104 2009 518 532
2. A. Agrawal, M.C. Neale, C.A. Prescott, and K.S. Kendler Cannabis and other illicit drugs: Comorbid use and abuse/dependence in males and females Behav. Genet. 34 2004 217 228 (Pubitemid 38437619)
3. A. Agrawal, L. Wetherill, D.M. Dick, X. Xuei, A. Hinrichs, V. Hesselbrock, J. Kramer, J.I. Nurnberger Jr., M. Schuckit, L.J. Bierut, H.J. Edenberg, and T. Foroud Evidence for association between polymorphisms in the cannabinoid receptor 1 (CNR1) gene and cannabis dependence Am. J. Med. Genet. B Neuropsychiatr. Genet. 150B 2009 736 740
4. M. Arendt, R. Rosenberg, L. Fjordback, J. Brandholdt, L. Foldager, L. Sher, and P. Munk-Jorgensen Testing the self-medication hypothesis of depression and aggression in cannabis-dependent subjects Psychol. Med. 37 2007 935 945 (Pubitemid 46993594)
5. R.C. Belue, A.C. Howlett, T.M. Westlake, and D.E. Hutchings The ontogeny of cannabinoid receptors in the brain of postnatal and aging rats Neurotoxicol. Teratol. 17 1995 25 30
6. A. Biegon, and I.A. Kerman Autoradiographic study of pre- and postnatal distribution of cannabinoid receptors in human brain Neuroimage 14 2001 1463 1468 (Pubitemid 33124194)
7. M. Biscaia, B. Fernandez, A. Higuera-Matas, M. Miguens, M.P. Viveros, C. Garcia-Lecumberri, and E. Ambrosio Sex-dependent effects of periadolescent exposure to the cannabinoid agonist CP-55,940 on morphine self-administration behaviour and the endogenous opioid system Neuropharmacology 54 2008 863 873
8. M. Biscaia, S. Marin, B. Fernandez, E.M. Marco, M. Rubio, C. Guaza, E. Ambrosio, and M.P. Viveros 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) 170 2003 301 308 (Pubitemid 37491610)
9. L.C. Blume, C.E. Bass, S.R. Childers, G.D. Dalton, D.C. Roberts, J.M. Richardson, R. Xiao, D.E. Selley, and A.C. Howlett Striatal CB1 and D2 receptors regulate expression of each other, CRIP1A and delta opioid systems J. Neurochem. 124 2013 808 820
10. J.S. Brook, E.B. Balka, and M. Whiteman The risks for late adolescence of early adolescent marijuana use Am. J. Public Health 89 1999 1549 1554 (Pubitemid 29457910)
11. J.S. Brook, L. Richter, M. Whiteman, and P. Cohen Consequences of adolescent marijuana use: Incompatibility with the assumption of adult roles Genet. Soc. Gen. Psychol. Monogr. 125 1999 193 207
12. M. Canals, and G. Milligan Constitutive activity of the cannabinoid CB1 receptor regulates the function of co-expressed Mu opioid receptors J. Biol. Chem. 283 2008 11424 11434
13. R. Ciccocioppo, L. Antonelli, M. Biondini, M. Perfumi, P. Pompei, and M. Massi Memory impairment following combined exposure to delta(9)- tetrahydrocannabinol and ethanol in rats Eur. J. Pharmacol. 449 2002 245 252
14. H.H. Cleveland, and R.P. Wiebe Understanding the association between adolescent marijuana use and later serious drug use: Gateway effect or developmental trajectory? Dev. Psychopathol. 20 2008 615 632 (Pubitemid 351584027)
15. J. Corchero, L. Garcia-Gil, J. Manzanares, J.J. Fernandez-Ruiz, J.A. Fuentes, and J.A. Ramos Perinatal delta9-tetrahydrocannabinol exposure reduces proenkephalin gene expression in the caudate-putamen of adult female rats Life Sci. 63 1998 843 850 (Pubitemid 28378323)
16. J. Corchero, J. Romero, F. Berrendero, J. Fernandez-Ruiz, J.A. Ramos, J.A. Fuentes, and J. Manzanares Time-dependent differences of repeated administration with Delta9-tetrahydrocannabinol in proenkephalin and cannabinoid receptor gene expression and G-protein activation by mu-opioid and CB1-cannabinoid receptors in the caudate-putamen Brain Res. Mol. Brain Res. 67 1999 148 157 (Pubitemid 29170077)
17. H.E. Creemers, Z. Harakeh, D.M. Dick, J. Meyers, W.A. Vollebergh, J. Ormel, F.C. Verhulst, and A.C. Huizink DRD2 and DRD4 in relation to regular alcohol and cannabis use among adolescents: Does parenting modify the impact of genetic vulnerability? the TRAILS study Drug Alcohol Depend. 115 2011 35 42
18. J.A. DiNieri, X. Wang, H. Szutorisz, S.M. Spano, J. Kaur, P. Casaccia, D. Dow-Edwards, and Y.L. Hurd Maternal cannabis use alters ventral striatal dopamine D2 gene regulation in the offspring Biol. Psychiatry 70 2011 763 769
19. G. Dorard, S. Berthoz, O. Phan, M. Corcos, and C. Bungener Affect dysregulation in cannabis abusers: A study in adolescents and young adults Eur. Child Adolescent Psychiatry 17 2008 274 282
20. D. Dow-Edwards, and S. Izenwasser Pretreatment with Delta9- tetrahydrocannabinol (THC) increases cocaine-stimulated activity in adolescent but not adult male rats Pharmacol. Biochem. Behav. 100 2012 587 591
21. P.F. Durieux, B. Bearzatto, S. Guiducci, T. Buch, A. Waisman, M. Zoli, S.N. Schiffmann, and A. de Kerchove d'Exaerde D2R striatopallidal neurons inhibit both locomotor and drug reward processes Nat. Neurosci. 12 2009 393 395
22. M. Ellgren, A. Artmann, O. Tkalych, A. Gupta, H.S. Hansen, S.H. Hansen, L.A. Devi, and Y.L. Hurd Dynamic changes of the endogenous cannabinoid and opioid mesocorticolimbic systems during adolescence: THC effects Eur. Neuropsychopharmacol. 18 2008 826 834
23. M. Ellgren, Y.L. Hurd, and J. Franck Amphetamine effects on dopamine levels and behavior following cannabinoid exposure during adolescence Eur. J. Pharmacol. 497 2004 205 213 (Pubitemid 39092574)
24. M. Ellgren, S.M. Spano, and Y.L. Hurd Adolescent cannabis exposure alters opiate intake and opioid limbic neuronal populations in adult rats Neuropsychopharmacology 32 2007 607 615
25. R.F. Ferdinand, F. Sondeijker, J. van der Ende, J.P. Selten, A. Huizink, and F.C. Verhulst Cannabis use predicts future psychotic symptoms, and vice versa Addiction 100 2005 612 618 (Pubitemid 40646286)
26. D.M. Fergusson, and J.M. Boden Cannabis use and later life outcomes Addiction 103 2008 969 976 Discussion 977-968 (Pubitemid 351703484)
27. D.M. Fergusson, J.M. Boden, and L.J. Horwood Cannabis use and other illicit drug use: Testing the cannabis gateway hypothesis Addiction 101 2006 556 569 (Pubitemid 43375619)
28. D.M. Fergusson, and L.J. Horwood Does cannabis use encourage other forms of illicit drug use? Addiction 95 2000 505 520 (Pubitemid 30220246)
29. D.M. Fergusson, L.J. Horwood, and N. Swain-Campbell Cannabis use and psychosocial adjustment in adolescence and young adulthood Addiction 97 2002 1123 1135
30. M.J. Frank, and K. Hutchison Genetic contributions to avoidance-based decisions: Striatal D2 receptor polymorphisms Neuroscience 164 2009 131 140
31. M.J. Frank, A.A. Moustafa, H.M. Haughey, T. Curran, and K.E. Hutchison Genetic triple dissociation reveals multiple roles for dopamine in reinforcement learning Proc. Natl. Acad. Sci. U. S. A. 104 2007 16311 16316 (Pubitemid 350099356)
32. C.M. Gerard, C. Mollereau, G. Vassart, and M. Parmentier Molecular cloning of a human cannabinoid receptor which is also expressed in testis Biochem. J. 279 Pt 1 1991 129 134
33. C.R. Gerfen, T.M. Enber, Z. Susel, T.N. Chase, F.J. Monsma, L.C. Mahan, and D.R. Sibley D1 and D2 dopamine receptor regulated gene expression of striatonigral and striatopallidal neurons Science 250 1990 1429 1432 (Pubitemid 120031867)
34. C.R. Gerfen, and W.S. Young III Distribution of striatonigral and striatopallidal peptidergic neurons in both patch and matrix compartments: An in situ hybridization histochemistry and fluorescent retrograde tracing study Brain Res. 460 1988 161 167
35. M. Glass, M. Dragnunow, and R.L. Faull Cannabinoid receptors in the human brain: A detailed anatomical quantitative autoradiographic study in the fetal, neonatal and adult human brain Neurosci 77 1997 299 318 (Pubitemid 27079604)
36. J.P. Gong, E.S. Onaivi, H. Ishiguro, Q.R. Liu, P.A. Tagliaferro, A. Brusco, and G.R. Uhl Cannabinoid CB2 receptors: Immunohistochemical localization in rat brain Brain Res. 1071 2006 10 23 (Pubitemid 43255471)
37. G. Griffin, Q. Tao, and M.E. Abood Cloning and pharmacological characterization of the rat CB(2) cannabinoid receptor J. Pharmacol. Exp. Ther. 292 2000 886 894 (Pubitemid 30136579)
38. W.D. Hall, and M. Lynskey Is cannabis a gateway drug? Testing hypotheses about the relationship between cannabis use and the use of other illicit drugs Drug Alcohol Rev. 24 2005 39 48 (Pubitemid 41052845)
39. T. Harkany, E. Keimpema, K. Barabas, and J. Mulder Endocannabinoid functions controlling neuronal specification during brain development Mol. Cell Endocrinol. 286 2008 S84 S90
40. M.R. Hayatbakhsh, J.M. Najman, K. Jamrozik, A.A. Mamun, R. Alati, and W. Bor Cannabis and anxiety and depression in young adults: A large prospective study J. Am. Acad. Child Adolesc. Psychiatry 46 2007 408 417
41. A. Heinz, T. Siessmeier, J. Wrase, D. Hermann, S. Klein, S.M. Grusser, H. Flor, D.F. Braus, H.G. Buchholz, G. Grunder, M. Schreckenberger, M.N. Smolka, F. Rosch, K. Mann, and P. Bartenstein Correlation between dopamine D(2) receptors in the ventral striatum and central processing of alcohol cues and craving Am. J. Psychiatry 161 2004 1783 1789 (Pubitemid 39314671)
42. L. Heng, J.A. Beverley, H. Steiner, and K.Y. Tseng Differential developmental trajectories for CB1 cannabinoid receptor expression in limbic/associative and sensorimotor cortical areas Synapse 65 2011 278 286
43. M. Herkenham, A. Lynn, M. Little, M. Johnson, L. Melvin, B. De Costa, and K. Rice Cannabinoid receptor localization in brain Proc. Natl. Acad. Sci. U. S. A. 87 1990 1932
44. M. Herkenham, A.B. Lynn, B.R. de Costa, and E.K. Richfield Neuronal localization of cannabinoid receptors in the basal ganglia of the rat Brain Res. 547 1991 267 274
45. M. Herkenham, A.B. Lynn, M.R. Johnson, L.S. Melvin, B.R. de Costa, and K.C. Rice Characterization and localization of cannabinoid receptors in rat brain: A quantitative in vitro autoradiographic study J. Neurosci. The Off. J. Soc. Neurosci. 11 1991 563 583
46. D.J. Hermanson, and L.J. Marnett Cannabinoids, endocannabinoids, and cancer Cancer Metastasis Rev. 30 2011 599 612
47. A. Higuera-Matas, M.L. Soto-Montenegro, N. del Olmo, M. Miguens, I. Torres, J.J. Vaquero, J. Sanchez, C. Garcia-Lecumberri, M. Desco, and E. Ambrosio Augmented acquisition of cocaine self-administration and altered brain glucose metabolism in adult female but not male rats exposed to a cannabinoid agonist during adolescence Neuropsychopharmacology 33 2008 806 813 (Pubitemid 351252702)
48. T. Hikida, K. Kimura, N. Wada, K. Funabiki, and S. Nakanishi Distinct roles of synaptic transmission in direct and indirect striatal pathways to reward and aversive behavior Neuron 66 2010 896 907
49. A.J. Hill, C.M. Williams, B.J. Whalley, and G.J. Stephens Phytocannabinoids as novel therapeutic agents in CNS disorders Pharmacol. Ther. 133 2012 79 97
50. E.L. Hill, T. Gallopin, I. Ferezou, B. Cauli, J. Rossier, P. Schweitzer, and B. Lambolez Functional CB1 receptors are broadly expressed in neocortical GABAergic and glutamatergic neurons J. Neurophysiol. 97 2007 2580 2589 (Pubitemid 46557693)
51. C.J. Hopfer, S.E. Young, S. Purcell, T.J. Crowley, M.C. Stallings, R.P. Corley, S.H. Rhee, A. Smolen, K. Krauter, J.K. Hewitt, and M.A. Ehringer Cannabis receptor haplotype associated with fewer cannabis dependence symptoms in adolescents Am. J. Med. Genet. B Neuropsychiatr. Genet. 141B 2006 895 901 (Pubitemid 44905444)
52. A.C. Howlett, F. Barth, T.I. Bonner, G. Cabral, P. Casellas, W.A. Devane, C.C. Felder, M. Herkenham, K. Mackie, B.R. Martin, R. Mechoulam, and R.G. Pertwee International Union of Pharmacology. XXVII. Classification of cannabinoid receptors Pharmacol. Rev. 54 2002 161 202 (Pubitemid 34575709)
53. S.M. Hyman, and R. Sinha Stress-related factors in cannabis use and misuse: Implications for prevention and treatment J. Subst. Abuse Treat 36 2009 400 413
54. L.D. Johnston, P.M. O'Malley, J.G. Bachman, and J.E. Schulenberg Monitoring the Future National Results on Adolescent Drug Use: Overview of Key Findings, 2011 2012 Institute for Social Research, The University of Michigan. Ann Arbor
55. D. Jutras-Aswad, M.M. Jacobs, G. Yiannoulos, P. Roussos, P. Bitsios, Y. Nomura, X. Liu, and Y.L. Hurd Cannabis-dependence risk relates to synergism between neuroticism and proenkephalin SNPs associated with amygdala gene expression: Case-control study PloS One 7 2012 e39243
56. D. Kandel Stages in adolescent involvement in drug use Science 190 1975 912 914
57. D.B. Kandel, K. Yamaguchi, and L.C. Klein Testing the gateway hypothesis Addiction 101 2006 470 472 Discussion 474-476 (Pubitemid 43375608)
58. W. Kang, S.P. Wilson, and M.A. Wilson Overexpression of proenkephalin in the amygdala potentiates the anxiolytic effects of benzodiazepines Neuropsychopharmacol. Off. Publ. Am. Coll. Neuropsychopharmacol. 22 2000 77 88
59. I. Katona, and T.F. Freund Endocannabinoid signaling as a synaptic circuit breaker in neurological disease Nat. Med. 14 2008 923 930
60. A.E. Kelley, V.P. Bakshi, S.N. Haber, T.L. Steininger, M.J. Will, and M. Zhang Opioid modulation of taste hedonics within the ventral striatum Physiol. Behav. 76 2002 365 377 (Pubitemid 34765590)
61. K.S. Kendler, L.M. Karkowski, M.C. Neale, and C.A. Prescott Illicit psychoactive substance use, heavy use, abuse, and dependence in a US population-based sample of male twins Arch. Gen. Psychiatry 57 2000 261 269 (Pubitemid 30140435)
62. K.S. Kendler, and C.A. Prescott Cannabis use, abuse, and dependence in a population-based sample of female twins Am. J. Psychiatry 155 1998 1016 1022 (Pubitemid 28357724)
63. J.R. Kilmer, S.B. Hunt, C.M. Lee, and C. Neighbors Marijuana use, risk perception, and consequences: Is perceived risk congruent with reality? Addict Behav. 32 2007 3026 3033 (Pubitemid 47470104)
64. T.A. Klein, J. Neumann, M. Reuter, J. Hennig, D.Y. von Cramon, and M. Ullsperger Genetically determined differences in learning from errors Science 318 2007 1642 1645 (Pubitemid 350233666)
65. J. Koskinen, J. Lohonen, H. Koponen, M. Isohanni, and J. Miettunen Rate of cannabis use disorders in clinical samples of patients with schizophrenia: A meta-analysis Schizophr. Bull. 36 2010 1115 1130
66. J.C. Kung, T.C. Chen, B.C. Shyu, S. Hsiao, and A.C. Huang Anxiety- and depressive-like responses and c-fos activity in preproenkephalin knockout mice: Oversensitivity hypothesis of enkephalin deficit-induced posttraumatic stress disorder J. Biomed. Sci. 17 2010 29
67. J.L. Lanciego, P. Barroso-Chinea, A.J. Rico, L. Conte-Perales, L. Callen, E. Roda, V. Gomez-Bautista, I.P. Lopez, C. Lluis, J.L. Labandeira-Garcia, and R. Franco Expression of the mRNA coding the cannabinoid receptor 2 in the pallidal complex of Macaca fascicularis J. Psychopharmacol. 25 2011 97 104
68. C. Le Moine, E. Normand, A.F. Guitteny, B. Fouque, R. Teoule, and B. Bloch Dopamine receptor gene expression by enkephalin neurons in rat forebrain Proc. Natl. Acad. Sci. U. S. A. 87 1990 230 234
69. J.M. Lessem, C.J. Hopfer, B.C. Haberstick, D. Timberlake, M.A. Ehringer, A. Smolen, and J.K. Hewitt Relationship between adolescent marijuana use and young adult illicit drug use Behav. Genet. 36 2006 498 506 (Pubitemid 43967646)
70. C. Lopez-Quintero, and Y. Neumark Effects of risk perception of marijuana use on marijuana use and intentions to use among adolescents in Bogota, Colombia Drug Alcohol Depend. 109 2010 65 72
71. M.T. Lynskey, C. Coffey, L. Degenhardt, J.B. Carlin, and G. Patton A longitudinal study of the effects of adolescent cannabis use on high school completion Addiction 98 2003 685 692 (Pubitemid 36638207)
72. R.J. Maccoun Competing accounts of the gateway effect: The field thins, but still no clear winner Addiction 101 2006 473 474 Discussion 474-476
73. H.H. Maes, C.E. Woodard, L. Murrelle, J.M. Meyer, J.L. Silberg, J.K. Hewitt, M. Rutter, E. Simonoff, A. Pickles, R. Carbonneau, M.C. Neale, and L.J. Eaves Tobacco, alcohol and drug use in eight- to sixteen-year-old twins: The Virginia twin study of adolescent behavioral development J. Stud. Alcohol 60 1999 293 305 (Pubitemid 29214829)
74. P. Mailleux, M. Parmentier, and J.J. Vanderhaeghen Distribution of cannabinoid receptor messenger RNA in the human brain: An in situ hybridization histochemistry with oligonucleotides Neurosci. Lett. 143 1992 200 204
75. G. Marsicano, and B. Lutz Expression of the cannabinoid receptor CB1 in distinct neuronal subpopulations in the adult mouse forebrain Eur. J. Neurosci. 11 1999 4213 4225 (Pubitemid 30009252)
76. S. Mato, E. Del Olmo, and A. Pazos Ontogenetic development of cannabinoid receptor expression and signal transduction functionality in the human brain Eur. J. Neurosci. 17 2003 1747 1754 (Pubitemid 36645324)
77. L.A. Matsuda, T.I. Bonner, and S.J. Lolait Localization of cannabinoid receptor mRNA in rat brain J. Comp. Neurol. 327 1993 535 550 (Pubitemid 23033649)
78. L.A. Matsuda, S.J. Lolait, M.J. Brownstein, A.C. Young, and T.I. Bonner Structure of a cannabinoid receptor and functional expression of the cloned cDNA Nature 346 1990 561 564
79. M. McGue, I. Elkins, and W.G. Iacono Genetic and environmental influences on adolescent substance use and abuse Am. J. Med. Genet. 96 2000 671 677
80. C.R. McLaughlin, B.R. Martin, D.R. Compton, and M.E. Abood Cannabinoid receptors in developing rats: Detection of mRNA and receptor binding Drug and Alcohol Depend. 36 1994 27 31 (Pubitemid 24253613)
81. M. Michaelides, P.K. Thanos, R. Kim, J. Cho, M. Ananth, G.J. Wang, and N.D. Volkow PET imaging predicts future body weight and cocaine preference Neuroimage 59 2012 1508 1513
82. D.R. Miles, M.B. van den Bree, A.E. Gupman, D.B. Newlin, M.D. Glantz, and R.W. Pickens A twin study on sensation seeking, risk taking behavior and marijuana use Drug Alcohol Depend. 62 2001 57 68 (Pubitemid 32149965)
83. L.J. Morel, B. Giros, and V. Dauge Adolescent exposure to chronic delta-9-tetrahydrocannabinol blocks opiate dependence in maternally deprived rats Neuropsychopharmacology 34 2009 2469 2476
84. D. Morgan, K.A. Grant, H.D. Gage, R.H. Mach, J.R. Kaplan, O. Prioleau, S.H. Nader, N. Buchheimer, R.L. Ehrenkaufer, and M.A. Nader Social dominance in monkeys: Dopamine D2 receptors and cocaine self-administration Nat. Neurosci. 5 2002 169 174 (Pubitemid 34121585)
85. J. Mulder, T. Aguado, E. Keimpema, K. Barabas, C.J. Ballester Rosado, L. Nguyen, K. Monory, G. Marsicano, V. Di Marzo, Y.L. Hurd, F. Guillemot, K. Mackie, B. Lutz, M. Guzman, H.C. Lu, I. Galve-Roperh, and T. Harkany Endocannabinoid signaling controls pyramidal cell specification and long-range axon patterning Proc. Natl. Acad. Sci. U. S. A. 105 2008 8760 8765 (Pubitemid 351987753)
86. S. Munro, K.L. Thomas, and M. Abu-Shaar Molecular characterization of a peripheral receptor for cannabinoids Nature 365 1993 61 65 (Pubitemid 23305569)
87. M.A. Nader, D. Morgan, H.D. Gage, S.H. Nader, T.L. Calhoun, N. Buchheimer, R. Ehrenkaufer, and R.H. Mach PET imaging of dopamine D2 receptors during chronic cocaine self-administration in monkeys Nat. Neurosci. 9 2006 1050 1056 10.1038/nn1737 (Pubitemid 44264918)
88. E.S. Onaivi, H. Ishiguro, J.P. Gong, S. Patel, A. Perchuk, P.A. Meozzi, L. Myers, Z. Mora, P. Tagliaferro, E. Gardner, A. Brusco, B.E. Akinshola, Q.R. Liu, B. Hope, S. Iwasaki, T. Arinami, L. Teasenfitz, and G.R. Uhl Discovery of the presence and functional expression of cannabinoid CB2 receptors in brain Ann. N. Y. Acad. Sci. 1074 2006 514 536 (Pubitemid 44532857)
89. L.V. Panlilio, M. Solinas, S.A. Matthews, and S.R. Goldberg Previous exposure to THC alters the reinforcing efficacy and anxiety-related effects of cocaine in rats Neuropsychopharmacology 32 2007 646 657
90. G.C. Patton, C. Coffey, J.B. Carlin, L. Degenhardt, M. Lynskey, and W. Hall Cannabis use and mental health in young people: Cohort study BMJ 325 2002 1195 1198 (Pubitemid 35398781)
91. A. Perez-Rosado, J. Manzanares, J. Fernandez-Ruiz, and J.A. Ramos Prenatal Delta(9)-tetrahydrocannabinol exposure modifies proenkephalin gene expression in the fetal rat brain: Sex-dependent differences Brain Res. Dev. Brain Res. 120 2000 77 81 (Pubitemid 30155868)
92. D.A. Pettit, M.P. Harrison, J.M. Olson, R.F. Spencer, and G.A. Cabral Immunohistochemical localization of the neural cannabinoid receptor in rat brain J. Neurosci. Res. 51 1998 391 402 (Pubitemid 28078470)
93. M. Pistis, S. Perra, G. Pillolla, M. Melis, A.L. Muntoni, and G.L. Gessa Adolescent exposure to cannabinoids induces long-lasting changes in the response to drugs of abuse of rat midbrain dopamine neurons Biol. Psychiatry 56 2004 86 94 (Pubitemid 38849412)
94. S.H. Rhee, J.K. Hewitt, S.E. Young, R.P. Corley, T.J. Crowley, and M.C. Stallings Genetic and environmental influences on substance initiation, use, and problem use in adolescents Arch. Gen. Psychiatry 60 2003 1256 1264 (Pubitemid 37494079)
95. F. Rodriguez de Fonseca, J.A. Ramos, A. Bonnin, and J.J. Fernández-Ruiz Presence of cannabinoid binding sites in the brain from early postnatal ages Neuroreport 4 1993 135 138 (Pubitemid 23080859)
96. J.T. Sakai, C.J. Hopfer, C. Hartman, B.C. Haberstick, A. Smolen, R.P. Corley, M.C. Stallings, S.E. Young, D. Timberlake, J.K. Hewitt, and T.J. Crowley Test of association between TaqIA A1 allele and alcohol use disorder phenotypes in a sample of adolescent patients with serious substance and behavioral problems Drug Alcohol Depend. 88 2007 130 137 (Pubitemid 46482814)
97. SAMHSA Results from the 2010 National Survey on Drug Use and Health: National Findings 2011 Office of Applied Studies, NSDUH Series H-41, HHS Publication No. (SMA) 11-4658 Rockville, MD
98. H. Sano, Y. Yasoshima, N. Matsushita, T. Kaneko, K. Kohno, I. Pastan, and K. Kobayashi Conditional ablation of striatal neuronal types containing dopamine D2 receptor disturbs coordination of basal ganglia function J. Neurosci. 23 2003 9078 9088 (Pubitemid 37243808)
99. M.E. Singh, I.S. McGregor, and P.E. Mallet Perinatal exposure to delta(9)-tetrahydrocannabinol alters heroin-induced place conditioning and fos-immunoreactivity Neuropsychopharmacol. Off. Publ. Am. Coll. Neuropsychopharmacol. 31 2006 58 69 (Pubitemid 43250941)
100. P.D. Skoubis, H.A. Lam, J. Shoblock, S. Narayanan, and N.T. Maidment Endogenous enkephalins, not endorphins, modulate basal hedonic state in mice Eur. J. Neurosci. 21 2005 1379 1384 (Pubitemid 40516636)
101. M.S. Spano, M. Ellgren, X. Wang, and Y.L. Hurd Prenatal cannabis exposure increases heroin seeking with allostatic changes in limbic enkephalin systems in adulthood Biol. Psychiatry 61 2007 554 563 (Pubitemid 46185333)
102. M.S. Spano, P. Fadda, W. Fratta, and L. Fattore Cannabinoid-opioid interactions in drug discrimination and self-administration: Effect of maternal, postnatal, adolescent and adult exposure to the drugs Curr. Drug Targets 11 2010 450 461
103. R.E. Tarter, M. Vanyukov, L. Kirisci, M. Reynolds, and D.B. Clark Predictors of marijuana use in adolescents before and after licit drug use: Examination of the gateway hypothesis Am. J. Psychiatry 163 2006 2134 2140 (Pubitemid 46114234)
104. P.K. Thanos, M. Michaelides, H. Benveniste, G.J. Wang, and N.D. Volkow The effects of cocaine on regional brain glucose metabolism is attenuated in dopamine transporter knockout mice Synapse 62 2008 319 324 (Pubitemid 351451799)
105. H.C. Tomasiewicz, M.M. Jacobs, M.B. Wilkinson, S.P. Wilson, E.J. Nestler, and Y.L. Hurd Proenkephalin mediates the enduring effects of adolescent cannabis exposure associated with adult opiate vulnerability Biol. Psychiatry 72 2012 803 810
106. M.T. Tsuang, M.J. Lyons, J.M. Meyer, T. Doyle, S.A. Eisen, J. Goldberg, W. True, N. Lin, R. Toomey, and L. Eaves Co-occurrence of abuse of different drugs in men: The role of drug-specific and shared vulnerabilities Arch. Gen. Psychiatry 55 1998 967 972 (Pubitemid 28506837)
107. J.S. Tucker, P.L. Ellickson, R.L. Collins, and D.J. Klein Are drug experimenters better adjusted than abstainers and users?: A longitudinal study of adolescent marijuana use J. Adolesc. Health 39 2006 488 494 (Pubitemid 44375039)
108. R.F. Tyndale, J.I. Payne, A.L. Gerber, and J.C. Sipe The fatty acid amide hydrolase C385A (P129T) missense variant in cannabis users: Studies of drug use and dependence in Caucasians Am. J. Med. Genet. B Neuropsychiatr. Genet. 144B 2007 660 666 (Pubitemid 47077151)
109. O. Valverde, F. Noble, F. Beslot, V. Dauge, M.C. Fournie-Zaluski, and B.P. Roques Delta9-tetrahydrocannabinol releases and facilitates the effects of endogenous enkephalins: Reduction in morphine withdrawal syndrome without change in rewarding effect Eur. J. Neurosci. 13 2001 1816 1824 (Pubitemid 32488071)
110. M.B. van den Bree, E.O. Johnson, M.C. Neale, and R.W. Pickens Genetic and environmental influences on drug use and abuse/dependence in male and female twins Drug Alcohol Depend. 52 1998 231 241 (Pubitemid 28529581)
111. W.A. van Gastel, J.H. Maccabe, C.D. Schubart, A. Vreeker, W. Tempelaar, R.S. Kahn, and M.P. Boks Cigarette smoking and cannabis use are equally strongly associated with psychotic-like experiences: A cross-sectional study in 1929 young adults Psychol. Med. 2013 1 9
112. M.D. Van Sickle, M. Duncan, P.J. Kingsley, A. Mouihate, P. Urbani, K. Mackie, N. Stella, A. Makriyannis, D. Piomelli, J.S. Davison, L.J. Marnett, V. Di Marzo, Q.J. Pittman, K.D. Patel, and K.A. Sharkey Identification and functional characterization of brainstem cannabinoid CB2 receptors Science 310 2005 329 332 (Pubitemid 41457202)
113. V. Van Waes, J.A. Beverley, H. Siman, K.Y. Tseng, and H. Steiner CB1 cannabinoid receptor expression in the striatum: Association with corticostriatal circuits and developmental regulation Front Pharmacol. 3 2012 21
114. M. Verdurand, V. Nguyen, D. Stark, D. Zahra, M.C. Gregoire, I. Greguric, and K. Zavitsanou 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
115. D. Vigano, T. Rubino, and D. Parolaro Molecular and cellular basis of cannabinoid and opioid interactions Pharmacol. Biochem. Behav. 81 2005 360 368 (Pubitemid 40807133)
116. N.D. Volkow, L. Chang, G.J. Wang, J.S. Fowler, Y.S. Ding, M. Sedler, J. Logan, D. Franceschi, J. Gatley, R. Hitzemann, A. Gifford, C. Wong, and N. Pappas Low level of brain dopamine D2 receptors in methamphetamine abusers: Association with metabolism in the orbitofrontal cortex Am. J. Psychiatry 158 2001 2015 2021 (Pubitemid 33104107)
117. N.D. Volkow, J.S. Fowler, G.J. Wang, and J.M. Swanson Dopamine in drug abuse and addiction: Results from imaging studies and treatment implications Mol. Psychiatry 9 2004 557 569 (Pubitemid 38850435)
118. N.D. Volkow, G.J. Wang, J.S. Fowler, J. Logan, S.J. Gatley, A. Gifford, R. Hitzemann, Y.S. Ding, and N. Pappas Prediction of reinforcing responses to psychostimulants in humans by brain dopamine D2 receptor levels Am. J. Psychiatry 156 1999 1440 1443 (Pubitemid 29416545)
119. G.J. Wang, N.D. Volkow, J.S. Fowler, J. Logan, N.N. Abumrad, R.J. Hitzemann, N.S. Pappas, and K. Pascani Dopamine D2 receptor availability in opiate-dependent subjects before and after naloxone-precipitated withdrawal Neuropsychopharmacol. Off. Publ. Am. Coll. Neuropsychopharmacol. 16 1997 174 182 (Pubitemid 27086432)
120. X. Wang, D. Dow-Edwards, V. Andersen, H. Minkoff, and Y.L. Hurd Discrete opioid gene expression impairment in the human fetal brain associated with maternal marijuana use Pharmacogenomic. J. 6 2006
121. X. Wang, D. Dow-Edwards, E. Keller, and Y.L. Hurd Preferential limbic expression of the cannabinoid receptor mRNA in the human fetal brain Neuroscience 118 2003 681 694 (Pubitemid 36506956)
122. K. Yamaguchi, and D.B. Kandel Patterns of drug use from adolescence to young adulthood: III. Predictors of progression Am. J. Public Health 74 1984 673 681 (Pubitemid 14119524)
123. M.J. Zvolensky, A.A. Vujanovic, A. Bernstein, M.O. Bonn-Miller, E.C. Marshall, and T.M. Leyro Marijuana use motives: A confirmatory test and evaluation among young adult marijuana users Addict. Behav. 32 2007 3122 3130 (Pubitemid 47464762)