Cannabis and the developing brain: Insights from behavior

European Journal of Pharmacology

Volumn 585, Issue 2-3, 2008, Pages 441-452

  Trezza, Viviana ^a   Cuomo, Vincenzo ^b   Vanderschuren, Louk J M J ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Adolescence; Behavior; Cannabis; Development; Pregnancy

Indexed keywords

2 ARACHIDONOYLGLYCEROL; 2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; 4 (1,1 DIMETHYLHEPTYL) 1',2',3',4',5',6' HEXAHYDRO 2,3' DIHYDROXY 6' (3 HYDROXYPROPYL)BIPHENYL; ANANDAMIDE; CANNABINOID RECEPTOR; CANNABIS; CYCLOHEXYLCARBAMIC ACID 3' CARBAMOYLBIPHENYL 3 YL ESTER; DRONABINOL; ENDOCANNABINOID; FATTY ACID AMIDASE INHIBITOR; OPIATE ANTAGONIST;

BEHAVIOR; BRAIN DEVELOPMENT; COGNITION; DRUG MECHANISM; EMOTION; HUMAN; MEMORY; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; REVIEW;

ADOLESCENT; ANIMALS; BEHAVIOR; BEHAVIOR, ANIMAL; BRAIN; CANNABIS; ENDOCANNABINOIDS; FEMALE; HUMANS; NEURONAL PLASTICITY; PREGNANCY; SYNAPTIC TRANSMISSION;

EID: 43049103458     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejphar.2008.01.058     Document Type: Review

References (159)

1. Agrawal A., Neale M.C., Prescott C.A., and Kendler K.S. A twin study of early cannabis use and subsequent use and abuse/dependence of other illicit drugs. Psychol. Med. 34 (2004) 1227-1237
2. Ameri A. The effects of cannabinoids on the brain. Prog. Neurobiol. 58 (1999) 315-348
3. Andreasson S., Allebeck P., Engstrom A., and Rydberg U. Cannabis and schizophrenia. A longitudinal study of Swedish conscripts. Lancet. 2 (1987) 1483-1486
4. Antonelli T., Tanganelli S., Tomasini M.C., Finetti S., Trabace L., Steardo L., Sabino V., Carratu M.R., Cuomo V., and Ferraro L. Long-term effects on cortical glutamate release induced by prenatal exposure to the cannabinoid receptor agonist (R)-(+)-[2,3-dihydro-5-methyl-3-(4-morpholinyl-methyl)pyrrolo[1,2,3-de]-1, 4-benzoxazin-6-yl]-1-naphthalenylmethanone: an in vivo microdialysis study in the awake rat. Neuroscience 124 (2004) 367-375
5. Antonelli T., Tomasini M.C., Tattoli M., Cassano T., Tanganelli S., Finetti S., Mazzoni E., Trabace L., Steardo L., Cuomo V., and Ferraro L. Prenatal exposure to the CB1 receptor agonist WIN 55,212-2 causes learning disruption associated with impaired cortical NMDA receptor function and emotional reactivity changes in rat offspring. Cereb. Cortex 15 (2005) 2013-2020
6. Araki W., and Wurtman R.J. Control of membrane phosphatidylcholine biosynthesis by diacylglycerol levels in neuronal cells undergoing neurite outgrowth. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 11946-11950
7. Arseneault L., Cannon M., Poulton R., Murray R., Caspi A., and Moffitt T.E. Cannabis use in adolescence and risk for adult psychosis: longitudinal prospective study. BMJ 325 (2002) 1212-1213
8. Bayley N. Bayley Scales of Infant Development (1969), The Psychological Corporation, New York, NY
9. Beltramo M., Stella N., Calignano A., Lin S.Y., Makriyannis A., and Piomelli D. Functional role of high-affinity anandamide transport, as revealed by selective inhibition. Science 277 (1997) 1094-1097
10. Berghuis P., Rajnicek A.M., Morozov Y.M., Ross R.A., Mulder J., Urban G.M., Monory K., Marsicano G., Matteoli M., Canty A., Irving A.J., Katona I., Yanagawa Y., Rakic P., Lutz B., Mackie K., and Harkany T. Hardwiring the brain: endocannabinoids shape neuronal connectivity. Science 316 (2007) 1212-1216
11. Berrendero F., Garcia-Gil L., Hernandez M.L., Romero J., Cebeira M., de Miguel R., Ramos J.A., and Fernandez-Ruiz J.J. Localization of mRNA expression and activation of signal transduction mechanisms for cannabinoid receptor in rat brain during fetal development. Development 125 (1998) 3179-3188
12. Berrendero F., Mendizabal V., Murtra P., Kieffer B.L., and Maldonado R. Cannabinoid receptor and WIN 55 212-2-stimulated [35S]-GTPgammaS binding in the brain of mu-, delta- and kappa-opioid receptor knockout mice. Eur. J. Neurosci. 18 (2003) 2197-2202
13. Berrendero F., Sepe N., Ramos J.A., Di Marzo V., and Fernandez-Ruiz J.J. Analysis of cannabinoid receptor binding and mRNA expression and endogenous cannabinoid contents in the developing rat brain during late gestation and early postnatal period. Synapse 33 (1999) 181-191
14. Bignami G. Economical test methods for developmental neurobehavioral toxicity. Environ. Health Perspect. 104 Suppl. 2 (1996) 285-298
15. Biscaia M., Marin S., Fernandez B., Marco E.M., Rubio M., Guaza C., Ambrosio E., and 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). 170 (2003) 301-308
16. Bonnin A., de Miguel R., Castro J.G., Ramos J.A., and Fernandez-Ruiz J.J. Effects of perinatal exposure to delta 9-tetrahydrocannabinol on the fetal and early postnatal development of tyrosine hydroxylase-containing neurons in rat brain. J. Mol. Neurosci. 7 (1996) 291-308
17. Boycott R. The Time is Right to Decriminalise Cannabis. The Independent on Sunday (28/9/1997)
18. Campolongo P., Trezza V., Cassano T., Gaetani S., Morgese M.G., Ubaldi M., Soverchia L., Antonelli T., Ferraro L., Massi M., Ciccocioppo R., and Cuomo V. Perinatal exposure to delta-9-tetrahydrocannabinol causes enduring cognitive deficits associated with alteration of cortical gene expression and neurotransmission in rats. Addict. Biol. 12 (2007) 485-495
19. Carlson G., Wang Y., and Alger B.E. Endocannabinoids facilitate the induction of LTP in the hippocampus. Nat. Neurosci. 5 (2002) 723-724
20. Caspi A., Moffitt T.E., Cannon M., McClay J., Murray R., Harrington H., Taylor A., Arseneault L., Williams B., Braithwaite A., Poulton R., and Craig I.W. Moderation of the effect of adolescent-onset cannabis use on adult psychosis by a functional polymorphism in the catechol-O-methyltransferase gene: longitudinal evidence of a gene × environment interaction. Biol. Psychiatry 57 (2005) 1117-1127
21. Castaldo P., Magi S., Gaetani S., Cassano T., Ferraro L., Antonelli T., Amoroso S., and Cuomo V. Prenatal exposure to the cannabinoid receptor agonist WIN55,212-2 increases glutamate uptake through overexpression of GLT1 and EAAC1 glutamate transporter subtypes in rat frontal cerebral cortex. Neuropharmacology 53 (2007) 369-378
22. Cha Y.M., Jones K.H., Kuhn C.M., Wilson W.A., and Swartzwelder H.S. Sex differences in the effects of delta9-tetrahydrocannabinol on spatial learning in adolescent and adult rats. Behav. Pharmacol. 18 (2007) 563-569
23. Cha Y.M., White A.M., Kuhn C.M., Wilson W.A., and Swartzwelder H.S. Differential effects of delta9-THC on learning in adolescent and adult rats. Pharmacol. Biochem. Behav. 83 (2006) 448-455
24. Chevaleyre V., and Castillo P.E. Endocannabinoid-mediated metaplasticity in the hippocampus. Neuron 43 (2004) 871-881
25. Chevaleyre V., Takahashi K.A., and Castillo P.E. Endocannabinoid-mediated synaptic plasticity in the CNS. Annu. Rev. Neurosci. 29 (2006) 37-76
26. Compton D.R., Rice K.C., De Costa B.R., Razdan R.K., Melvin L.S., Johnson M.R., and Martin B.R. Cannabinoid structure-activity relationships: correlation of receptor binding and in vivo activities. J. Pharmacol. Exp. Ther. 265 (1993) 218-226
27. Corchero J., Avila M.A., Fuentes J.A., and Manzanares J. delta-9-tetrahydrocannabinol increases prodynorphin and proenkephalin gene expression in the spinal cord of the rat. Life Sci. 61 (1997) PL 39-PL 43
28. Corchero J., Fuentes J.A., and Manzanares J. delta 9-tetrahydrocannabinol increases proopiomelanocortin gene expression in the arcuate nucleus of the rat hypothalamus. Eur. J. Pharmacol. 323 (1997) 193-195
29. Coyle I., Wayner M.J., and Singer G. Behavioral teratogenesis: a critical evaluation. Pharmacol. Biochem. Behav. 4 (1976) 191-200
30. Cravatt B.F., Giang D.K., Mayfield S.P., Boger D.L., Lerner R.A., and Gilula N.B. Molecular characterization of an enzyme that degrades neuromodulatory fatty-acid amides. Nature 384 (1996) 83-87
31. Dalterio S.L. Cannabinoid exposure: effects on development. Neurobehav. Toxicol. Teratol. 8 (1986) 345-352
32. Day N., Cornelius M., Goldschmidt L., Richardson G., Robles N., and Taylor P. The effects of prenatal tobacco and marijuana use on offspring growth from birth through 3 years of age. Neurotoxicol. Teratol. 14 (1992) 407-414
33. Day N.L., Richardson G.A., Goldschmidt L., Robles N., Taylor P.M., Stoffer D.S., Cornelius M.D., and Geva D. Effect of prenatal marijuana exposure on the cognitive development of offspring at age three. Neurotoxicol. Teratol. 16 (1994) 169-175
34. Devane W.A., Dysarz F.A., Johnson M.R., Melvin L.S., and Howlett A.C. Determination and characterization of a cannabinoid receptor in rat brain. Mol. Pharmacol. 34 (1988) 605-613
35. Devane W.A., Hanus L., Breuer A., Pertwee R.G., Stevenson L.A., Griffin G., Gibson D., Mandelbaum A., Etinger A., and Mechoulam R. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 258 (1992) 1946-1949
36. Di Forti M., Morrison P.D., Butt A., and Murray R.M. Cannabis use and psychiatric and cognitive disorders: the chicken or the egg?. Curr. Opin. Psychiatry 20 (2007) 228-234
37. Di Marzo V., Bifulco M., and De Petrocellis L. The endocannabinoid system and its therapeutic exploitation. Nat. Rev. Drug Discov. 3 (2004) 771-784
38. Dinh T.P., Carpenter D., Leslie F.M., Freund T.F., Katona I., Sensi S.L., Kathuria S., and Piomelli D. Brain monoglyceride lipase participating in endocannabinoid inactivation. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 10819-10824
39. D'Souza D.C. Cannabinoids and psychosis. Int. Rev. Neurobiol. 78 (2007) 289-326
40. Ehrenreich H., Rinn T., Kunert H.J., Moeller M.R., Poser W., Schilling L., Gigerenzer G., and Hoehe M.R. Specific attentional dysfunction in adults following early start of cannabis use. Psychopharmacology (Berl.) 142 (1999) 295-301
41. Ellgren M., Spano S.M., and Hurd Y.L. Adolescent cannabis exposure alters opiate intake and opioid limbic neuronal populations in adult rats. Neuropsychopharmacology 32 (2007) 607-615
42. Fattore L., Deiana S., Spano S.M., Cossu G., Fadda P., Scherma M., and Fratta W. Endocannabinoid system and opioid addiction: behavioural aspects. Pharmacol. Biochem. Behav. 81 (2005) 343-359
43. Fergusson D.M., Boden J.M., and Horwood L.J. Cannabis use and other illicit drug use: testing the cannabis gateway hypothesis. Addiction 101 (2006) 556-569
44. Fergusson D.M., Horwood L.J., and Swain-Campbell N. Cannabis use and psychosocial adjustment in adolescence and young adulthood. Addiction 97 (2002) 1123-1135
45. Fernandez-Ruiz J., Berrendero F., Hernandez M.L., and Ramos J.A. The endogenous cannabinoid system and brain development. Trends Neurosci. 23 (2000) 14-20
46. Fernandez-Ruiz J., Gomez M., Hernandez M., de Miguel R., and Ramos J.A. Cannabinoids and gene expression during brain development. Neurotox. Res. 6 (2004) 389-401
47. Freund T.F., Katona I., and Piomelli D. Role of endogenous cannabinoids in synaptic signaling. Physiol. Rev. 83 (2003) 1017-1066
48. Fride E. The endocannabinoid-CB(1) receptor system in pre- and postnatal life. Eur. J. Pharmacol. 500 (2004) 289-297
49. Fried P.A. Conceptual issues in behavioral teratology and their application in determining long-term sequelae of prenatal marihuana exposure. J. Child Psychol. Psychiatry 43 (2002) 81-102
50. Fried P.A., and Makin J.E. Neonatal behavioural correlates of prenatal exposure to marihuana, cigarettes and alcohol in a low risk population. Neurotoxicol. Teratol. 9 (1987) 1-7
51. Fried P.A., and Smith A.M. A literature review of the consequences of prenatal marihuana exposure. An emerging theme of a deficiency in aspects of executive function. Neurotoxicol Teratol. 23 (2001) 1-11
52. Fried P.A., and Watkinson B. 12- and 24-month neurobehavioural follow-up of children prenatally exposed to marihuana, cigarettes and alcohol. Neurotoxicol. Teratol. 10 (1988) 305-313
53. Fried P.A., and Watkinson B. 36- and 48-month neurobehavioral follow-up of children prenatally exposed to marijuana, cigarettes, and alcohol. J. Dev. Behav. Pediatr. 11 (1990) 49-58
54. Fried P.A., O'Connell C.M., and Watkinson B. 60- and 72-month follow-up of children prenatally exposed to marijuana, cigarettes, and alcohol: cognitive and language assessment. J. Dev. Behav. Pediatr. 13 (1992) 383-391
55. Fried P.A., Watkinson B., and Gray R. A follow-up study of attentional behavior in 6-year-old children exposed prenatally to marijuana, cigarettes, and alcohol. Neurotoxicol. Teratol. 14 (1992) 299-311
56. Fried P.A., Watkinson B., and Gray R. Differential effects on cognitive functioning in 9- to 12-year olds prenatally exposed to cigarettes and marihuana. Neurotoxicol. Teratol. 20 (1998) 293-306
57. Fried P.A., Watkinson B., James D., and Gray R. Current and former marijuana use: preliminary findings of a longitudinal study of effects on IQ in young adults. CMAJ 166 (2002) 887-891
58. Fried P.A., Watkinson B., and Gray R. Neurocognitive consequences of marihuana-a comparison with pre-drug performance. Neurotoxicol. Teratol. 27 (2005) 231-239
59. Gaoni Y., and Mechoulam R. Isolation, structure and partial synthesis of an active constituent of hashish. J. Am. Chem. Soc. 86 (1964) 1646-1647
60. Garcia-Gil L., De Miguel R., Munoz R.M., Cebeira M., Villanua M.A., Ramos J.A., and Fernandez-Ruiz J.J. Perinatal delta(9)-tetrahydrocannabinol exposure alters the responsiveness of hypothalamic dopaminergic neurons to dopamine-acting drugs in adult rats. Neurotoxicol. Teratol. 19 (1997) 477-487
61. Garcia-Gil L., De Miguel R., Romero J., Perez A., Ramos J.A., and Fernandez-Ruiz J.J. Perinatal delta9-tetrahydrocannabinol exposure augmented the magnitude of motor inhibition caused by GABA(B), but not GABA(A), receptor agonists in adult rats. Neurotoxicol. Teratol. 21 (1999) 277-283
62. Gardner E.L. Endocannabinoid signaling system and brain reward: emphasis on dopamine. Pharmacol. Biochem. Behav. 81 (2005) 263-284
63. Ginsburg K. The Importance of Play in Promoting Healthy Child Development and Maintaining Strong Parent-Child Bonds (2006), American Academy of Pediatrics
64. Gonzalez B., de Miguel R., Martin S., Perez-Rosado A., Romero J., Garcia-Lecumberri C., Fernandez-Ruiz J., Ramos J.A., and Ambrosio E. Effects of perinatal exposure to delta 9-tetrahydrocannabinol on operant morphine-reinforced behavior. Pharmacol. Biochem. Behav. 75 (2003) 577-584
65. Goode E. The Marijuana Smokers (1970), Basic Books, New York, NY
66. Goparaju S.K., Ueda N., Taniguchi K., and Yamamoto S. Enzymes of porcine brain hydrolyzing 2-arachidonoylglycerol, an endogenous ligand of cannabinoid receptors. Biochem. Pharmacol. 57 (1999) 417-423
67. Gray K.A., Day N.L., Leech S., and Richardson G.A. Prenatal marijuana exposure: effect on child depressive symptoms at ten years of age. Neurotoxicol. Teratol. 27 (2005) 439-448
68. Grotenhermen F. The toxicology of cannabis and cannabis prohibition. Chem. Biodivers. 4 (2007) 1744-1769
69. Hampson R.E., and Deadwyler S.A. Cannabinoids, hippocampal function and memory. Life Sci. 65 (1999) 715-723
70. Henquet C., Krabbendam L., Spauwen J., Kaplan C., Lieb R., Wittchen H.U., and van Os J. Prospective cohort study of cannabis use, predisposition for psychosis, and psychotic symptoms in young people. BMJ 330 (2005) 11
71. Hernandez M., Berrendero F., Suarez I., Garcia-Gil L., Cebeira M., Mackie K., Ramos J.A., and Fernandez-Ruiz J. Cannabinoid CB(1) receptors colocalize with tyrosine hydroxylase in cultured fetal mesencephalic neurons and their activation increases the levels of this enzyme. Brain Res. 857 (2000) 56-65
72. Herkenham M., Lynn A.B., Little M.D., Johnson M.R., Melvin L.S., de Costa B.R., and Rice K.C. Cannabinoid receptor localization in brain. Proc. Natl. Acad. Sci. U. S. A. 87 (1990) 1932-1936
73. Hillard C.J., Wilkison D.M., Edgemond W.S., and Campbell W.B. Characterization of the kinetics and distribution of N-arachidonylethanolamine (anandamide) hydrolysis by rat brain. Biochim. Biophys. Acta. 1257 (1995) 249-256
74. Houser S.J., Eads M., Embrey J.P., and Welch S.P. Dynorphin B and spinal analgesia: induction of antinociception by the cannabinoids CP55,940, Delta(9)-THC and anandamide. Brain Res. 857 (2000) 337-342
75. Howlett A.C., and Fleming R.M. Cannabinoid inhibition of adenylate cyclase. Pharmacology of the response in neuroblastoma cell membranes. Mol Pharmacol. 26 (1984) 532-538
76. Huizink A.C., and Mulder E.J. Maternal smoking, drinking or cannabis use during pregnancy and neurobehavioral and cognitive functioning in human offspring. Neurosci. Biobehav. Rev. 30 (2006) 24-41
77. Hutchings D.E., Martin B.R., Gamagaris Z., Miller N., and Fico T. Plasma concentrations of delta-9-tetrahydrocannabinol in dams and fetuses following acute or multiple prenatal dosing in rats. Life Sci. 44 (1989) 697-701
78. Jakubovic A., Hattori T., and McGeer P.L. Radiactivity in suckled rats after giving 14C-tetrahydrocannabinol to the mother. Eur. J. Pharmacol. 22 (1977) 221-223
79. Jones K.L., and Smith D.W. Recognition of the fetal alcohol syndrome in early infancy. Lancet 2 (1973) 999-1001
80. Kamon J., Budney A., and Stanger C. A contingency management intervention for adolescent marijuana abuse and conduct problems. J. Am. Acad. Child Adolesc. Psychiatry 44 (2005) 513-521
81. Katona I., Urban G.M., Wallace M., Ledent C., Jung K.M., Piomelli D., Mackie K., and Freund T.F. Molecular composition of the endocannabinoid system at glutamatergic synapses. J. Neurosci. 26 (2006) 5628-5637
82. Kawamura Y., Fukaya M., Maejima T., Yoshida T., Miura E., Watanabe M., Ohno-Shosaku T., and Kano M. The CB1 cannabinoid receptor is the major cannabinoid receptor at excitatory presynaptic sites in the hippocampus and cerebellum. J. Neurosci. 26 (2006) 2991-3001
83. Kibel D.A., Laffont I., and Liddle P.F. The composition of the negative syndrome of chronic schizophrenia. Br. J. Psychiatry. 162 (1993) 744-750
84. Kosterlitz H.W., and Hughes J. Some thoughts on the significance of enkephalin, the endogenous ligand. Life Sci. 17 (1975) 91-96
85. Kumar A.M., Haney M., Becker T., Thompson M.L., Kream R.M., and Miczek K. Effect of early exposure to delta-9-tetrahydrocannabinol on the levels of opioid peptides, gonadotropin-releasing hormone and substance P in the adult male rat brain. Brain Res. 525 (1990) 78-83
86. Lambert D.M., and Fowler C.J. The endocannabinoid system: drug targets, lead compounds, and potential therapeutic applications. J. Med. Chem. 48 (2005) 5059-5087
87. Leech S.L., Richardson G.A., Goldschmidt L., and Day N.L. Prenatal substance exposure: effects on attention and impulsivity of 6-year-olds. Neurotoxicol. Teratol. 21 (1999) 109-118
88. Lupica C.R., Riegel A.C., and Hoffman A.F. Marijuana and cannabinoid regulation of brain reward circuits. Br. J. Pharmacol. 143 (2004) 227-234
89. Lynskey M.T., Heath A.C., Bucholz K.K., Slutske W.S., Madden P.A., Nelson E.C., Statham D.J., and Martin N.G. Escalation of drug use in early-onset cannabis users vs co-twin controls. JAMA 289 (2003) 427-433
90. Mackie K. Cannabinoid receptors as therapeutic targets. Annu. Rev. Pharmacol. Toxicol. 46 (2006) 101-122
91. Mackie K. Mechanisms of CB1 receptor signaling: endocannabinoid modulation of synaptic strength. Int. J. Obes. (Lond). 30 Suppl. 1 (2006) S19-S23
92. Macleod J., Davey Smith G., Hickman M., and Egger M. Cannabis and psychosis. Lancet 370 1539 (2007) 1539-1540 author reply
93. Macleod J., Oakes R., Copello A., Crome I., Egger M., Hickman M., Oppenkowski T., Stokes-Lampard H., and Davey Smith G. Psychological and social sequelae of cannabis and other illicit drug use by young people: a systematic review of longitudinal, general population studies. Lancet 363 (2004) 1579-1588
94. Manzanares J., Corchero J., Romero J., Fernandez-Ruiz J.J., Ramos J.A., and Fuentes J.A. Chronic administration of cannabinoids regulates proenkephalin mRNA levels in selected regions of the rat brain. Brain. Res. Mol. Brain. Res. 55 (1998) 126-132
95. Manzanares J., Corchero J., Romero J., Fernandez-Ruiz J.J., Ramos J.A., and Fuentes J.A. Pharmacological and biochemical interactions between opioids and cannabinoids. Trends Pharmacol. Sci. 20 (1999) 287-294
96. Martin B.R., Compton D.R., Thomas B.F., Prescott W.R., Little P.J., Razdan R.K., Johnson M.R., Melvin L.S., Mechoulam R., and Ward S.J. Behavioral, biochemical, and molecular modeling evaluations of cannabinoid analogs. Pharmacol. Biochem. Behav. 40 (1991) 471-478
97. Matsuda L.A., Lolait S.J., Brownstein M.J., Young A.C., and Bonner T.I. Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 346 (1990) 561-564
98. McLaughlin C.R., and Abood M.E. Developmental expression of cannabinoid receptor mRNA. Brain Res. Dev. Brain Res. 76 (1993) 75-78
99. Mechoulam R. The pharmacohistory of Cannabis sativa. Cannabinoids as Therapeutic Agents (1986), CRC Press, Boca Raton, FL
100. Mechoulam R., Ben-Shabat S., Hanus L., Ligumsky M., Kaminski N.E., Schatz A.R., Gopher A., Almog S., Martin B.R., Compton D.R., et al. Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochem. Pharmacol. 50 (1995) 83-90
101. Mechoulam R., and Hanus L. A historical overview of chemical research on cannabinoids. Chem. Phys. Lipids 108 (2000) 1-13
102. Mereu G., Fa M., Ferraro L., Cagiano R., Antonelli T., Tattoli M., Ghiglieri V., Tanganelli S., Gessa G.L., and Cuomo V. Prenatal exposure to a cannabinoid agonist produces memory deficits linked to dysfunction in hippocampal long-term potentiation and glutamate release. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 4915-4920
103. Molina-Holgado F., Alvarez F.J., Gonzalez I., Antonio M.T., and Leret M.L. Maternal exposure to delta 9-tetrahydrocannabinol (delta 9-THC) alters indolamine levels and turnover in adult male and female rat brain regions. Brain Res. Bull. 43 (1997) 173-178
104. Molina-Holgado F., Amaro A., Gonzalez M.I., Alvarez F.J., and Leret M.L. Effect of maternal delta 9-tetrahydrocannabinol on developing serotonergic system. Eur. J. Pharmacol. 316 (1996) 39-42
105. Moore T.H., Zammit S., Lingford-Hughes A., Barnes T.R., Jones P.B., Burke M., and Lewis G. Cannabis use and risk of psychotic or affective mental health outcomes: a systematic review. Lancet 370 (2007) 319-328
106. Morral A.R., McCaffrey D.F., and Paddock S.M. Reassessing the marijuana gateway effect. Addiction 97 (2002) 1493-1504
107. Munro S., Thomas K.L., and Abu-Shaar M. Molecular characterization of a peripheral receptor for cannabinoids. Nature 365 (1993) 61-65
108. Navarro M., Rubio P., and de Fonseca F.R. Behavioural consequences of maternal exposure to natural cannabinoids in rats. Psychopharmacology (Berl.) 122 (1995) 1-14
109. NIDA. NIDA Research Monograph Series: Marijuana Abuse (2005), NIH
110. Onaivi E.S., Ishiguro H., Gong J.P., Patel S., Perchuk A., Meozzi P.A., Myers L., Mora Z., Tagliaferro P., Gardner E., Brusco A., Akinshola B.E., Liu Q.R., Hope B., Iwasaki S., Arinami T., Teasenfitz L., and Uhl G.R. Discovery of the presence and functional expression of cannabinoid CB2 receptors in brain. Ann. N. Y. Acad. Sci. 1074 (2006) 514-536
111. O'Shea M., McGregor I.S., and Mallet P.E. Repeated cannabinoid exposure during perinatal, adolescent or early adult ages produces similar long-lasting deficits in object recognition and reduced social interaction in rats. J. Psychopharmacol. 20 (2006) 611-621
112. O'Shea M., Singh M.E., McGregor I.S., and Mallet P.E. Chronic cannabinoid exposure produces lasting memory impairment and increased anxiety in adolescent but not adult rats. J Psychopharmacol. 18 (2004) 502-508
113. Owen J. Cannabis: An Apology. The Independent on Sunday (18/3/2007)
114. Pacher P., Batkai S., and Kunos G. The endocannabinoid system as an emerging target of pharmacotherapy. Pharmacol. Rev. 58 (2006) 389-462
115. Panikashvili D., Simeonidou C., Ben-Shabat S., Hanus L., Breuer A., Mechoulam R., and Shohami E. An endogenous cannabinoid (2-AG) is neuroprotective after brain injury. Nature 413 (2001) 527-531
116. Patton G.C., Coffey C., Carlin J.B., Degenhardt L., Lynskey M., and Hall W. Cannabis use and mental health in young people: cohort study. BMJ 325 (2002) 1195-1198
117. Patton G.C., Coffey C., Carlin J.B., Sawyer S.M., and Lynskey M. Reverse gateways? Frequent cannabis use as a predictor of tobacco initiation and nicotine dependence. Addiction 100 (2005) 1518-1525
118. Perez-Rosado A., Manzanares J., Fernandez-Ruiz J., and Ramos J.A. 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
119. Pert C.B., and Snyder S.H. Opiate receptor: demonstration in nervous tissue. Science 179 (1973) 1011-1014
120. Pertwee R.G., and Ross R.A. Cannabinoid receptors and their ligands. Prostaglandins. Leukot. Essent. Fatty Acids 66 (2002) 101-121
121. Piomelli D. The molecular logic of endocannabinoid signalling. Nat. Rev. Neurosci. 4 (2003) 873-884
122. Piomelli D., Tarzia G., Duranti A., Tontini A., Mor M., Compton T.R., Dasse O., Monaghan E.P., Parrott J.A., and Putman D. Pharmacological profile of the selective FAAH inhibitor KDS-4103 (URB597). CNS Drug Rev. 12 (2006) 21-38
123. Pope Jr. H.G., Gruber A.J., Hudson J.I., Cohane G., Huestis M.A., and Yurgelun-Todd D. Early-onset cannabis use and cognitive deficits: what is the nature of the association?. Drug Alcohol Depend. 69 (2003) 303-310
124. Quinn H.R., Matsumoto I., Callaghan P.D., Long E.E., Arnold J.C., Gunasekaran N., Thompson M.R., Dawson B., Mallet P.E., Kashem M., M.-M. H., Iwazaki T., and 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 33 (2007) 1113-1126
125. Ramos J.A., Gomez M., and de Miguel R. Effects on development. Handb. Exp Pharmacol. (2005) 643-656
126. Richardson G.A., Day N.L., and Goldschmidt L. Prenatal alcohol, marijuana, and tobacco use: infant mental and motor development. Neurotoxicol. Teratol. 17 (1995) 479-487
127. Richardson G.A., Ryan C., Willford J., Day N.L., and Goldschmidt L. Prenatal alcohol and marijuana exposure: effects on neuropsychological outcomes at 10 years. Neurotoxicol. Teratol. 24 (2002) 309-320
128. Rios C., Gomes I., and Devi L.A. mu opioid and CB1 cannabinoid receptor interactions: reciprocal inhibition of receptor signaling and neuritogenesis. Br. J. Pharmacol. 148 (2006) 387-395
129. Rodriguez de Fonseca F., Ramos J.A., Bonnin A., and Fernandez-Ruiz J.J. Presence of cannabinoid binding sites in the brain from early postnatal ages. NeuroReport 4 (1993) 135-138
130. Romero J., Garcia-Palomero E., Berrendero F., Garcia-Gil L., Hernandez M.L., Ramos J.A., and Fernandez-Ruiz J.J. Atypical location of cannabinoid receptors in white matter areas during rat brain development. Synapse 26 (1997) 317-323
131. Romero J., Garcia-Palomero E., Fernandez-Ruiz J.J., and Ramos J.A. Involvement of GABA(B) receptors in the motor inhibition produced by agonists of brain cannabinoid receptors. Behav. Pharmacol. 7 (1996) 299-302
132. Rubio P., Rodriguez de Fonseca F., Munoz R.M., Ariznavarreta C., Martin-Calderon J.L., and Navarro M. Long-term behavioral effects of perinatal exposure to delta 9-tetrahydrocannabinol in rats: possible role of pituitary-adrenal axis. Life Sci. 56 (1995) 2169-2176
133. Rueda D., Navarro B., Martinez-Serrano A., Guzman M., and Galve-Roperh I. The endocannabinoid anandamide inhibits neuronal progenitor cell differentiation through attenuation of the Rap1/B-Raf/ERK pathway. J. Biol. Chem. 277 (2002) 46645-46650
134. Russo E.B. History of cannabis and its preparations in saga, science, and sobriquet. Chem. Biodivers. 4 (2007) 1614-1648
135. Schneider M., and 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 28 (2003) 1760-1769
136. Schoffelmeer A.N., Hogenboom F., Wardeh G., and De Vries T.J. Interactions between CB1 cannabinoid and mu opioid receptors mediating inhibition of neurotransmitter release in rat nucleus accumbens core. Neuropharmacology 51 (2006) 773-781
137. Schramm-Sapyta N.L., Cha Y.M., Chaudhry S., Wilson W.A., Swartzwelder H.S., and Kuhn C.M. Differential anxiogenic, aversive, and locomotor effects of THC in adolescent and adult rats. Psychopharmacology (Berl.) 191 (2007) 867-877
138. Sillence D.J., and Allan D. Utilization of phosphatidylcholine and production of diradylglycerol as a consequence of sphingomyelin synthesis. Biochem. J. 331 Pt 1 (1998) 251-256
139. Singh M.E., McGregor I.S., and Mallet P.E. Perinatal exposure to delta(9)-tetrahydrocannabinol alters heroin-induced place conditioning and fos-immunoreactivity. Neuropsychopharmacology 31 (2006) 58-69
140. Smith A.M., Fried P.A., Hogan M.J., and Cameron I. Effects of prenatal marijuana on visuospatial working memory: an fMRI study in young adults. Neurotoxicol. Teratol. 28 (2006) 286-295
141. Spano M.S., Ellgren M., Wang X., and Hurd Y.L. Prenatal cannabis exposure increases heroin seeking with allostatic changes in limbic enkephalin systems in adulthood. Biol. Psychiatry 61 (2007) 554-563
142. Spear L.P. The adolescent brain and age-related behavioral manifestations. Neurosci. Biobehav. Rev. 24 (2000) 417-463
143. Stefanis N.C., Delespaul P., Henquet C., Bakoula C., Stefanis C.N., and Van Os J. Early adolescent cannabis exposure and positive and negative dimensions of psychosis. Addiction 99 (2004) 1333-1341
144. Suarez I., Bodega G., Fernandez-Ruiz J., Ramos J.A., Rubio M., and Fernandez B. Down-regulation of the AMPA glutamate receptor subunits GluR1 and GluR2/3 in the rat cerebellum following pre- and perinatal delta9-tetrahydrocannabinol exposure. Cerebellum 3 (2004) 66-74
145. Szabo B., and Schlicker E. Effects of cannabinoids on neurotransmission. Handb. Exp. Pharmacol. (2005) 327-365
146. Trezza V., and Vanderschuren L.J.M.J. Bidirectional cannabinoid modulation of social behavior in adolescent rats. Psychopharmacology (Berl.) 197 (2007) 217-227
147. Ueda N., Kurahashi Y., Yamamoto S., and Tokunaga T. Partial purification and characterization of the porcine brain enzyme hydrolyzing and synthesizing anandamide. J. Biol. Chem. 270 (1995) 23823-23827
148. Valverde O., Noble F., Beslot F., Dauge V., Fournie-Zaluski M.C., and Roques B.P. 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
149. Van Sickle M.D., Duncan M., Kingsley P.J., Mouihate A., Urbani P., Mackie K., Stella N., Makriyannis A., Piomelli D., Davison J.S., Marnett L.J., Di Marzo V., Pittman Q.J., Patel K.D., and Sharkey K.A. Identification and functional characterization of brainstem cannabinoid CB2 receptors. Science 310 (2005) 329-332
150. Vanderschuren L.J.M.J., Niesink R.J.M., and Van Ree J.M. The neurobiology of social play behavior in rats. Neurosci. Biobehav. Rev. 21 (1997) 309-326
151. Vela G., Fuentes J.A., Bonnin A., Fernandez-Ruiz J., and Ruiz-Gayo M. Perinatal exposure to delta 9-tetrahydrocannabinol (delta 9-THC) leads to changes in opioid-related behavioral patterns in rats. Brain Res. 680 (1995) 142-147
152. Vela G., Martin S., Garcia-Gil L., Crespo J.A., Ruiz-Gayo M., Javier Fernandez-Ruiz J., Garcia-Lecumberri C., Pelaprat D., Fuentes J.A., Ramos J.A., and Ambrosio E. Maternal exposure to delta9-tetrahydrocannabinol facilitates morphine self-administration behavior and changes regional binding to central mu opioid receptors in adult offspring female rats. Brain Res. 807 (1998) 101-109
153. Vigano D., Rubino T., and Parolaro D. Molecular and cellular basis of cannabinoid and opioid interactions. Pharmacol. Biochem. Behav. 81 (2005) 360-368
154. Vinod K.Y., and Hungund B.L. Cannabinoid-1 receptor: a novel target for the treatment of neuropsychiatric disorders. Expert Opin. Ther. Targets 10 (2006) 203-210
155. Vorhees C.V. Concepts in teratology and developmental toxicology derived from animal research. Ann. N. Y. Acad. Sci. 562 (1989) 31-41
156. Wang X., Dow-Edwards D., Anderson V., Minkoff H., and Hurd Y.L. Discrete opioid gene expression impairment in the human fetal brain associated with maternal marijuana use. Pharmacogenomics J. 6 (2006) 255-264
157. Wang X., Dow-Edwards D., Keller E., and Hurd Y.L. Preferential limbic expression of the cannabinoid receptor mRNA in the human fetal brain. Neuroscience 118 (2003) 681-694
158. Wiley J.L., O'Connell M.M., Tokarz M.E., and Wright Jr. M.J. Pharmacological effects of acute and repeated administration of delta(9)-tetrahydrocannabinol in adolescent and adult rats. J. Pharmacol. Exp. Ther. 320 (2007) 1097-1105
159. Zhou D., and Song Z.H. CB1 cannabinoid receptor-mediated neurite remodeling in mouse neuroblastoma N1E-115 cells. J. Neurosci. Res. 65 (2001) 346-353