Neurobiological alterations at adult age triggered by adolescent exposure to cannabinoids

Pharmacological Research

Volumn 60, Issue 2, 2009, Pages 132-138

  Realini, N ^a   Rubino, T ^a   Parolaro, D ^a  

^a UNIVERSITY OF INSUBRIA   (Italy)

Author keywords

Adolescence; Behaviour; Cannabinoids; Long lasting consequences; Neurobiological substrates

Indexed keywords

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; CANNABIS; DRONABINOL; ENDOCANNABINOID; GLIAL FIBRILLARY ACIDIC PROTEIN; POSTSYNAPTIC DENSITY PROTEIN 95; SYNAPTOBREVIN 2;

ADOLESCENT; ADULT; ANXIETY DISORDER; BRAIN DEVELOPMENT; BRAIN REGION; CANNABIS ADDICTION; CHILD DEVELOPMENT; COGNITIVE DEFECT; COGNITIVE DEVELOPMENT; DEPRESSION; DRUG ABUSE; EMOTIONAL DISORDER; EMOTIONALITY; EPISODIC MEMORY; EXPERIMENTAL MODEL; HUMAN; MEDICAL LITERATURE; MEMORY DISORDER; NEUROCHEMISTRY; NEUROLOGIC DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSYCHOSIS; REVIEW; RISK FACTOR; SCHIZOPHRENIA; SEXUAL MATURATION; SOCIAL EVOLUTION; SYNAPSE; VERBAL MEMORY; WORKING MEMORY;

ADOLESCENT; ADULT; BEHAVIOR; BRAIN; CANNABINOIDS; COGNITION DISORDERS; HUMANS; LONGITUDINAL STUDIES; NEUROBIOLOGY;

EID: 67449119178     PISSN: 10436618     EISSN: 10961186     Source Type: Journal    
DOI: 10.1016/j.phrs.2009.03.006     Document Type: Review

References (94)

1. UNODC, United Nations Office on drugs and crime. Annual report 2008, covering activities in 2007.
2. SAMHSA. Substance Abuse and Mental Health Service Administration. Results from the 2007 National Survey on Drug Use and Health. NSDUH Series H-25. DHHS (2007), National Findings Office of Applied Studies, Rockville, MD
3. NSDUH: National Survey on Drug Use and Health, The Report, Marijuana Use and Perceived Risk of Use among Adolescents: 2002 to 2007. Office of Applied Studies, Substance Abuse and Mental Health Services Administration (SAMHSA). January 2009.
4. Sisk C.L., and Zehr J.L. Pubertal hormones organize the adolescent brain and behavior. Front Neuroendocrinol 26 3-4 (2005) 163-174
5. Pinos H., Collado P., Rodriguez-Zafra M., Rodriguez C., Segovia S., and Guillamon A. The development of sex differences in the locus coeruleus of the rat. Brain Res Bull 56 (2001) 73-78
6. Rankin S.L., Partlow G.D., McCurdy R.D., Giles E.D., and Fisher K.R. Postnatal neurogenesis in the vasopressin and oxytocin containing nucleus of the pig hypothalamus. Brain Res 971 (2003) 189-196
7. Nunez J.L., Lauschke D.M., and Juraska J.M. Cell death in the development of the posterior cortex in male and female rats. J Comp Neurol 436 (2001) 32-41
8. Benes F.M., Taylor J.B., and Cunningham M.C. Convergence and plasticity of monoaminergic systems in the medial prefrontal cortex during the postnatal period: implications for the development of psychopathology. Cereb Cortex 10 (2000) 1014-1027
9. Cunningham M.G., Bhattacharyya S., and Benes F.M. Amygdalo-cortical sprouting continues into early adulthood: implications for the development of normal and abnormal function during adolescence. J Comp Neurol 453 (2002) 116-130
10. Lewis D.A., Cruz D., Eggan S., and Erickson S. Postnatal development of prefrontal inhibitory circuits and the pathophysiology of cognitive dysfunction in schizophrenia. Ann NY Acad Sci 1021 (2004) 64-76
11. Benes F.M., Turtle M., Khan Y., and Farol P. Myelination of a key relay zone in the hippocampal formation occurs in the human brain during childhood, adolescence, and adulthood. Arch Gen Psychiatry 51 (1994) 477-484
12. Nunez J.L., Jurgens H.A., and Juraska J.M. Androgens reduce cell death in the developing rat visual cortex. Brain Res Dev Brain Res 125 (2000) 83-88
13. Woo T.U., Pucak M.L., Kye C.H., Matus C.V., and Lewis D.A. Peripubertal refinement of the intrinsic and associational circuitry in monkey prefrontal cortex. Neuroscience 80 (1997) 1149-1158
14. Goldstein L.A., Kurz E.M., and Sengelaub D.R. Androgen regulation of dendritic growth and retraction in the development of a sexually dimorphic spinal nucleus. J Neurosci 10 (1990) 935-946
15. Meyer G., Ferres-Torres R., and Mas M. The effects of puberty and castration on hippocampal dendritic spines of mice. A Golgi study. Brain Res 155 (1978) 108-112
16. Bourgeois J.P., Goldman-Rakic P.S., and Rakic P. Synaptogenesis in the prefrontal cortex of rhesus monkeys. Cereb Cortex 4 (1994) 78-96
17. Bourgeois J.P., and Rakic P. Changes of synaptic density in the primary visual cortex of the macaque monkey from fetal to adult stage. J Neurosci 13 (1993) 2801-2820
18. Andersen S.L., Thompson A.T., Rutstein M., Hostetter J.C., and Teicher M.H. Dopamine receptor pruning in prefrontal cortex during the periadolescent period in rats. Synapse 37 (2000) 167-169
19. Gerocs K., Rethelyi M., and Halasz B. Quantitative analysis of dendritic protrusions in the medial preoptic area during postnatal development. Brain Res 391 (1986) 49-57
20. Huttenlocher P.R., and Dabholkar A.S. Regional differences in synaptogenesis in human cerebral cortex. J Comp Neurol 387 (1997) 167-178
21. Giedd J.N. Structural magnetic resonance imaging of the adolescent brain. Ann NY Acad Sci 1021 (2004) 77-85
22. Giedd J.N., Blumenthal J., JeVries N.O., Castellanos F.X., Liu H., Zijdenbos A., et al. Brain development during childhood and adolescence: a longitudinal MRI study. Nat Neurosci 2 (1999) 861-863
23. Gogtay N., Giedd J.N., Lusk L., Hayashi K.M., Greenstein D., Vaituzis A.C., et al. Dynamic mapping of human cortical development during childhood through early adulthood. Proc Natl Acad Sci USA 101 (2004) 8174-8179
24. Koshibu K., Levitt P., and Ahrens E.T. Sex-specific postpuberty changes in mouse brain structures revealed by three-dimensional magnetic resonance microscopy. Neuroimage 22 (2004) 1636-1645
25. Sowell E.R., Thompson P.M., Tessner K.D., and Toga A.W. Mapping continued brain growth and gray matter density reduction in dorsal frontal cortex: inverse relationships during postadolescent brain maturation. J Neurosci 21 (2001) 8819-8829
26. Sowell E.R., Trauner D.A., Gamst A., and Jernigan T.L. Development of cortical and subcortical brain structures in childhood and adolescence: a structural MRI study. Dev Med Child Neurol 44 (2002) 4-16
27. Harkany T., Keimpema E., Barabás K., and Mulder J. Endocannabinoid functions controlling neuronal specification during brain development. Mol Cell Endocrinol 286 (2008) S84-90
28. Trezza V., Cuomo V., and Vanderschuren L.J. Cannabis and the developing brain: insights from behavior. Eur J Pharmacol 585 2-3 (2008) 441-452
29. Moore T.H., Zammit S., Lingford-Hughes A., Barnes T.R., Jones P.B., Burke M., et al. Cannabis use and risk of psychotic or affective mental health outcomes: a systematic review. Lancet 370 9584 (2007) 319-328
30. Fried P.A., James D.S., and Watkinson B. Growth and pubertal milestones during adolescence in offspring prenatally exposed to cigarettes and marijuana. Neurotoxicol Teratol 23 (2001) 431-436
31. Martin C.A., Kelly T.H., Rayens M.K., Brogli B.R., Brenzel A., Smith W.J., et al. Sensation seeking, puberty, and nicotine, alcohol, and marijuana use in adolescence. J Am Acad Child Adolesc Psychiatry 41 (2002) 1495-1502
32. Patton G.C., McMorris B.J., Toumbourou J.W., Hemphill S.A., Donath S., and Catalano R.F. Puberty and the onset of substance use and abuse. Pediatrics 114 (2004) e300-e306
33. Trad P.V. Developmental vicissitudes that promote drug abuse in adolescents. Am J Drug Alcohol Abuse 20 (1994) 459-481
34. Kandel D.B., Yamaguchi K., and Klein L.C. Testing the gateway hypothesis. Addiction 101 (2006) 470-472
35. Rubino T., and Parolaro D. Long lasting consequences of cannabis exposure in adolescence. Mol Cell Endocrinol 286 1-2 Suppl. 1 (2008) S108-S113
36. Cahill C.M., Malhi G.S., Ivanovski B., Lagopoulos J., and Cohen M. Cognitive compromise in bipolar disorder with chronic cannabis use: cause or consequence?. Expert Rev Neurother 6 4 (2006) 591-598
37. Craft R.M. Sex differences in behavioral effects of cannabinoids. Life Sci 77 20 (2005) 2471-2478
38. Fattore L., Spano M.S., Altea S., Angius F., Fadda P., and Fratta W. Cannabinoid self-administration in rats: sex differences and the influence of ovarian function. Br J Pharmacol 152 5 (2007) 795-804
39. Pacher P., Bátkai S., and Kunos G. The endocannabinoid system as an emerging target of pharmacotherapy. Pharmacol Rev 58 3 (2006) 389-462
40. Reims Symposium. In: Nahas, Sutin, Harvey, and Agurell (Eds). Marijuana and medicine (1999), Humana Press, Totowa 15
41. Rubino T., Vigano' D., Realini N., Guidali C., Braida D., Capurro V., et al. Chronic Delta(9)-tetrahydrocannabinol during adolescence provokes sex-dependent changes in the emotional profile in adult rats: behavioral and biochemical correlates. Neuropsychopharmacology 33 11 (2008) 2760-2771
42. 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
43. 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
44. 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
45. Schneider M., and Koch M. Deficient social and play behavior in juvenile and adult rats after neonatal cortical lesion: effects of chronic pubertal cannabinoid treatment. Neuropsychopharmacology 30 (2005) 944-957
46. 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
47. 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
48. Biscaia M., Marín S., Fernández B., Marco E.M., Rubio M., Guaza C., et al. Chronic treatment with CP-55 940 during the peri-adolescent period differentially affects the behavioural responses of male and female rats in adulthood. Psychopharmacology 170 (2003) 301-308
49. Wegener N., and Koch M. Behavioural disturbances and altered Fos protein expression in adult rats after chronic pubertal cannabinoid treatment. Brain Res 1253 (2009) 81-91
50. Lapiz-Bluhm M.D., Bondi C.O., Doyen J., Rodriguez G.A., Bédard-Arana T., and Morilak D.A. Behavioural assays to model cognitive and affective dimensions of depression and anxiety in rats. J Neuroendocrinol 20 (2008) 1115-1137
51. Ramos A. Animal models of anxiety: do I need multiple tests?. Trends Pharmacol Sci 29 (2008) 493-498
52. Nibuya M., Nestler E.J., and Duman R.S. Chronic antidepressant administration increases the expression of cAMP response element binding protein (CREB) in rat hippocampus. J Neurosci 16 (1996) 2365-2372
53. Thome J., Sakai N., Shin K., Steffen C., Zhang Y.J., Impey S., et al. cAMP response element-mediated gene transcription is upregulated by chronic antidepressant treatment. J Neurosci 20 (2000) 4030-4036
54. Sairanen M., O'Leary O.F., Knuuttila J.E., and Castren E. Chronic antidepressant treatment selectively increases expression of plasticity-related proteins in the hippocampus and medial prefrontal cortex of the rat. Neuroscience 144 (2007) 368-374
55. Tiraboschi E., Tardito D., Kasahara J., Moraschi S., Pruneri P., Gennarelli M., et al. Selective phosphorylation of nuclear CREB by fluoxetine is linked to activation of CaM kinase IV and MAP kinase cascades. Neuropsychopharmacology 29 (2004) 1831-1840
56. Carlezon Jr. W.A., Duman R.S., and Nestler E.J. The many faces of CREB. Trends Neurosci 28 (2005) 436-445
57. Newton S.S., Thome J., Wallace T.L., Shirayama Y., Schlesinger L., and Sakai N. et al Inhibition of cAMP response element-binding protein or dynorphin in the nucleus accumbens produces an antidepressant-like effect. J Neurosci 22 (2002) 10883-10890
58. Fergusson D.M., Horwood L.J., and Swain-Campbell N. Cannabis use and psychosocial adjustment in adolescence and young adulthood. Addiction 97 9 (2002) 1123-1135
59. 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 7374 (2002) 1195-1198
60. Hayatbakhsh M.R., Najman J.M., Jamrozik K., Mamun A.A., Alati R., and Bor W. Cannabis and anxiety and depression in young adults: a large prospective study. J Am Acad Child Adolesc Psychiatry 46 3 (2007) 408-417
61. 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
62. Harder V.S., Stuart E.A., and Anthony J.C. Adolescent cannabis problems and young adult depression: male-female stratified propensity score analyses. Am J Epidemiol 168 6 (2008) 592-601
63. Schneider M., and Koch M. The effect of chronic peripubertal cannabinoid treatment on deficient object recognition memory in rats after neonatal mPFC lesion. Eur Neuropsychopharmacol 1 (2007) 180-186
64. Quinn H.R., Matsumoto I., Callaghan P.D., Long L.E., Arnold J.C., Gunasekaran N., et al. 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 5 (2008) 1113-1126
65. Rubino T., Realini N., Braida D., Alberio T., Capurro V., Viganò D., et al. The depressive phenotype induced in adult female rats by adolescent exposure to THC is associated with cognitive impairment and altered neuroplasticity in the prefrontal cortex. Neurotoxic Res 15 1 (2009) 567-607
66. Rubino T., Realini N., Braida D., Guidi S., Capurro V., Viganò D., et al. Changes in hippocampal morphology and neuroplasticity induced by adolescent THC treatment are associated with cognitive impairment in adulthood, January 20. Hippocampus (2009) 10.1002/hipo.20554
67. Cahill L. Why sex matters for neuroscience. Nat Rev Neurosci 7 6 (2006) 477-484
68. Piefke M., Weiss P., Markowitsch H., and Fink G. Gender differences in the functional neuroanatomy of emotional episodic autobiographical memory. Hum Brain Mapp 24 (2005) 313-324
69. Pope Jr. H.G., Gruber A.J., Hudson J.I., Huestis M.A., and Yurgelun-Todd D. Neuropsychological performance in long-term cannabis users. Arch Gen Psychiatry 58 (2001) 909-915
70. Jacobsen L.K., Mencl W.E., Westerveld M., and Pugh K.R. Impact of cannabis use on brain function in adolescents. Ann NY Acad Sci 1021 (2004) 384-390
71. Solowij N., and Battisti R. The chronic effects of cannabis on memory in humans: a review. Curr Drug Abuse Rev 1 (2008) 81-98
72. Schweinsburg A.D., Brown S.A., and Tapert S.F. The influence of marijuana use on neurocognitive functioning in adolescents. Curr Drug Abuse Rev 1 (2008) 99-111
73. Bolla K.I., Brown K., Eldreth D., Tate K., and Cadet J.L. Dose-related neurocognitive effects of marijuana use. Neurology 59 (2002) 1337-1343
74. Pope Jr. H.G., and Yurgelun-Todd D. The residual cognitive effects of heavy marijuana use in college students. J Am Med Assoc 275 (1996) 521-527
75. Pope Jr. H.G., Jacobs A., Mialet J.P., Yurgelun-Todd D., and Gruber S. Evidence for a sex-specific residual effect of cannabis on visuo-spatial memory. Psychother Psychosomat 66 (1997) 179-184
76. Solowij N., Stephens R.S., Roffman R.A., Babor T., Kadden R., Miller M., et al. Cognitive functioning of long-term heavy cannabis users seeking treatment. JAMA 287 9 (2002) 1123-1131
77. Croft R.J., Mackay A.J., Mills A.T., and Gruzelier J.G. The relative contributions of ecstasy and cannabis to cognitive impairment. Psychopharmacology 153 (2001) 373-379
78. Ashton H. Defining the indefinable: comments on Smith. Addiction 97 6 (2002) 756
79. Andréasson S., Allebeck P., Engström A., and Rydberg U. Cannabis and schizophrenia. A longitudinal study of Swedish conscripts. Lancet 2 (1987) 1483-1486
80. Arseneault L., Cannon M., Witton J., and Murray R.M. Causal association between cannabis and psychosis: examination of the evidence. Br J Psychiatry 184 (2004) 110-117
81. Henquet C., Murray R., Linszen D., and van Os J. The environment and schizophrenia: the role of cannabis use. Schizophr Bull 31 3 (2005) 608-612
82. Ellgren M., Hurd Y.L., and Franck J. Amphetamine effects on dopamine levels and behaviour following cannabinoid exposure during adolescence. Eur J Pharmacol 497 (2004) 205-213
83. 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
84. Biscaia M., Fernández B., Higuera-Matas A., Miguéns M., Viveros M.P., García-Lecumberri C., et al. 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 5 (2008) 863-873
85. Pistis M., Perra S., Pillolla G., Melis M., Muntoni A.L., and 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 56 (2004) 86-94
86. Higuera-Matas A., Luisa Soto-Montenegro M., Del Olmo N., Miguens M., Torres I., Jose Vaquero J., et al. 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
87. Cleveland H.H., and Wiebe R.P. Understanding the association between adolescent marijuana use and later serious drug use: gateway effect or developmental trajectory?. Dev Psychopathol 20 2 (2008) 615-632
88. Yamaguchi K., and Kandel D.B. Patterns of drug use from adolescence to young adulthood: II sequences of progression. Am J Public Health 74 (1984) 668-672
89. Kandel D.B., Yamaguchi K., and Chen K. Stages of progression in drug involvement from adolescence to adulthood: further evidence for the gateway theory. J Stud Alcohol 53 (1992) 447-457
90. Fergusson D.M., and Horwood L.J. Does cannabis use encourage other forms of illicit drug use?. Addiction 95 (2000) 505-520
91. MacCoun R. In what sense (if any) is marijuana a gateway drug?. FAS Drug Policy Anal Bull 4 (1998) 3-5
92. Morral A.R., McCaffrey D.F., and Paddock S.M. Reassessing the marijuana gateway effect. Addiction 97 (2002) 1493-1504
93. Lynskey M.T., Heath A.C., Bucholz K.K., Slutske W.S., Madden P.A., Nelson E.C., et al. Escalation of drug use in early-onset cannabis users vs co-twin controls. JAMA 289 (2003) 427-433
94. Agrawal A., Lynskey M.T., Bucholz K.K., Martin N.G., Madden P.A., and Heath A.C. Contrasting models of genetic co-morbidity for cannabis and other illicit drugs in adult Australian twins. Psychol Med 37 (2007) 49-60