Adolescent exposure to nicotine and/or the cannabinoid agonist CP 55,940 induces gender-dependent long-lasting memory impairments and changes in brain nicotinic and CB 1 cannabinoid receptors

Journal of Psychopharmacology

Volumn 25, Issue 12, 2011, Pages 1676-1690

  Mateos, B ^a   Borcel, E ^a   Loriga, R ^b   Luesu, W ^b   Bini, V ^b   Llorente, R ^a   Castelli, M P ^b   Viveros, M P ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b UNIVERSITY OF CAGLIARI   (Italy)

Author keywords

Adolescence; brain CB1 cannabinoid and nicotinic receptors; cannabinoid; memory abilities; nicotine; withdrawal

Indexed keywords

4 (1,1 DIMETHYLHEPTYL) 1',2',3',4',5',6' HEXAHYDRO 2,3' DIHYDROXY 6' (3 HYDROXYPROPYL)BIPHENYL; CANNABINOID 1 RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN GAMMA SUBUNIT; NICOTINE;

ANATOMICAL VARIATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; GENDER; HIPPOCAMPUS; MALE; MAZE TEST; MEMORY DISORDER; MENTAL TASK; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; RAT; SEX DIFFERENCE;

ANIMALS; AUTORADIOGRAPHY; BODY WEIGHT; BRAIN; CYCLOHEXANOLS; FEMALE; MALE; MAZE LEARNING; MEMORY DISORDERS; NICOTINE; RATS; RATS, WISTAR; RECEPTOR, CANNABINOID, CB1; RECEPTORS, NICOTINIC; SEX CHARACTERISTICS;

EID: 84856087671     PISSN: 02698811     EISSN: 14617285     Source Type: Journal    
DOI: 10.1177/0269881110370503     Document Type: Article

References (69)

1. Adriani W, Laviola G. Windows of vulnerability to psychopathology and therapeutic strategy in the adolescent rodent model. Behav Pharmacol. 2004 ; 15: 341-352 (Pubitemid 39238344)
2. Agrawal A, Lynskey MT, Madden PA, Pergadia ML, Bucholz KK, Heath AC. Simultaneous cannabis and tobacco use and cannabis-related outcomes in young women. Drug Alcohol Depend. 2009 ; 101: 8-12
3. Ameri A. The effects of cannabinoids on the brain. Prog Neurobiol. 1999 ; 58: 315-348 (Pubitemid 29230000)
4. Arthur D, Levin ED. Chronic inhibition of alpha4beta2 nicotinic receptors in the ventral hippocampus of rats: impacts on memory and nicotine response. Psychopharmacology (Berl). 2002 ; 160: 140-145 (Pubitemid 34212239)
5. Barker GR, Bird F, Alexander V, Warburton EC. Recognition memory for objects, place and temporal order: a disconnection analysis of the role of the medial prefrontal cortex and perirhinal cortex. J Neurosci. 2007 ; 27: 2948-2957 (Pubitemid 46438982)
6. Biscaia M, Marín S, Fernández B, 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 (Berl). 2003 ; 170: 301-308 (Pubitemid 37491610)
7. Castelli MP, Piras AP, D'Agostino A, et al. Dysregulation of the endogenous cannabinoid system in adult rats prenatally treated with the cannabinoid agonist Win 55,212-2. Eur J Pharmacol. 2007 ; 573: 11-19 (Pubitemid 47464211)
8. Crews F, He J, Hodge C. Adolescent cortical development: a critical period of vulnerability for addiction. Pharmacol Biochem Behav. 2007 ; 86: 189-199 (Pubitemid 46282057)
9. Dix SL, Aggleton JP. Extending the spontaneous preference test of recognition: evidence of object-location and object-context recognition. Behav Brain Res. 1999 ; 99: 191-200 (Pubitemid 29083445)
10. Egerton A, Allison C, Brett RR, Pratt JA. Cannabinoids and prefrontal cortical function: insights from preclinical studies. Neurosci Biobehav Rev. 2006 ; 30: 680-695
11. Eichenbaum H. Hippocampus cognitive processes and neural representations that underlie declarative memory. Neuron. 2004 ; 44: 109-120 (Pubitemid 39348834)
12. Ellgren SM, Spano SM, Hurd YL. Adolescent cannabis exposure alters opiate intake and opioid limbic neuronal populations in adult rats. Neuropsychopharmacology. 2007 ; 32: 607-615
13. Ennaceur A, Delacour J. A new one trial test for neurobiological studies of memory in rats: I. Behavioral data. Behav Brain Res. 1988 ; 31: 47-59
14. Ennaceur A, Michalikova S, Bradford A, Ahmed S. Detailed analysis of the behavior of Lister and Wistar rats in anxiety, object recognition and object location tasks. Behav Brain Res. 2005 ; 159: 247-266 (Pubitemid 40462501)
15. Farhang B, Diaz S, Tang SL, Wagner EJ. Sex differences in the cannabinoid regulation of energy homeostasis. Psychoneuroendocrinology. 2009 ; 34 (Suppl 1). S237 - S246
16. Ferraro L, Tomasini MC, Beggiato S, et al. Short- and long-term consequences of prenatal exposure to the cannabinoid agonist WIN55,212-2 on rat glutamate transmission and cognitive functions. J Neural Transm. 2009 ; 116: 1017-1027
17. File SE Experimental Approaches to Anxiety and Depression. Elliot JM Heal DJ Marsden CA, ed. New York: Wiley ; 1992: 25-44.
18. González S, Cascio MG, Fernández-Ruiz J, Fezza F, Di Marzo V, Ramos JA. Changes in endocannabinoid contents in the brain of rats chronically exposed to nicotine, ethanol or cocaine. Brain Res. 2002 ; 954: 73-81 (Pubitemid 35223443)
19. Herkenham M, Lynn AB, Johnson MR, et al. Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J Neurosci. 1991 ; 11: 563-583
20. Herkenham M, Lynn AB, Little MD, et al. Cannabinoid receptor localization in brain. Proc Natl Acad Sci USA. 1990 ; 87: 1932-1936
21. Irvine EE, Cheeta S, File SE. Tolerance to nicotine's effects in the elevated plus-maze and increased anxiety during withdrawal. Pharmacol Biochem Behav. 2001 ; 68: 319-325 (Pubitemid 32231194)
22. Jacobsen LK, Krystal JH, Mencl WE, Westerveld M, Frost SJ, Pugh KR. Effects of smoking and smoking abstinence on cognition in adolescent tobacco smokers. Biol Psychiatry. 2005 ; 57: 56-66 (Pubitemid 39647592)
23. Jacobsen LK, Mencl WE, Constable RT, Westerveld M, Pugh KR. Impact of smoking abstinence on working memory neurocircuitry in adolescent daily tobacco smokers. Psychopharmacology (Berl). 2007 ; 193: 557-566 (Pubitemid 47094373)
24. Jacobsen LK, Pugh KR, Constable RT, Westerveld M, Mencl WE. Functional correlates of verbal memory deficits emerging during nicotine withdrawal in abstinent adolescent cannabis users. Biol Psychiatry. 2006 ; 61: 31-40 (Pubitemid 44855735)
25. Johnston AL, File SE. Sex differences in animal tests of anxiety. Physiol Behav. 1991 ; 49: 245-250
26. Lamota L, Bermudez-Silva FJ, Marco EM, et al. Effects of adolescent nicotine and SR 147778 (Surinabant) administration on food intake, somatic growth and metabolic parameters in rats. Neuropharmacology. 2008 ; 54: 194-205 (Pubitemid 350299415)
27. Larkin AE, Fahey B, Gobbo O, et al. Blockade of NMDA receptors pre-training, but not post-training, impairs object displacement learning in the rat. Brain Res. 2008 ; 1199: 126-132
28. Levin ED, McClernon FJ, Rezvani AH. Nicotinic effects on cognitive function: behavioral characterization, pharmacological specification, and anatomic localization. Psychopharmacology. 2006 ; 184: 523-539 (Pubitemid 43255869)
29. Lichtman AH, Varvel SA, Martin BR. Endocannabinoids in cognition and dependence. Prostaglandins Leukot Essent Fatty Acids. 2002 ; 66: 269-285 (Pubitemid 34743601)
30. López-Moreno JA, González-Cuevas G, Navarro M. The CB1 cannabinoid receptor antagonist rimonabant chronically prevents the nicotine-induced relapse to alcohol. Neurobiol Dis. 2007 ; 25: 274-283 (Pubitemid 46124008)
31. López-Moreno JA, González-Cuevas G, Rodríguez de Fonseca F, Navarro M. Long-lasting increase of alcohol relapse by the cannabinoid receptor agonist WIN 55,212-2 during alcohol deprivation. J Neurosci. 2004 ; 24: 8245-8252 (Pubitemid 39280804)
32. Lundqvist T. Cognitive consequences of cannabis use: comparison with abuse of stimulants and heroin with regard to attention, memory and executive functions. Pharmacol Biochem Behav. 2005 ; 81: 319-330 (Pubitemid 40807130)
33. Marco EM, Granstrem O, Moreno E, et al. Subchronic nicotine exposure in adolescence induces long-term effects on hippocampal and striatal cannabinoid-CB1 and mu-opioid receptors in rats. Eur J Pharmacol. 2007 ; 557: 37-43 (Pubitemid 46135558)
34. Marco EM, Llorente R, Moreno E, Biscaia JM, Guaza C, Viveros MP. Adolescent exposure to nicotine modifies acute functional responses to cannabinoid agonists in rats. Behav Brain Res. 2006 ; 172: 46-53 (Pubitemid 44063551)
35. McGregor IS, Issakidis CN, Prior G. Aversive effects of the synthetic cannabinoid CP 55,940 in rats. Pharmacol Biochem Behav. 1996 ; 53: 657-664 (Pubitemid 26088545)
36. Mendrek A, Monterosso J, Simon SL, et al. Working memory in cigarette smokers: comparison to non-smokers and effects of abstinence. Addict Behav. 2006 ; 31: 833-844
37. Mitchell JB, Laiacona J. The medial frontal cortex and temporal memory: tests using spontaneous exploratory behaviour in the rat. Behav Brain Res. 1998 ; 97: 107-113 (Pubitemid 28558854)
38. Mugnaini M, Tessari M, Tarter G, Merlo Pich E, Chiamulera C, Bunnemann B. Upregulation of [3H]methyllycaconitine binding sites following continuous infusion of nicotine, without changes of alpha7 or alpha6 subunit mRNA: an autoradiography and in situ hybridization study in rat brain. Eur J Neurosci. 2002 ; 16: 1633-1646 (Pubitemid 35370695)
39. Nordentoft M, Hjorthøj C. Cannabis use and risk of psychosis in later life. Lancet. 2007 ; 370: 293-294 (Pubitemid 47096843)
40. O'Shea M, McGregor IS, Mallet PE. 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. 2006 ; 20: 611-621 (Pubitemid 44315859)
41. O'Shea M, Singh ME, McGregor IS, Mallet PE. Chronic cannabinoid exposure produces lasting memory impairment and increased anxiety in adolescent but not adult rats. J Psychopharmacol. 2004 ; 18: 502-508 (Pubitemid 39665118)
42. Paxinos G, Watson C The Rat Brain in Stereotaxic Coordinates. 1997 ) The Rat Brain in Stereotaxic Coordinates, 3rd edn. San Diego: Academic Press. San Diego: Academic Press ; 1997 :
43. Pellow S, Chopin P, File SE, Briley M. Validation of open:closed arms entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods. 1985 ; 14: 149-167 (Pubitemid 16239568)
44. Pope HG, Gruber AJ, Hudson JI, Cohane G, Huestis MA, Yurgelun-Todd D. Early-onset cannabis use and cognitive deficits: what is the nature of the association?. Drug Alcohol Depend. 2003 ; 69: 303-310 (Pubitemid 36293942)
45. Pope HG, Jacobs A, Mialet JP, Yurgelun-Todd D, Gruber S. Evidence for a sex-specific residual effect of cannabis on visuospatial memory. Psychother Psychosom. 1997 ; 66: 179-184 (Pubitemid 27331200)
46. Reich CG, Taylor ME, McCarthy MM. Differential effects of chronic unpredictable stress on hippocampal CB1 receptors in male and female rats. Behav Brain Res. 2009 ; 203: 264-269
47. Rodriguez de Fonseca F, Ramos JA, Bonnin A, Fernandez-Ruiz JJ. Presence of cannabinoid binding sites in the brain from early postnatal ages. Neuroreport. 1993 ; 4: 135-138 (Pubitemid 23080859)
48. Rossato JI, Bevilaqua LR, Myskiw JC, Medina JH, Izquierdo I, Cammarota M. On the role of hippocampal protein synthesis in the consolidation and reconsolidation of object recognition memory. Learn Mem. 2007 ; 14: 34-46
49. Rubino T, Realini N, Braida D, et al. Changes in hippocampal morphology and neuroplasticity induced by adolescent THC treatment are associated with cognitive impairment in adulthood. Hippocampus. 2009 ; 19: 763-772
50. Rubino T, Viganò D, Massi P, Parolaro D. Cellular mechanisms of δ9-tetrahydrocannabinol behavioural sensitization. Eur J Neur. 2003 ; 17: 325-330 (Pubitemid 36459512)
51. Rubino T, Viganò D, Realini N, et al. 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
52. 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 (Pubitemid 41070841)
53. Schneider M, Koch M. The effect of chronic peripubertal cannabinoid treatment on deficient object recognition memory in rats after neonatal mPFC lesion. Eur Neuropsychopharmacol. 2007 ; 17: 180-186 (Pubitemid 44779191)
54. Schneider M, Schömig E, Leweke FM. Acute and chronic cannabinoid treatment differentially affects recognition memory and social behavior in pubertal and adult rats. Addict Biol. 2008 ; 13: 345-357
55. Semenova S, Stolerman IP, Markou A. Chronic nicotine administration improves attention while nicotine withdrawal induces performance deficits in the 5-choice serial reaction time task in rats. Pharmacol Biochem Behav. 2007 ; 87: 360-368 (Pubitemid 47101880)
56. Shoaib M, Bizarro L. Deficits in a sustained attention task following nicotine withdrawal in rats. Psychopharmacology. 2005 ; 178: 211-222 (Pubitemid 40379216)
57. Slawecki CJ, Thorsell A, Ehlers CL. Long-term neurobehavioral effects of alcohol or nicotine exposure in adolescent animal models. Ann N Y Acad Sci. 2004 ; 1021: 448-452 (Pubitemid 38879663)
58. Solowij N, Battisti R. The chronic effects of cannabis on memory in humans: a review. Curr Drug Abuse Rev. 2008 ; 1: 81-98
59. Solowij N, Michie PT. Cannabis and cognitive dysfunction: parallels with endophenotypes of schizophrenia?. J Psychiatry Neurosci. 2007 ; 32: 30-52
60. Solowij N, Stephens RS, Roffman RA, et al. Marijuana Treatment Project Research Group. Cognitive functioning of long-term heavy cannabis users seeking treatment. JAMA. 2002 ; 287: 1123-1131 (Pubitemid 34252081)
61. Spear LP. The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev. 2000 ; 24: 417-463 (Pubitemid 30243061)
62. Stolerman IP, Mirza NR, Hahn B, Shoaib M. Nicotine in an animal model of attention. Eur J Pharmacol. 2000 ; 393: 147-154 (Pubitemid 30193411)
63. Sullivan JM. Cellular and molecular mechanisms underlying learning and memory impairments produced by cannabinoids. Learn Mem. 2000 ; 7: 132-139 (Pubitemid 30407778)
64. Trauth JA, Seidler FJ, McCook EC, Slotkin TA. Adolescent nicotine exposure causes persistent upregulation of nicotinic cholinergic receptors in rat brain regions. Brain Res. 1999 ; 851: 9-19 (Pubitemid 30038124)
65. Trezza V, Cuomo V, Vanderschuren LJMJ. Cannabis and the developing brain: Insights from behaviour. Eur J Pharmacol. 2008 ; 585: 441-452
66. Viveros MP, Llorente R, Moreno E, Marco EM. Behavioural and neuroendocrine effects of cannabinoids in critical developmental periods. Behav Pharmacol. 2005 ; 16: 353-362 (Pubitemid 41404806)
67. Viveros MP, Marco EM, File SE. Nicotine and cannabinoids: parallels, contrasts and interactions. Neurosci Biobehav Rev. 2006 ; 30: 1161-1181 (Pubitemid 44856747)
68. Viveros MP, Marco EM, Llorente R, López-Gallardo M. Endocannabinoid system and synaptic plasticity: implications for emotional responses. Neural Plast. 2007 ; 2007: 52908
69. Wenger T, Gerendai I, Fezza F, et al. The hypothalamic levels of the endocannabinoid, anandamide, peak immediately before the onset of puberty in female rats. Life Sci. 2002 ; 70: 1407-1414 (Pubitemid 34159097)