Chronic cannabinoid exposure reduces phencyclidine-induced schizophrenia-like positive symptoms in adult rats

Psychopharmacology

Volumn 225, Issue 3, 2013, Pages 531-542

  Spano, Maria Sabrina ^a   Fattore, Liana ^a,b   Cadeddu, Francesca ^b   Fratta, Walter ^b   Fadda, Paola ^b  

^a CNR   (Italy)

^b UNIVERSITY OF CAGLIARI   (Italy)

Author keywords

Abuse; Anxiety; Cannabinoids; Comorbidity; Locomotor activity; PCP; Psychosis; Schizophrenia; Self administration

Indexed keywords

2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; CANNABINOID; PHENCYCLIDINE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; DRUG ABUSE; DRUG SELF ADMINISTRATION; LOCOMOTION; MALE; MOTIVATION; NONHUMAN; POSITIVE SYNDROME; PRIORITY JOURNAL; RAT; REARING; SCHIZOPHRENIA;

ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; BENZOXAZINES; CANNABINOID RECEPTOR AGONISTS; CANNABINOIDS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; HALLUCINOGENS; INJECTIONS, INTRAVENOUS; MALE; MORPHOLINES; MOTOR ACTIVITY; NAPHTHALENES; PHENCYCLIDINE; RATS; RATS, INBRED STRAINS; SCHIZOPHRENIA; SCHIZOPHRENIC PSYCHOLOGY; SELF ADMINISTRATION;

EID: 84873720051     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-012-2839-1     Document Type: Article

References (101)

1. Adams B, Moghaddam B (1998) Corticolimbic dopamine neurotransmission is temporally dissociated from the cognitive and locomotor effects of phencyclidine. J Neurosci 18:5545-5554
2. Arseneault L, Cannon M, Witton J, Murray RM (2004) Causal association between cannabis and psychosis: examination of the evidence. Br J Psychiatry 184:110-117
3. Ballmaier M, Bortolato M, Rizzetti C, Zoli M, Gessa G, Heinz A, Spano P (2007) Cannabinoid receptor antagonists counteract sensorimotor gating deficits in the phencyclidine model of psychosis. Neuropsychopharmacology 32:2098-2107
4. Bersani G, Orlandi V, Kotzalidis GD, Pancheri P (2002) Cannabis and schizophrenia: impact on onset, course, psychopathology and outcomes. Eur Arch Psychiatry Clin Neurosci 252:86-92
5. Braga RJ, Petrides G, Figueira I (2004) Anxiety disorders in schizophrenia. Compr Psychiatry 45:460-468
6. Breivogel CS, Childers SR (1998) The functional neuroanatomy of brain cannabinoid receptors. Neurobiol Dis 5:417-431
7. Bruhwyler J, Chleide E, Mercier M (1990) Clozapine: an atypical neuroleptic. Neurosci Biobehav Rev Winter 14:357-363
8. Campiani G, Nacci V, Bechelli S, Ciani SM, Garofalo A, Fiorini I, Wikström H, de Boer P, Liao Y, Tepper PG, Cagnotto A, Mennini T (1998) New antipsychotic agents with serotonin and dopamine antagonist properties based on a pyrrolo[2,1-b][1,3]benzothiazepine structure. J Med Chem 41:3763-3772
9. Cannizzaro C, Martire M, Cannizzaro E, Provenzano G, Gagliano M, Carollo A, Mineo A, Steardo L (2001) Long-lasting handling affects behavioural reactivity in adult rats of both sexes prenatally exposed to diazepam. Brain Res 904:225-233
10. Choleris E, Thomas AW, Kavaliers M, Prato FS (2001) A detailed ethological analysis of the mouse open field test: effects of diazepam, chlordiazepoxide and an extremely low frequency pulsed magnetic field. Neurosci Biobehav Rev 25:235-260
11. Corbett R, Camacho F, Woods AT, Kerman LL, Fishkin RJ, Brooks K, Dunn RW (1995) Antipsychotic agents antagonize non-competitive N-methyl-d-aspartate antagonist-induced behaviors. Psychopharmacology 120:67-74
12. Corbillé AG, Valjent E, Marsicano G, Ledent C, Lutz B, Hervé D, Girault JA (2007) Role of cannabinoid type 1 receptors in locomotor activity and striatal signaling in response to psychostimulants. J Neurosci 27:6937-6947
13. D'Souza DC, Abi-Saab WM, Madonick S, Wray Y, Forselius K, Mcdougall L, Brush L, Cassello K, Krystal JH (2000) Cannabinoids and psychosis: evidence from studies with I.V. THC in schizophrenic patients and controls. Schizophr Res 41(Suppl):33
14. D'Souza DC, Abi-Saab WM, Madonick S, Forselius-Bielen K, Doersch A, Braley G, Gueorguieva R, Cooper TB, Krystal JH (2005) Delta-9- tetrahydrocannabinol effects in schizophrenia: implications for cognition, psychosis, and addiction. Biol Psychiatry 57:594-608
15. Daenen EW, Wolterink G, Van Ree JM (2003) Hyperresponsiveness to phencyclidine in animals lesioned in the amygdala on day 7 of life. Implications for an animal model of schizophrenia. Eur Neuropsychopharmacol 13:273-279
16. Degenhardt L, Hall W, Lynskey M (2001) Alcohol, cannabis and tobacco use among Australians: a comparison of their associations with other drug use and use disorders, affective and anxiety disorders, and psychosis. Addiction 96:1603-1614
17. Degenhardt L, Tennant C, Gilmour S, Schofield D, Nash L, Hall W, McKay D (2007) The temporal dynamics of relationships between cannabis, psychosis and depression among young adults with psychotic disorders: findings from a 10-month prospective study. Psychol Med 37:927-934
18. Duke PJ, Pantelis C, McPhillips MA, Barnes TR (2001) Comorbid non-alcohol substance misuse among people with schizophrenia: epidemiological study in central London. Br J Psychiatry 179:509-513
19. Duncan GE, Sheitman BB, Lieberman JA (1999) An integrated view of pathophysiological models of schizophrenia. Brain Res Brain Res Rev 29:250-264
20. Ellenbroek BA, Liégeois JF (2003) JL 13, an atypical antipsychotic: a preclinical review. CNS Drug Rev Spring 9:41-56
21. Fattore L, Cossu G, Martellotta MC, Fratta W (2001) Intravenous self-administration of the cannabinoid CB1 receptor agonist WIN 55,212-2 in rats. Psychopharmacology 156:410-416
22. Fattore L, Spano MS, Altea S, Angius F, Fadda P, Fratta W (2007) Cannabinoid self-administration in rats: sex differences and the influence of ovarian function. Br J Pharmacol 152:795-804
23. Fattore L, Spano MS, Altea S, Fadda P, Fratta W (2010) Drug- and cue-induced reinstatement of cannabinoid seeking behaviour in male and female rats: influences of ovarian hormones. Brit J Pharmacol 160:724-735
24. Fernández-Ruiz J, Gonzáles S (2005) Cannabinoid control of motor function at the basal ganglia. Handb Exp Pharmacol 168:479-507
25. Freed WJ, Bing LA, Wyatt RJ (1984) Effects of neuroleptics on phencyclidine (PCP)-induced locomotor stimulation in mice. Neuropharmacology 23:175-181
26. Gentsch C, Lichtsteiner M, Feer H (1987) Open field and elevated plus-maze: a behavioural comparison between spontaneously hypertensive (SHR) and Wistar-Kyoto (WKY) rats and the effects of chlordiazepoxide. Behav Brain Res 25:101-107
27. Gorriti MA, Rodríguez de Fonseca F, Navarro M, Palomo T (1999) Chronic (-)-delta9-tetrahydrocannabinol treatment induces sensitization to the psychomotor effects of amphetamine in rats. Eur J Pharmacol 365:133-142
28. Gray JA (1979) Anxiety and the brain: not by neurochemistry alone. Psychol Med 9:605-609
29. Grossen NE, Kelley MJ (1972) Species-specific behavior and acquisition of avoidance behavior in rats. J Comp Physiol Psychol 81:307-310
30. Hájos N, Freund TF (2002) Distinct cannabinoid sensitive receptors regulate hippocampal excitation and inhibition. Chem Phys Lipids 121(1-2):73-82
31. Haller J, Szirmai M, Varga B, Ledent C, Freund TF (2005) Cannabinoid CB1 receptor dependent effects of the NMDA antagonist phencyclidine in the social withdrawal model of schizophrenia. Behav Pharmacol 16:415-422
32. Herkenham M, Lynn AB, Johnson MR, Melvin LS, de Costa BR, Rice KC (1991) Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J Neurosci 11:563-583
33. Hill MN, Gorzalka BB (2009) The endocannabinoid system and the treatment of mood and anxiety disorders. CNS Neurol Disord Drug Targets 8:451-458
34. Hori T, Subramaniam S, Srivastava LK, Quirion R (2000) Behavioral and neurochemical alterations following repeated phencyclidine administration in rats with neonatal ventral hippocampal lesions. Neuropharmacology 39:2478-2491
35. Jablensky A, Sartorius N, Ernberg G, Anker M, Korten A, Cooper JE, Day R, Bertelsen A (1992) Schizophrenia: manifestations, incidence and course in different cultures. A World Health Organization ten-country study. Psychol Med Monogr 20:1-97
36. Javitt DC, Zukin SR (1991) Recent advances in the phencyclidine model of schizophrenia. Am J Psychiatry 148:1301-1308
37. Jentsch JD, Roth RH (1999) The neuropsychopharmacology of phencyclidine: from NMDA receptor hypofunction to the dopamine hypothesis of schizophrenia. Neuropsychopharmacology 20:201-225
38. Jiang W, Zhang Y, Xiao L, Van Cleemput J, Ji SP, Bai G, Zhang X (2005) Cannabinoids promote embryonic and adult hippocampus neurogenesis and produce anxiolytic- and antidepressant-like effects. J Clin Invest 115:3104-3116
39. Jinks AL, McGregor IS (1997) Modulation of anxiety-related behaviours following lesions of the prelimbic or infralimbic cortex in the rat. Brain Res 772:181-190
40. Johnson KM, Phillips M, Wang C, Kevetter GA (1998) Chronic phencyclidine induces behavioral sensitization and apoptotic cell death in the olfactory and piriform cortex. J Neurosci Res 52:709-722
41. Katona I, Rancz EA, Acsady L, Ledent C, Mackie K, Hajos N, Freund TF (2001) Distribution of CB1 cannabinoid receptors in the amygdala and their role in the control of GABAergic transmission. J Neurosci 21:9506-9518
42. Katsetos CD, Hyde TM, Herman MM (1997) Neuropathology of the cerebellum in schizophrenia-an update: 1996 and future directions. Biol Psychiatry 42:213-224
43. Kavaliers M, Choleris E (2001) Antipredator responses and defensive behavior: ecological and ethological approaches for the neurosciences. Neurosci Biobehav Rev 25:577-586
44. Kitaichi K, Yamada K, Yoneda Y, Ogita K, Hasegawa T, Furukawa H, Nabeshima T (1995) Risperidone prevents the development of supersensitivity, but not tolerance, to phencyclidine in rats treated with subacute phencyclidine. Life Sci 56:531-543
45. Krebs-Thomson K, Lehmann-Masten V, Naiem S, Paulus MP, Geyer MA (1998) Modulation of phencyclidine-induced changes in locomotor activity and patterns in rats by serotonin. Eur J Pharmacol 343:135-143
46. Lafenêtre P, Chaouloff F, Marsicano G (2007) The endocannabinoid system in the processing of anxiety and fear and how CB1 receptors may modulate fear extinction. Pharmacol Res 56:367-381
47. Long LE, Chesworth R, Huang XF, McGregor IS, Arnold JC, Karl T (2009) A behavioural comparison of acute and chronic Delta9-tetrahydrocannabinol and cannabidiol in C57BL/6JArc mice. Int J Neuropsychopharmacol 29:1-16
48. Mailleux P, Vanderhaeghen JJ (1993) Dopaminergic regulation of cannabinoid receptor mRNA levels in the rat caudate-putamen: an in situ hybridization study. J Neurochem 61:1705-1712
49. Maj J, Rogóz Z, Skuza G, Mazela H (1996) Neuropharmacological profile of EMD 57445, a sigma receptor ligand with potential antipsychotic activity. Eur J Pharmacol 315:235-243
50. Marco EM, García-Gutiérrez MS, Bermúdez-Silva FJ, Moreira FA, Guimarães F, Manzanares J, Viveros MP (2011) Endocannabinoid system and psychiatry: in search of a neurobiological basis for detrimental and potential therapeutic effects. Front Behav Neurosci 5:63
51. Marcotte ER, Pearson DM, Srivastava LK (2001) Animal models of schizophrenia: a critical review. J Psychiatry Neurosci 26:395-410
52. Masserano JM, Karoum F, Wyatt RJ (1999) SR 141716A, a CB1 cannabinoid receptor antagonist, potentiates the locomotor stimulant effects of amphetamine and apomorphine. Behav Pharmacol 10:429-432
53. Masuo Y, Noguchi J, Morita S, Matsumoto Y (1995) Effect of intracerebroventricular administration of pituitary adenylate cyclase-activating polypeptide (PACAP) on the motor activity and reserpine-induced hypothermia in murines. Brain Res 700:219-226
54. Matsuda LA, Bonner TI, Lolait SJ (1993) Localization of cannabinoid receptor mRNA in rat brain. J Comp Neurol 327:535-550
55. Menezes PR, Mann AH (1996) Mortality among patients with non-affective functional psychoses in a metropolitan area of south-eastern Brazil. Rev Saude Publica 30:304-309
56. Miyamoto M, Narumi S, Nagai T, Nagawa Y (1984) A TRH analog (DN-1417): motor stimulation with rearing related to catecholaminergic mechanism in rats. Neuropharmacology 23:61-72
57. Moghaddam B, Jackson ME (2003) Glutamatergic animal models of schizophrenia. Ann N Y Acad Sci 1003:131-137
58. Mohn AR, Gainetdinov RR, Caron MG, Koller BH (1999) Mice with reduced NMDA receptor expression display behaviors related to schizophrenia. Cell 98:427-436
59. Moreira FA, Guimanares FS (2005) Cannabidiol inhibits the hyperlocomotion induced by psychotomimetic drugs in mice. Eur J Pharmacol 512:199-205
60. Morris BJ, Cochran SM, Pratt JA (2005) PCP: from pharmacology to modelling schizophrenia. Curr Opin Pharmacol 5:101-106
61. Murray TF, Horita A (1979) Phencyclidine-induced stereotyped behavior in rats: dose response effects and antagonism by neuroleptics. Life Sci 24:2217-2225
62. Nabeshima T, Yamaguchi K, Yamada K, Hiramatsu M, Furukawa H, Kameyama T (1983) Phencyclidine-induced stereotyped behaviors in rats following specific neurotoxin lesions of the striatum. Eur J Pharmacol 93:229-234
63. Nabeshima T, Fukaya H, Yamaguchi K, Ishikawa K, Furukawa H, Kameyama T (1987) Development of tolerance and supersensitivity to phencyclidine in rats after repeated administration of phencyclidine. Eur J Pharmacol 135:23-33
64. Nagai T, Noda Y, Une T, Furukawa K, Furukawa H, Kan QM, Nabeshima T (2003) Effect of AD-5423 on animal models of schizophrenia: phencyclidine- induced behavioral changes in mice. Neuroreport 14:269-272
65. Nicolás MJ, López-Azcárate J, Valencia M, Alegre M, Pérez-Alcázar M, Iriarte J, Artieda J (2011) Ketamine-induced oscillations in the motor circuit of the rat basal ganglia. PLoS One 6:21814
66. Nunn JA, Rizza F, Peters ER (2001) The incidence of schizotypy among cannabis and alcohol users. J Nerv Ment Dis 189:741-748
67. Parolaro D, Realini N, Vigano D, Guidali C, Rubino T (2010) The endocannabinoid system and psychiatric disorders. Exp Neurol 224:3-14
68. Peralta V, Cuesta MJ (1992) Influence of cannabis abuse on schizophrenic psychopathology. Acta Psychiatr Scand 85:127-130
69. Pistis M, Perra S, Pillolla G, Melis M, Gessa GL, Muntoni AL (2004) Cannabinoids modulate neuronal firing in the rat basolateral amygdala: evidence for CB1- and non-CB1-mediated actions. Neuropharmacology 46:115-125
70. Pryor GT, Husain S, Larse F, McKenzie CE, Carrr JD, Braude MC (1977) Interactions between delta9-tetrahydrocannabinol and phencyclidine hydrochloride in rats. Pharmacol Biochem Behav 6:126-136
71. Regier DA, Farmer ME, Rae DS, Locke BZ, Keith SJ, Judd LL, Goodwin FK (1990) Comorbidity of mental disorders with alcohol and other drug abuse. Results from the Epidemiologic Catchment Area (ECA) Study. JAMA 264:2511-2518
72. Rodríguez de Fonseca F, Del Arco I, Martín-Calderón JL, Gorriti MA, Navarro M (1998) Role of the endogenous cannabinoid system in the regulation of motor activity. Neurobiol Dis 5:483-501
73. Rosen JL, Miller TJ, D'Andrea JT, McGlashan TH, Woods SW (2006) Comorbid diagnoses in patients meeting criteria for the schizophrenia prodrome. Schizophr Res 85:124-131
74. Sams-Dodd F (1995) Distinct effects of d-amphetamine and phencyclidine on the social behaviour of rats. Behav Pharmacol 6:55-65
75. Sams-Dodd F (1998) Effects of continuous D-amphetamine and phencyclidine administration on social behaviour, stereotyped behaviour, and locomotor activity in rats. Neuropsychopharmacology 19:18-25
76. Schneier FR, Siris SG (1987) A review of psychoactive substance use and abuse in schizophrenia. Patterns of drug choice. J Nerv Ment Dis 175:641-652
77. Schofield D, Tennant C, Nash L, Degenhardt L, Cornish A, Hobbs C, Brennan G (2006) Reasons for cannabis use in psychosis. Aust N Z J Psychiatry 40:570-574
78. Schwarcz G, Karajgi B (2010) Improvement in refractory psychosis with dronabinol: four case reports. J Clin Psychiatry 71:1552-1553
79. Schwarcz G, Karajgi B, McCarthy R (2009) Synthetic delta-9- tetrahydrocannabinol (dronabinol) can improve the symptoms of schizophrenia. J Clin Psychopharmacol 29:255-258
80. Skosnik PD, Spatz-Glenn L, Park S (2001) Cannabis use is associated with schizotypy and attentional disinhibition. Schizophr Res 48:83-92
81. Solowij N, Yücel M, Respondek C, Whittle S, Lindsay E, Pantelis C, Lubman DI (2011) Cerebellar white-matter changes in cannabis users with and without schizophrenia. Psychol Med 41:2349-2359
82. Spano MS, Fadda P, Frau R, Fattore L, Fratta W (2010) Cannabinoid self-administration attenuates PCP-induced schizophrenia-like symptoms in adult rats. Eur Neuropsychopharmacol 20:25-36
83. Steinpreis RE, Sokolowski JD, Papanikolaou A, Salamone JD (1994) The effects of haloperidol and clozapine on PCP- and amphetamine-induced suppression of social behavior in the rat. Pharmacol Biochem Behav 47:579-585
84. Sturgeon RD, Fessler RG, Meltzer HY (1979) Behavioral rating scales for assessing phencyclidine-induced locomotor activity, stereotyped behavior and ataxia in rats. Eur J Pharmacol 59:169-179
85. Sturgeon RD, Fessler RG, London SF, Meltzer HY (1982) Behavioral effects of chronic phencyclidine administration in rats. Psychopharmacology 76:52-56
86. Tang Y, Zou H, Strong JA, Cui Y, Xie Q, Zhao G, Jin M, Yu L (2006) Paradoxical effects of very low dose MK-801. Eur J Pharmacol 537:77-84
87. Thiemann G, van der Stelt M, Petrosino S, Molleman A, Di Marzo V, Hasenöhrl RU (2008) The role of the CB1 cannabinoid receptor and its endogenous ligands, anandamide and 2-arachidonoylglycerol, in amphetamine-induced behavioural sensitization. Behav Brain Res 187:289-296
88. Tibbo P, Swainson J, Chue P, LeMelledo JM (2003) Prevalence and relationship to delusions and hallucinations of anxiety disorders in schizophrenia. Depress Anxiety 17:65-72
89. Townsend MH, Wilson MS (2005) Comorbid anxiety disorders and divalproex sodium use among partial hospital patients with psychotic disorders. Compr Psychiatry 46:368-370
90. Treit D, Fundytus M (1989) Thigmotaxis as a test for anxiolytic activity in rats. Pharmacol Biochem Behav 31:959-962
91. Turner WM, Tsuang MT (1990) Impact of substance abuse on the course and outcome of schizophrenia. Schizophr Bull 16:87-95
92. Tzavara ET, Wade M, Nomikos GG (2003) Biphasic effects of cannabinoids on acetylcholine release in the hippocampus: site and mechanism of action. J Neurosci 23:9374-9384
93. Van Mastrigt S, Addington J, Addington D (2004) Substance misuse at presentation to an early psychosis program. Soc Psychiatry Psychiatr Epidemiol 39:69-72
94. Vanderschuren LJ, Kalivas PW (2000) Alterations in dopaminergic and glutamatergic transmission in the induction and expression of behavioral sensitization: a critical review of preclinical studies. Psychopharmacology 151:99-120
95. Verdoux H, Tournier M, Cougnard A (2005) Impact of substance use on the onset and course of early psychosis. Schizophr Res 79:69-71
96. Viveros MP, Marco EM, File SE (2005) Endocannabinoid system and stress and anxiety responses. Pharmacol Biochem Behav 81:331-342
97. Viveros MP, Marco EM, Llorente R, López-Gallardo M (2007) Endocannabinoid system and synaptic plasticity: implications for emotional responses. Neural Plast 52908
98. Winklbaur B, Ebner N, Sachs G, Thau K, Fischer G (2006) Substance abuse in patients with schizophrenia. Dialogues Clin Neurosci 8:37-43
99. Wolf ME (1998) The role of excitatory amino acids in behavioral sensitization to psychomotor stimulants. Prog Neurobiol 54:679-720
100. Xu X, Domino EF (1994) Phencyclidine-induced behavioral sensitization. Pharmacol Biochem Behav 47:603-608
101. Yui K, Goto K, Ikemoto S, Ishiguro T, Angrist B, Duncan GE, Sheitman BB, Lieberman JA, Bracha SH, Ali SF (1999) Neurobiological basis of relapse prediction in stimulant-induced psychosis and schizophrenia: the role of sensitization. Mol Psychiatry 4:512-523