δ 9-Tetrahydrocannabinol-dependent mice undergoing withdrawal display impaired spatial memory

Psychopharmacology

Volumn 217, Issue 4, 2011, Pages 485-494

  Wise, Laura E ^a   Varvel, Stephen A ^a   Selley, Dana E ^a   Wiebelhaus, Jason M ^a   Long, Kelly A ^a   Middleton, Lisa S ^a   Sim Selley, Laura J ^a   Lichtman, Aron H ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

Abstinence; Adenylate cyclase; Cannabinoids; Cerebellum; Hippocampus; Learning and memory; Water maze; Withdrawal; Working memory

Indexed keywords

2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; ADENYLATE CYCLASE; CANNABIS; DRONABINOL; FORSKOLIN; RIMONABANT;

ANIMAL EXPERIMENT; ARTICLE; CEREBELLUM; CONTROLLED STUDY; DOSE RESPONSE; DRUG POTENCY; ENZYME ACTIVATION; ENZYME ACTIVITY; FORCED SWIMMING TEST; HIPPOCAMPUS; MALE; MAZE TEST; MEMORY DISORDER; MOTIVATION; MOUSE; NONHUMAN; PRECIPITATION; PRIORITY JOURNAL; SENSORIMOTOR FUNCTION; SHORT TERM MEMORY; SPATIAL MEMORY; TASK PERFORMANCE; WITHDRAWAL SYNDROME; WORKING MEMORY;

ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; MALE; MARIJUANA ABUSE; MAZE LEARNING; MEMORY DISORDERS; MEMORY, SHORT-TERM; MICE; MICE, INBRED C57BL; PIPERIDINES; PYRAZOLES; SPATIAL BEHAVIOR; SUBSTANCE WITHDRAWAL SYNDROME; TETRAHYDROCANNABINOL;

EID: 82955233608     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-011-2305-5     Document Type: Article

References (66)

1. 9- tetrahydrocannabinol: studies on precipitated and abrupt withdrawal. J Pharmacol Exp Ther 278:1290-1295 (Pubitemid 27166981)
2. Bolla KI, Brown K, Eldreth D, Tate K, Cadet JL (2002) Dose-related neurocognitive effects of marijuana use. Neurology 59:1337-1343 (Pubitemid 35285983)
3. Brodkin J, Moerschbaecher JM (1997) SR141716A antagonizes the disruptive effects of cannabinoid ligands on learning in rats. J Pharmacol Exp Ther 282:1526-1532 (Pubitemid 27408337)
4. Budney AJ, Hughes JR, Moore BA, Novy PL (2001) Marijuana abstinence effects in marijuana smokers maintained in their home environment. Arch Gen Psychiatry 58:917-924 (Pubitemid 32937913)
5. Budney AJ, Vandrey RG, Hughes JR, Thostenson JD, Bursac Z (2008) Comparison of cannabis and tobacco withdrawal: severity and contribution to relapse. J Subst Abuse Treat 35:362-368
6. Cook SA, Lowe JA, Martin BR (1998) CB1 receptor antagonist precipitates withdrawal in mice exposed to Delta9-tetrahydrocannabinol. J Pharmacol Exp Ther 285:1150-1156 (Pubitemid 28277913)
7. da Silva GE, Takahashi RN (2002) SR 141716A prevents delta 9- tetrahydrocannabinol-induced spatial learning deficit in a Morristype water maze in mice. Prog Neuropsychopharmacol Biol Psychiatry 26:321-325 (Pubitemid 34038061)
8. Dahhaoui M, Lannou J, Stelz T, Caston J, Guastavino JM (1992a) Role of the cerebellum in spatial orientation in the rat. Behav Neural Biol 58:180-189 (Pubitemid 23033361)
9. Dahhaoui M, Stelz T, Caston J (1992b) Effects of lesion of the inferior olivary complex by 3-acetylpyridine on learning and memory in the rat. J Comp Physiol A 171:657-664
10. Deadwyler SA, Hampson RE (2008) Endocannabinoids modulate encoding of sequential memory in the rat hippocampus. Psychopharmacology (Berl) 198:577-586
11. Deadwyler SA, Heyser C, Hampson RE (1995) Complete adaptation to the memory disruptive effects of delta-9-thc following 35 days of exposure. Neurosci Res Commun 17:9-18
12. Eldreth DA, Matochik JA, Cadet JL, Bolla KI (2004) Abnormal brain activity in prefrontal brain regions in abstinent marijuana users. Neuroimage 23:914-920 (Pubitemid 39446525)
13. Flament D, Ellermann JM, Kim SG, Ugurbil K, Ebner TJ (1996) Functional magnetic resonance imaging of cerebellar activation during the learning of a visuomotor dissociation task. Hum Brain Mapp 4:210-226 (Pubitemid 27010226)
14. Grant I, Gonzalez R, Carey CL, Natarajan L, Wolfson T (2003) Non-acute (residual) neurocognitive effects of cannabis use: a meta-analytic study. J Int Neuropsychol Soc 9:679-689 (Pubitemid 36889595)
15. Hampson RE, Deadwyler SA (2000) Cannabinoids reveal the necessity of hippocampal neural encoding for short-term memory in rats. J Neurosci 20:8932-8942
16. Hampson RE, Simeral JD, Kelly EJ, Deadwyler SA (2003) Tolerance to the memory disruptive effects of cannabinoids involves adaptation by hippocampal neurons. Hippocampus 13:543-556 (Pubitemid 36958279)
17. Harrison GP Jr, Gruber AJ, Hudson JI, Huestis MA, Yurgelun-Todd D (2002) Cognitive measures in long-term cannabis users. J Clin Pharmacol 42:41S-47S (Pubitemid 35205045)
18. 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
19. Huang P, Liu-Chen LY, Unterwald EM, Cowan A(2009) Hyperlocomotion and paw tremors are two highly quantifiable signs of SR141716-precipitated withdrawal from delta9-tetrahydrocannabinol in C57BL/ 6 mice. Neurosci Lett 465:66-70
20. Hutcheson DM, Tzavara ET, Smadja C, Valjent E, Roques BP, Hanoune J, Maldonado R (1998) Behavioural and biochemical evidence for signs of abstinence in mice chronically treated with delta-9-tetrahydrocannabinol. Br J Pharmacol 125:1567-1577 (Pubitemid 28548570)
21. Jones RT, Benowitz N (1976) The 30-day trip-clinical studies of cannabis tolerance and dependence. In: Braude MC, Szara S (eds) Pharmacology of marihuana. Raven, New York, pp 627-642
22. Jones RT, Benowitz N, Bachman J (1976) Clinical studies of cannabis tolerance and dependence. Ann NY Acad Sci 282:221-239 (Pubitemid 8023834)
23. Joyal CC, Meyer C, Jacquart G, Mahler P, Caston J, Lalonde R (1996) Effects of midline and lateral cerebellar lesions on motor coordination and spatial orientation. Brain Res 739:1-11 (Pubitemid 26387356)
24. Landsman RS, Burkey TH, Consroe P, Roeske WR, Yamamura HI (1997) SR141716A is an inverse agonist at the human cannabinoid CB1 receptor. Eur J Pharmacol 334:R1-R2 (Pubitemid 27417820)
25. Leggio MG, Neri P, Graziano A, Mandolesi L, Molinari M, Petrosini L (1999) Cerebellar contribution to spatial event processing: characterization of procedural learning. Exp Brain Res 127:1-11 (Pubitemid 29290552)
26. Lichtman AH (2000) SR 141716A enhances spatial memory as assessed in a radial-arm maze task in rats. Eur J Pharmacol 404:175-179
27. Lichtman AH, Martin BR (1996) D9-tetrahydrocannabinol impairs spatial memory through a cannabinoid receptor mechanism. Psychopharmacol 126:125-131 (Pubitemid 26246762)
28. Lichtman AH, Martin BR (2005) Cannabinoid tolerance and dependence. Handb Exp Pharmacol (168):691-717
29. Lichtman AH, Poklis JL, Poklis A, Wilson DM, Martin BR (2001a) The pharmacological activity of inhalation exposure to marijuana smoke in mice. Drug Alcohol Depend 63:107-116 (Pubitemid 32488924)
30. Lichtman AH, Sheikh SM, Loh HH, Martin BR (2001b) Opioid and cannabinoid modulation of precipitated withdrawal in delta(9)- tetrahydrocannabinol and morphine-dependent mice. J Pharmacol Exp Ther 298:1007-1014 (Pubitemid 32761916)
31. Lichtman AH, Varvel SA, Martin BR (2002) Endocannabinoids in cognition and dependence. Prostaglandins Leukot Essent Fatty Acids 66:269-285 (Pubitemid 34743601)
32. Maldonado R, Rodriguez de Fonseca F (2002) Cannabinoid addiction: behavioral models and neural correlates. J Neurosci 22:3326-3331 (Pubitemid 37465736)
33. Mallet PE, Beninger RJ (1998) The cannabinoid CB1 receptor antagonist SR141716A attenuates the memory impairment produced by delta-9- tetrahydrocannabinol or anandamide. Psychopharmacol 140:11-19 (Pubitemid 28524302)
34. Martin LA, Goldowitz D, Mittleman G (2003) The cerebellum and spatial ability: dissection of motor and cognitive components with a mouse model system. Eur J Neurosci 18:2002-2010 (Pubitemid 37372383)
35. Matsuda LA, Bonner TI, Lolait SJ (1993) Localization of cannabinoid receptor mRNA in rat brain. J Comp Neurol 327:535-550 (Pubitemid 23033649)
36. McHale S, Hunt N (2008) Executive function deficits in short-term abstinent cannabis users. Hum Psychopharmacol 23:409-415
37. Mennes CE, Ben Abdallah A, Cottler LB (2009) The reliability of self-reported cannabis abuse, dependence and withdrawal symptoms: multisite study of differences between general population and treatment groups. Addict Behav 34:223-226
38. Nestor L, Roberts G, Garavan H, Hester R (2008) Deficits in learning and memory: parahippocampal hyperactivity and frontocortical hypoactivity in cannabis users. Neuroimage 40:1328-1339
39. Niyuhire F, Varvel SA, Martin BR, Lichtman AH (2007) Exposure to marijuana smoke impairs memory retrieval in mice. J Pharmacol Exp Ther 322:1067-1075 (Pubitemid 47295775)
40. Petrosini L, Molinari M, Dell'Anna ME (1996) Cerebellar contribution to spatial event processing: Morris water maze and T-maze. Eur J Neurosci 8:1882-1896 (Pubitemid 26302283)
41. Pope HG Jr, Gruber AJ, Hudson JI, Huestis MA, Yurgelun-Todd D (2001) Neuropsychological performance in long-term cannabis users. Arch Gen Psychiatry 58:909-915 (Pubitemid 32937912)
42. Rhee MH, Nevo I, Avidor-Reiss T, Levy R, Vogel Z (2000) Differential superactivation of adenylyl cyclase isozymes after chronic activation of the CB(1) cannabinoid receptor. Mol Pharmacol 57:746-752 (Pubitemid 30183715)
43. Robinson L, McKillop-Smith S, Ross NL, Pertwee RG, Hampson RE, Platt B, Riedel G (2008) Hippocampal endocannabinoids inhibit spatial learning and limit spatial memory in rats. Psychopharmacology (Berl) 198:551-563
44. Rubino T, Massi P, Vigano D, Fuzio D, Parolaro D (2000a) Long-term treatment with SR141716A, the CB1 receptor antagonist, influences morphine withdrawal syndrome. Life Sci 66:2213-2219 (Pubitemid 30313088)
45. Rubino T, Vigano D, Massi P, Spinello M, Zagato E, Giagnoni G, Parolaro D (2000b) Chronic delta-9-tetrahydrocannabinol treatment increases cAMP levels and cAMP-dependent protein kinase activity in some rat brain regions [in process citation]. Neuropharmacology 39:1331-1336 (Pubitemid 30173197)
46. Rubino T, Vigano D, Zagato E, Sala M, Parolaro D (2000c) In vivo characterization of the specific cannabinoid receptor antagonist, SR141716A: behavioral and cellular responses after acute and chronic treatments. Synapse 35:8-14
47. Sacchetti B, Baldi E, Lorenzini CA, Bucherelli C (2002) Cerebellar role in fear-conditioning consolidation. Proc Natl Acad Sci USA 99:8406-8411 (Pubitemid 34651065)
48. Salomon Y (1979) Adenylate cyclase assay. Adv Cyclic Nucleotide Res 10:35-55
49. Schlosburg JE, Carlson BL, Ramesh D, Abdullah RA, Long JZ, Cravatt BF, Lichtman AH (2009) Inhibitors of endocannabinoidmetabolizing enzymes reduce precipitated withdrawal responses in THC-dependent mice. AAPS J 11:342-352
50. Schwartz RH, Gruenewald PJ, Klitzner M, Fedio P (1989) Short-term memory impairment in cannabis-dependent adolescents. Am J Dis Child 143:1214-1219 (Pubitemid 19246194)
51. , Cassidy MP, Martin BR, Sim-Selley LJ (2004) Long-term administration of Delta9-tetrahydrocannabinol desensitizes CB1-, adenosine A1-, and GABAB-mediated inhibition of adenylyl cyclase in mouse cerebellum. Mol Pharmacol 66:1275-1284 (Pubitemid 39411067)
52. Sim-Selley LJ, Brunk LK, Selley DE (2001) Inhibitory effects of SR141716A on G-protein activation in rat brain. Eur J Pharmacol 414:135-143 (Pubitemid 32181880)
53. Solowij N, Stephens RS, Roffman RA, Babor T, Kadden R, Miller M, Christiansen K, McRee B, Vendetti J (2002) Cognitive functioning of long-term heavy cannabis users seeking treatment. JAMA 287:1123-1131 (Pubitemid 34252081)
54. Substance Abuse and Mental Health Services Administration (SAMHSA). (2010). Results from the 2009 National Survey on Drug Use and Health: Volume I. Summary of National Findings (Office of Applied Studies, NSDUH Series H-38A, HHS Publication No. SMA 10-4586Findings). Rockville, MD
55. Terranova JP, Storme JJ, Lafon N, Perio A, Rinaldi-Carmona M, Le Fur G, Soubrie P (1996) Improvement of memory in rodents by the selective CB1 cannabinoid receptor antagonist, SR 141716. Psychopharmacol 126:165-172 (Pubitemid 26246767)
56. Thompson RF, Steinmetz JE (2009) The role of the cerebellum in classical conditioning of discrete behavioral responses. Neuroscience 162:732-755
57. Tsou K, Patrick S, Walker JM (1995) Physical withdrawal in rats tolerant to D9-tetrahydrocannabinol precipitated by a cannabinoid receptor antagonist. Eur J Pharmacol 280:R13-R15
58. Tzavara ET, Valjent E, Firmo C, Mas M, Beslot F, Defer N, Roques BP, Hanoune J, Maldonado R (2000) Cannabinoid withdrawal is dependent upon PKA activation in the cerebellum. Eur J Neurosci 12:1038-1046 (Pubitemid 30168783)
59. Vandrey R, Budney AJ, Kamon JL, Stanger C (2005) Cannabis withdrawal in adolescent treatment seekers. Drug Alcohol Depend 78:205-210 (Pubitemid 40544608)
60. Vandrey RG, Budney AJ, Hughes JR, Liguori A (2008) A withinsubject comparison of withdrawal symptoms during abstinence from cannabis, tobacco, to both substances. Drug Alcohol Depend 92:48-54 (Pubitemid 350213236)
61. Varvel SA, Lichtman AH (2002) Evaluation of CB1 receptor knockout mice in theMorris water maze. J Pharmacol Exp Ther 301:915-924 (Pubitemid 34595080)
62. Varvel SA, Anum EA, Lichtman AH (2005) Disruption of CB(1) receptor signaling impairs extinction of spatial memory in mice. Psychopharmacology (Berl) 179:863-872 (Pubitemid 40767906)
63. Varvel SA, Cravatt BF, Engram AE, Lichtman AH (2006) Fatty acid amide hydrolase (?/?) mice exhibit an increased sensitivity to the disruptive effects of anandamide or oleamide in a working memory water maze task. J Pharmacol Exp Ther 317:251-257
64. Wilson DM, Varvel SA, Harloe JP, Martin BR, Lichtman AH (2006) SR 141716 (Rimonabant) precipitates withdrawal in marijuanadependent mice. Pharmacol Biochem Behav 85:105-113 (Pubitemid 44773724)
65. Wise LE, Iredale PA, Stokes RJ, Lichtman AH (2007) Combination of rimonabant and donepezil prolongs spatial memory duration. Neuropsychopharmacology 32:1805-1812 (Pubitemid 47076380)
66. Wolff MC, Leander JD (2003) SR141716A, a cannabinoid CB1 receptor antagonist, improves memory in a delayed radial maze task. Eur J Pharmacol 477:213-217 (Pubitemid 38366393)