Persistent effects of chronic Δ9-THC exposure on motor impulsivity in rats

Psychopharmacology

Volumn 232, Issue 16, 2015, Pages 3033-3043

  Irimia, Cristina ^a   Polis, Ilham Y ^a   Stouffer, David ^a   Parsons, Loren H ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

5 Choice Serial Reaction Time Task; Attention; Cognitive impairment; Impulsivity; Marijuana

Indexed keywords

TETRAHYDROCANNABINOLIC ACID; CANNABINOID RECEPTOR AGONIST; DRONABINOL;

ANIMAL EXPERIMENT; ARTICLE; ATTENTION DISTURBANCE; BEHAVIOR DISORDER; CONTROLLED STUDY; DRUG DEPENDENCE; IMPULSIVENESS; LONG TERM EXPOSURE; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; TASK PERFORMANCE; WITHDRAWAL SYNDROME; ANIMAL; ATTENTION; DECISION MAKING; DOSE RESPONSE; DRUG EFFECTS; INHIBITION (PSYCHOLOGY); MOTOR ACTIVITY; REACTION TIME; WISTAR RAT;

ANIMALS; ATTENTION; CANNABINOID RECEPTOR AGONISTS; CHOICE BEHAVIOR; DOSE-RESPONSE RELATIONSHIP, DRUG; DRONABINOL; IMPULSIVE BEHAVIOR; INHIBITION (PSYCHOLOGY); MALE; MOTOR ACTIVITY; RATS; RATS, WISTAR; REACTION TIME;

EID: 84937971654     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-015-3942-x     Document Type: Article

References (63)

1. Azorlosa JL, Heishman SJ, Stitzer ML, Mahaffey JM (1992) Marijuana smoking: effect of varying delta 9-tetrahydrocannabinol content and number of puffs. J Pharmacol Exp Ther 261:114-122
2. Bari A, Dalley JW, Robbins TW (2008) The application of the 5-choice serial reaction time task for the assessment of visual attentional processes and impulse control in rats. Nat Protoc 3:759-767
3. Battistella G, Fornari E, Annoni J-M, Chtioui H, Dao K, Fabritius M, Favrat B, Mall J-F, Maeder P, Giroud C (2014) Long-term effects of cannabis on brain structure. Neuropsychopharmacology 39:2041-2048
4. Bidwell L, Henry E, Willcutt E, Kinnear M, Ito T (2014) Childhood and current ADHD symptom dimensions are associated with more severe cannabis outcomes in college students. Drug Alcohol Depend 135:88-94
5. Bolla KI, Eldreth DA, Matochik JA, Cadet JL (2005) Neural substrates of faulty decision-making in abstinent marijuana users. Neuroimage 26:480-492
6. Borgelt LM, Franson KL, Nussbaum AM, Wang GS (2013) The pharmacologic and clinical effects of medical cannabis. Pharmacotherapy 33:195-209
7. Caberlotto L, Rimondini R, Hansson A, Eriksson S, Heilig M (2004) Corticotropin-releasing hormone (CRH) mRNA expression in rat central amygdala in cannabinoid tolerance and withdrawal: evidence for an allostatic shift? Neuropsychopharmacology 29:15-22
8. Cascini F, Aiello C, Di Tanna G (2012) Increasing delta-9-tetrahydrocannabinol (Δ-9-THC) content in herbal cannabis over time: systematic review and meta-analysis. Curr Drug Abuse Rev 5:32-40
9. Chee P, Logan G, Schachar R, Lindsay P, Wachsmuth R (1989) Effects of event rate and display time on sustained attention in hyperactive, normal, and control children. J Abnorm Child Psychol 17:371-391
10. Churchwell JC, Lopez-Larson M, Yurgelun-Todd DA (2010) Altered frontal cortical volume and decision making in adolescent cannabis users. Front Psychol 1:1-8
11. Cone EJ, Huestis MA (1993) Relating blood concentrations of tetrahydrocannabinol and metabolites to pharmacologic effects and time of marijuana usage. Ther Drug Monit 15:527-532
12. Crean RD, Crane NA, Mason BJ (2011a) An evidence based review of acute and long-term effects of cannabis use on executive cognitive functions. J Addict Med 5:1
13. Crean RD, Tapert SF, Minassian A, MacDonald K, Crane NA, Mason BJ (2011b) Effects of chronic, heavy cannabis use on executive functions. J Addict Med 5:9
14. Cunha PJ, Nicastri S, de Andrade AG, Bolla KI (2010) The frontal assessment battery (FAB) reveals neurocognitive dysfunction in substance-dependent individuals in distinct executive domains: abstract reasoning, motor programming, and cognitive flexibility. Addict Behav 35:875-881
15. Dalley JW, Mar AC, Economidou D, Robbins TW (2008) Neurobehavioral mechanisms of impulsivity: fronto-striatal systems and functional neurochemistry. Pharmacol Biochem Behav 90:250-260
16. Dalley JW, Everitt BJ, Robbins TW (2011) Impulsivity, compulsivity, and top-down cognitive control. Neuron 69:680-694
17. De Wit H (2008) Impulsivity as a determinant and consequence of drug use: a review of underlying processes. Addict Biol 14:22-31
18. Eagle DM, Baunez C (2010) Is there an inhibitory-response-control system in the rat? Evidence from anatomical and pharmacological studies of behavioral inhibition. Neurosci Biobehav Rev 34:50-72
19. Eldreth DA, Matochik JA, Cadet JL, Bolla KI (2004) Abnormal brain activity in prefrontal brain regions in abstinent marijuana users. Neuroimage 23:914-920
20. Evenden JL (1999) Varieties of impulsivity. Psychopharmacology (Berl) 146:348-361
21. Fadda P, Robinson L, Fratta W, Pertwee RG, Riedel G (2004) Differential effects of THC-or CBD-rich cannabis extracts on working memory in rats. Neuropharmacology 47:1170-1179
22. Fineberg NA, Potenza MN, Chamberlain SR, Berlin HA, Menzies L, Bechara A, Sahakian BJ, Robbins TW, Bullmore ET, Hollander E (2010) Probing compulsive and impulsive behaviors, from animal models to endophenotypes: a narrative review. Neuropsychopharmacology 35:591-604
23. Fletcher JM, Page JB, Francis DJ, Copeland K, Naus MJ, Davis CM, Morris R, Krauskopf D, Satz P (1996) Cognitive correlates of long-term cannabis use in Costa Rican men. Arch Gen Psychiatry 53:1051
24. Freeman TP, Morgan CJ, Hindocha C, Schafer G, Das RK, Curran HV (2014) Just say 'know': how do cannabinoid concentrations influence users' estimates of cannabis potency and the amount they roll in joints? Addiction 109:1686-1694
25. Goldstein RZ, Volkow ND (2011) Dysfunction of the prefrontal cortex in addiction: neuroimaging findings and clinical implications. Nat Rev Neurosci 12:652-669
26. Grotenhermen F (2003) Pharmacokinetics and pharmacodynamics of cannabinoids. Clin Pharmacokinet 42:327-360
27. Gruber SA, Yurgelun-Todd DA (2005) Neuroimaging of marijuana smokers during inhibitory processing: a pilot investigation. Cogn Brain Res 23:107-118
28. Han C, Robinson JK (2001) Cannabinoid modulation of time estimation in the rat. Behav Neurosci 115:243
29. Hanson KL, Winward JL, Schweinsburg AD, Medina KL, Brown SA, Tapert SF (2010) Longitudinal study of cognition among adolescent marijuana users over three weeks of abstinence. Addict Behav 35:970-976
30. Hester R, Nestor L, Garavan H (2009) Impaired error awareness and anterior cingulate cortex hypoactivity in chronic cannabis users. Neuropsychopharmacology 34:2450-2458
31. Irimia C, Wiskerke J, Natividad LA, Polis IY, de Vries TJ, Pattij T, Parsons LH (2015) Increased impulsivity in rats as a result of repeated cycles of alcohol intoxication and abstinence. Addict Biol 20:263-274
32. Jager G, Block RI, Luijten M, Ramsey NF (2010) Cannabis use and memory brain function in adolescent boys: a cross-sectional multicenter functional magnetic resonance imaging study. J Am Acad Child Adolesc Psychiatry 49:561-572, e563
33. Lichtman AH, Martin BR (2002) Marijuana withdrawal syndrome in the animal model. J Clin Pharmacol 42:20S-27S
34. Lundqvist T (2005) Cognitive consequences of cannabis use: comparison with abuse of stimulants and heroin with regard to attention, memory and executive functions. Pharmacol Biochem Behav 81:319-330
35. Lyvers M, Jamieson R, Thorberg FA (2013) Risky cannabis use is associated with alexithymia, frontal lobe dysfunction, and impulsivity in young adult cannabis users. J Psychoactive Drugs 45:394-403
36. Mason BJ, Crean R, Goodell V, Light JM, Quello S, Shadan F, Buffkins K, Kyle M, Adusumalli M, Begovic A (2012) A proof-of-concept randomized controlled study of gabapentin: effects on cannabis use, withdrawal and executive function deficits in cannabis-dependent adults. Neuropsychopharmacology 37:1689-1698
37. McDonald J, Schleifer L, Richards JB, de Wit H (2003) Effects of THC on behavioral measures of impulsivity in humans. Neuropsychopharmacology 28:1356-1365
38. Mehmedic Z, Chandra S, Slade D, Denham H, Foster S, Patel AS, Ross SA, Khan IA, ElSohly MA (2010) Potency trends of Δ9-THC and other cannabinoids in confiscated cannabis preparations from 1993 to 2008. J Forensic Sci 55:1209-1217
39. Meier MH, Caspi A, Ambler A, Harrington H, Houts R, Keefe RS, McDonald K, Ward A, Poulton R, Moffitt TE (2012) Persistent cannabis users show neuropsychological decline from childhood to midlife. Proc Natl Acad Sci U S A 109:E2657-E2664
40. Murphy ER, Fernando AB, Urcelay GP, Robinson ES, Mar AC, Theobald DE, Dalley JW, Robbins TW (2012) Impulsive behaviour induced by both NMDA receptor antagonism and GABAA receptor activation in rat ventromedial prefrontal cortex. Psychopharmacology (Berl) 219:401-410
41. Nakamura EM, Da Silva EA, Concilio GV, Adrian Wilkinson D, Masur J (1991) Reversible effects of acute and long-term administration of Δ-9-tetrahydrocannabinol (THC) on memory in the rat. Drug Alcohol Depend 28:167-175
42. Niesink RJ, van Laar MW (2013) Does cannabidiol protect against adverse psychological effects of THC? Front Psychiatry 4:130
43. O'Shea M, Singh ME, McGregor IS, Mallet PE (2004) Chronic cannabinoid exposure produces lasting memory impairment and increased anxiety in adolescent but not adult rats. J Psychopharmacol 18:502-508
44. Oleson EB, Cachope R, Fitoussi A, Tsutsui K, Wu S, Gallegos JA, Cheer JF (2014) Cannabinoid receptor activation shifts temporally engendered patterns of dopamine release. Neuropsychopharmacology 39:1441-1452
45. Pattij T, Janssen MW, Schepers I, González-Cuevas G, Vries T, Schoffelmeer AM (2007) Effects of the cannabinoid CB1 receptor antagonist rimonabant on distinct measures of impulsive behavior in rats. Psychopharmacology (Berl) 193:85-96
46. Pope HG, Gruber AJ, Hudson JI, Huestis MA, Yurgelun-Todd D (2001) Neuropsychological performance in long-term cannabis users. Arch Gen Psychiatry 58:909-915
47. Riccio CA, Reynolds CR, Lowe P, Moore JJ (2002) The continuous performance test: a window on the neural substrates for attention? Arch Clin Neuropsychol 17:235-272
48. Robbins T (2002) The 5-choice serial reaction time task: behavioural pharmacology and functional neurochemistry. Psychopharmacology (Berl) 163:362-380
49. SAMHSA (2013) Substance Abuse and Mental Health Services Administration, Results from the 2012 National Survey on Drug Use and Health: Summary of National Findings. Substance Abuse and Mental Health Services Administration, 2013, Rockville
50. Sanchez-Roige S, Baro V, Trick L, Pena-Oliver Y, Stephens DN, Duka T (2014) Exaggerated waiting impulsivity associated with human binge drinking, and high alcohol consumption in mice. Neuropsychopharmacology 39:2919-2927
51. Schreiner AM, Dunn ME (2012) Residual effects of cannabis use on neurocognitive performance after prolonged abstinence: a meta-analysis. Exp Clin Psychopharmacol 20:420-429
52. Swartzwelder NA, Risher ML, Abdelwahab SH, D'Abo A, Rezvani AH, Levin ED, Wilson WA, Swartzwelder HS, Acheson SK (2012) Effects of ethanol, Δ∈<∈∈>∈9<∈>∈-tetrahydrocannabinol, or their combination on object recognition memory and object preference in adolescent and adult male rats. Neurosci Lett 527:11-15
53. Tapert SF, Schweinsburg AD, Drummond SP, Paulus MP, Brown SA, Yang TT, Frank LR (2007) Functional MRI of inhibitory processing in abstinent adolescent marijuana users. Psychopharmacology (Berl) 194:173-183
54. Valiveti S, Hammell DC, Earles DC, Stinchcomb AL (2004) In vitro/in vivo correlation studies for transdermal Δ8-THC development. J Pharm Sci 93:1154-1164
55. 9-tetrahydrocannabinol administration to rats impairs acquisition and performance of a test of visuospatial divided attention. Neuropsychopharmacology 29:522-529
56. Verrico CD, Liu S, Bitler EJ, Gu H, Sampson AR, Bradberry CW, Lewis DA (2012) Delay-and dose-dependent effects of Δ9-tetrahydrocannabinol administration on spatial and object working memory tasks in adolescent rhesus monkeys. Neuropsychopharmacology 37:1357-1366
57. Verrico CD, Gu H, Peterson ML, Sampson AR, Lewis DA (2014) Repeated Δ9-tetrahydrocannabinol exposure in adolescent monkeys: persistent effects selective for spatial working memory. Am J Psychiatry 171:416-425
58. Voon V, Irvine MA, Derbyshire K, Worbe Y, Lange I, Abbott S, Morein-Zamir S, Dudley R, Caprioli D, Harrison NA (2014) Measuring "waiting" impulsivity in substance addictions and binge eating disorder in a novel analogue of rodent serial reaction time task. Biol Psychiatry 75:148-155
59. Wadsworth E, Moss S, Simpson S, Smith A (2006) Cannabis use, cognitive performance and mood in a sample of workers. J Psychopharmacol 20:14-23
60. Wise L, Varvel S, Selley D, Wiebelhaus J, Long K, Middleton L, Sim-Selley L, Lichtman A (2011) δ9-Tetrahydrocannabinol-dependent mice undergoing withdrawal display impaired spatial memory. Psychopharmacology (Berl) 217:485-494
61. Wiskerke J, Stoop N, Schetters D, Schoffelmeer AN, Pattij T (2011) Cannabinoid CB1 receptor activation mediates the opposing effects of amphetamine on impulsive action and impulsive choice. PLoS One 6, e25856
62. Wiskerke J, Van Mourik Y, Schetters D, Schoffelmeer AN, Pattij T (2012) On the role of cannabinoid CB1-and μ-opioid receptors in motor impulsivity. Front Pharmacol 3:8
63. Zuardi A, Shirakawa I, Finkelfarb E, Karniol I (1982) Action of cannabidiol on the anxiety and other effects produced by Δ9-THC in normal subjects. Psychopharmacology (Berl) 76:245-250