Part II: Strain- and sex-specific effects of adolescent exposure to THC on adult brain and behaviour: Variants of learning, anxiety and volumetric estimates

Behavioural Brain Research

Volumn 288, Issue , 2015, Pages 132-152

  Keeley, R J ^a   Trow, J ^a   Bye, C ^a   McDonald, R J ^a  

^a UNIVERSITY OF LETHBRIDGE   (Canada)

Author keywords

Behavior; Brain volumetrics; Rat; Sex; Strain; THC

Indexed keywords

DRONABINOL; PSYCHOTROPIC AGENT;

AGING; ANATOMY AND HISTOLOGY; ANIMAL; ANXIETY; BRAIN; DRUG EFFECTS; FEMALE; GROWTH, DEVELOPMENT AND AGING; LEARNING; LONG EVANS RAT; MALE; MEMORY; MOTOR PERFORMANCE; ORGAN SIZE; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGIC TEST; PSYCHOLOGY; SEXUAL DEVELOPMENT; SPECIES DIFFERENCE; WISTAR RAT;

AGING; ANIMALS; ANXIETY; BRAIN; DRONABINOL; FEMALE; LEARNING; MALE; MEMORY; MOTOR SKILLS; ORGAN SIZE; PSYCHOLOGICAL TESTS; PSYCHOTROPIC DRUGS; RATS, LONG-EVANS; RATS, WISTAR; SEX CHARACTERISTICS; SPECIES SPECIFICITY;

EID: 84937761413     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2015.01.001     Document Type: Article

References (90)

1. Health Canada Canadian Alcohol and Drug Use Monitoring Survey: summary of results for 2012. Ottawa, Canada 2013.
2. Solowij N., Battisti R. The chronic effects of cannabis on memory in humans: a review. Curr Drug Abuse Rev 2008, 1:81-98.
3. Schneider M. Puberty as a highly vulnerable developmental period for the consequences of cannabis exposure. Addict Biol 2008, 13:253-263.
4. Rubino T., Zamberletti E., Parolaro D. Adolescent exposure to cannabis as a risk factor for psychiatric disorders. J Psychopharmacol (Oxf) 2012, 26:177-188.
5. Patton G.C., Coffey C., Carlin J.B., Degenhardt L., Lynskey M., Hall W. Cannabis use and mental health in young people: cohort study. Br Med J 2002, 325:1195-1198.
6. Viveros M.P., Marco E.M., Lopez-Gallardo M., Garcia-Segura L.M., Wagner E.J. Framework for sex differences in adolescent neurobiology: a focus on cannabinoids. Neurosci Biobehav Rev 2011, 35:1740-1751.
7. Ashton C.H. Pharmacology and effects of cannabis: a brief review. Br J Psychiatry 2001, 178:101-106.
8. Abood M.E., Martin B.R. Neurobiology of marijuana abuse. Trends Pharmacol Sci 1992, 13:201-206.
9. Razdan R.K. Structure-activity relationships in cannabinoids. Pharm Rev 1986, 38:75-149.
10. Berry E.M., Mechoulam R. Tetrahydrocannabinol and endocannabinoids in feeding and appetite. Pharmacol Ther 2002, 95:185-190.
11. Mailleux P., Vanderhaeghen J.J. Distribution of neuronal cannabinoid receptor in the adult-rat brain - a comparative receptor-binding autoradiography and in situ hybridization histochemistry. Neuroscience 1992, 48:655-668.
12. Mackie K. Distribution of cannabinoid receptors in the central and peripheral nervous system. Handb Exp Pharmacol 2005, 29:9-325.
13. Herkenham M., Lynn A.B., Little M.D., Johnson M.R., Melvin L.S., Decosta B.R., et al. Cannabinoid receptor localization in brain. Proc Natl Acad Sci U S A 1990, 87:1932-1936.
14. Wilson R.I., Nicoll R.A. Endocannabinoid signaling in the brain. Science 2002, 296:678-682.
15. Marsicano G., Lutz B. Neuromodulatory functions of the endocannabinoid system. J Endocrinol Invest 2006, 29:27-46.
16. Piomelli D. The molecular logic of endocannabinoid signalling. Nat Rev Neurosci 2003, 4:873-884.
17. Marsicano G., Lutz B. Expression of the cannabinoid receptor CB1 in distinct neuronal subpopulations in the adult mouse forebrain. Eur J Neurosci 1999, 11:4213-4225.
18. Freund T.F., Katona I., Piomelli D. Role of endogenous cannabinoids in synaptic signaling. Physiol Rev 2003, 83:1017-1066.
19. Moreira F.A., Grieb M., Lutz B. Central side-effects of therapies based on CB1 cannabinoid receptor agonists and antagonists: focus on anxiety and depression. Best Pract Res Clin Endocrinol Metab 2009, 23:133-144.
20. Ruehle S., Rey A.A., Remmers F., Lutz B. The endocannabinoid system in anxiety, fear memory and habituation. J Psychopharmacol (Oxf) 2012, 26:23-39.
21. Herkenham M., Lynn A.B., Johnson M.R., Melvin L.S., de Costa B.R., Rice K.C. Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J Neurosci 1991, 11:563-583.
22. Mailleux P., Vanderhaeghen J.J. Distribution of neuronal cannabinoid receptor in the adult rat brain: a comparative receptor binding radioautography and in situ hybridization histochemistry. Neuroscience 1992, 48:655-668.
23. Cha Y.M., Jones K.H., Kuhn C.M., Wilson W.A., Swartzwelder H.S. Sex differences in the effects of Delta(9)-tetrahydrocannabinol on spatial learning in adolescent and adult rats. Behav Pharmacol 2007, 18:563-569.
24. O'Shea M., Singh M.E., McGregor I.S., Mallet P.E. Chronic cannabinoid exposure produces lasting memory impairment and increased anxiety in adolescent but not adult rats. J Psychopharmacol 2004, 18:502-508.
25. Rubino T., Guidali C., Vigano D., Realini N., Valenti M., Massi P., et al. CB1 receptor stimulation in specific brain areas differently modulate anxiety-related behaviour. Neuropharmacology 2008, 54:151-160.
26. Rubino T., Realini N., Braida D., Alberio T., Capurro V., Virgano 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. Neurotoxicity Res 2009, 15:291-302.
27. Rubino T., Realini N., Braida D., Guidi S., Capurro V., Vigano 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.
28. 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 2008, 33:2760-2771.
29. Cha Y.M., Jones K.H., Kuhn C.M., Wilson W.A., Swartzwelder H.S. Sex differences in the effects of delta9-tetrahydrocannabinol on spatial learning in adolescent and adult rats. Behav Pharmacol 2007, 18:563-569.
30. Keeley R.J., Trow J., McDonald R.J. Rat strain and sex differences in post-pubertal development and brain volumetrics. Physiol Behav 2015, [submitted for publication].
31. Harris G.C., Levine J.E. Pubertal acceleration of pulsatile gonadotropin-releasing hormone release in male rats as revealed by microdialysis. Endocrinology 2003, 144:163-171.
32. Ojeda S.R., Prevot V., Heger S., Lomniczi A., Dziedzic B., Mungenast A. Glia-to-neuron signaling and the neuroendocrine control of female puberty. Ann Med 2003, 35:244-255.
33. Wenger T., Croix D., Tramu G. The effect of chronic prepubertal administration of marihuana (delta-9-tetrahydrocannabinol) on the onset of puberty and the postpubertal reproductive functions in female rats. Biol Reprod 1988, 39:540-545.
34. Beery A.K., Zucker I. Sex bias in neuroscience and biomedical research. Neurosci Biobehav Rev 2011, 35:565-572.
35. Check Hayden E. Sex bias blights drug studies. Nature 2010, 464:332-333.
36. Hall W., Solowij N. Adverse effects of cannabis. Lancet 1998, 352:1611-1616.
37. Narimatsu S., Watanabe K., Matsunaga T., Yamamoto I., Imaoka S., Funae Y., et al. Cytochrome P-450 isozymes involved in the oxidative metabolism of delta 9-tetrahydrocannabinol by liver microsomes of adult female rats. Drug Metab Dispos 1992, 20:79-83.
38. Narimatsu S., Watanabe K., Yamamoto I., Yoshimura H. Sex difference in the oxidative metabolism of delta 9-tetrahydrocannabinol in the rat. Biochem Pharmacol 1991, 41:1187-1194.
39. Holahan M.R., Rekart J.L., Sandoval J., Routtenberg A. Spatial learning induces presynaptic structural remodeling in the hippocampal mossy fiber system of two rat strains. Hippocampus 2006, 16:560-570.
40. Keeley R.J., Wartman B.C., Hausler A.N., Holahan M.R. Effect of juvenile pretraining on adolescent structural hippocampal attributes as a substrate for enhanced spatial performance. Learn Mem (Cold Spring Harbor, NY) 2010, 17:344-354.
41. Antoniadis E.A., McDonald R.J. Amygdala, hippocampus and discriminative fear conditioning to context. Behav Brain Res 2000, 109:141-142.
42. Gonzalez B., de Miguel R., Martin S., Perez-Rosado A., Romero J., Garcia-Lecumberri C., et al. Effects of perinatal exposure to Delta(9)-tetrahydrocannabinol on operant morphine-reinforced behavior. Pharmacol Biochem Behav 2003, 75:577-584.
43. Gonzalez S., Bisogno T., Wenger T., Manzanares J., Milone A., Berrendero F., et al. Sex steroid influence on cannabinoid CB1 receptor mRNA and endocannabinoid levels in the anterior pituitary gland. Biochem Biophys Res Commun 2000, 270:260-266.
44. Navarro M., Rubio P., Defonseca F.R. Sex-dimorphic psychomotor activation after perinatal exposure to (-)-delta(9)-tetrahydrocannabinol - an ontogenic study in Wistar rats. Psychopharmacology (Berl) 1994, 116:414-422.
45. Valjent E., Maldonado R. A behavioural model to reveal place preference to Delta 9-tetrahydrocannabinol in mice. Psychopharmacology (Berl) 2000, 147:436-438.
46. Keeley R.J., Bye C., Trow J., McDonald R.J. Part I: Strain and sex differences in brain and behaviour of adult rats: learning and memory, anxiety and volumetric estimates. Behav Brain Res 2015, [in press].
47. Korenbrot C.C., Huhtaniemi I.T., Weiner R.I. Preputial separation as an external sign of pubertal development in the male rat. Biol Reprod 1977, 17:298-303.
48. Parker C.R., Mahesh V.B. Hormonal events surrounding the natural onset of puberty in female rats. Biol Reprod 1976, 14:347-353.
49. Goldman J.M., Murr A.S., Cooper R.L. The rodent estrous cycle: characterization of vaginal cytology and its utility in toxicological studies. Birth Defect Res Part B: Dev Reprod Toxicol 2007, 80:84-97.
50. Marcondes F.K., Bianchi F.J., Tanno A.P. Determination of the estrous cycle phases of rats: some helpful considerations. Braz J Biol 2002, 62:609-614.
51. Metz G.A., Whishaw I.Q. Skilled reaching an action pattern: stability in rat (Rattus norvegicus) grasping movements as a function of changing food pellet size. Behav Brain Res 2000, 116:111-122.
52. Amtul Z., Nikolova S., Gao L., Keeley R., Bechberger J., Fisher A., et al. Co-morbid Aβ toxicity and stroke: hippocampal atrophy, pathology and cognitive deficit. Neurobiol Aging 2014, 35:1605-1614.
53. Keeley R.J., Zelinski E.L., Fehr L., McDonald R.J. The effect of exercise on carbohydrate preference in female rats. Brain Res Bull 2014, 101:45-50.
54. Antoniadis E.A., Ko C.H., Ralph M.R., McDonald R.J. Circadian rhythms, aging and memory. Behav Brain Res 2000, 114:221-233.
55. Antoniadis E.A., McDonald R.J. Discriminative fear conditioning to context expressed by multiple measures of fear in the rat. Behav Brain Res 1999, 101:1-13.
56. Craig L.A., McDonald R.J. Chronic disruption of circadian rhythms impairs hippocampal memory in the rat. Brain Res Bull 2008, 76:141-151.
57. Muhammad A., Mychasiuk R., Hosain S., Nakahashi A., Carroll C., Gibb R., et al. Training on motor and visual spatial learning tasks in early adulthood produces large changes in dendritic organization of prefrontal cortex and nucleus accumbens in rats given nicotine prenatally. Neuroscience 2013, 252:178-189.
58. Gundersen H.J.G., Jensen E.B.V., Kieu K., Nielsen J. The efficiency of systematic sampling in stereology-reconsidered. J Microsc - Oxford 1999, 193:199-211.
59. Garcia-Finana M., Cruz-Orive L.M., Mackay C.E., Pakkenberg B., Roberts N. Comparison of MR imaging against physical sectioning to estimate the volume of human cerebral compartments. Neuroimage 2003, 18:505-516.
60. Gundersen H.J., Jensen E.B., Kieu K., Nielsen J. The efficiency of systematic sampling in stereology - reconsidered. J Microsc 1999, 193:199-211.
61. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 2007, Academic Press, USA.
62. Hallgren K.A. Computing inter-rater reliability for observational data: an overview and tutorial. Tutor Quant Methods Psychol 2012, 8:23-34.
63. Keeley R.J., Tyndall A.V., Scott G.A., Saucier D.M. Sex difference in cue strategy in a modified version of the Morris water task: correlations between brain and behaviour. PLOS ONE 2013, 8:e69727.
64. Patel S., Hillard C.J. Pharmacological evaluation of cannabinoid receptor ligands in a mouse model of anxiety: Further evidence for an anxiolytic role for endogenous cannabinoid signaling. J Pharmacol Exp Ther 2006, 318:304-311.
65. Viveros M.P., Marco E.M., File S.E. Endocannabinoid system and stress and anxiety responses. Pharmacol Biochem Behav 2005, 81:331-342.
66. Thomas H. A community survey of adverse effects of cannabis use. Drug Alcohol Depend 1996, 42:201-207.
67. Wegener N., Koch M. Behavioural disturbances and altered Fos protein expression in adult rats after chronic pubertal cannabinoid treatment. Brain Res 2009, 1253:81-91.
68. Adhikari A. Distributed circuits underlying anxiety. Front Behav Neurosci 2014, 8:112.
69. Fanselow M.S., Dong H-W. Are the dorsal and ventral hippocampus functionally distinct structures. Neuron 2010, 65:7-19.
70. Shin L.M., Liberzon I. The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology 2010, 35:169-191.
71. Markou A., Arroyo M., Everitt B.J. Effects of contingent and non-contingent cocaine on drug-seeking behavior measured using a second-order schedule of cocaine reinforcement in rats. Neuropsychopharmacology 1999, 20:542-555.
72. Maldonado R., Rodriguez de Fonseca F. Cannabinoid addiction: behavioral models and neural correlates. J Neurosci 2002, 22:3326-3331.
73. Takahashi R.N., Singer G. Self-administration of delta 9-tetrahydrocannabinol by rats. Pharmacol Biochem Behav 1979, 11:737-740.
74. Fattore L., Cossu G., Martellotta C.M., Fratta W. Intravenous self-administration of the cannabinoid CB1 receptor agonist WIN 55,212-2 in rats. Psychopharmacology (Berl) 2001, 156:410-416.
75. Carobrez A.P., Bertoglio L.J. Ethological and temporal analyses of anxiety-like behavior: the elevated plus-maze model 20 years on. Neurosci Biobehav Rev 2005, 29:1193-1205.
76. Hogg S. A review of the validity and variability of the elevated plus-maze as an animal model of anxiety. Pharmacol Biochem Behav 1996, 54:21-30.
77. Wall P.M., Messier C. Methodological and conceptual issues in the use of the elevated plus-maze as a psychological measurement instrument of animal anxiety-like behavior. Neurosci Biobehav Rev 2001, 25:275-286.
78. Weiss S.M., Wadsworth G., Fletcher A., Dourish C.T. Utility of ethological analysis to overcome locomotor confounds in elevated maze models of anxiety. Neurosci Biobehav Rev 1998, 23:265-271.
79. Jiang W., Zhang Y., Xiao L., Van Cleemput J., Ji S.P., Bai G., et al. Cannabinoids promote embryonic and adult hippocampus neurogenesis and produce anxiolytic- and antidepressant-like effects. J Clin Invest 2005, 115:3104-3116.
80. Keeley R.J., Trow J., McDonald R.J. The immediate effects of THC administration on weight gain and brain volume in female and male Long-Evans and Wistar rats. Physiol Behav 2015, [submitted for publication].
81. Smith A.M., Longo C.A., Fried P.A., Hogan M.J., Cameron I. Effects of marijuana on visuospatial working memory: an fMRI study in young adults. Psychopharmacology (Berl) 2010, 210:429-438.
82. Smith A.M., Zunini R.A.L., Anderson C.D., Longo C.A., Cameron I., Hogan M.J., et al. Impact of marijuana on response inhibition: an fMRI study in young adults. J Behav Brain Sci 2011, 1:124.
83. Smith M.J., Cobia D.J., Wang L., Alpert K.I., Cronenwett W.J., Goldman M.B., et al. Cannabis-related working memory deficits and associated subcortical morphological differences in healthy individuals and schizophrenia subjects. Schizophr Bull 2014, 40:287-299.
84. Solowij N., Walterfang M., Lubman D.I., Whittle S., Lorenzetti V., Styner M., et al. Alteration to hippocampal shape in cannabis users with and without schizophrenia. Schizophr Res 2013, 143:179-184.
85. Takahashi L.K., Haglin C., Kalin N.H. Prenatal stress potentiates stress-induced behavior and reduces the propensity to play in juvenile rats. Physiol Behav 1992, 51:319-323.
86. Takahashi L.K., Turner J.G., Kalin N.H. Prenatal stress alters brain catecholaminergic activity and potentiates stress-induced behavior in adult rats. Brain Res 1992, 574:131-137.
87. Weinstock M. Gender differences in the effects of prenatal stress on brain development and behaviour. Neurochem Res 2007, 32:1730-1740.
88. Weinstock M. Sex-dependent changes induced by prenatal stress in cortical and hippocampal morphology and behaviour in rats: an update. Stress (Amsterdam, Netherlands) 2011, 14:604-613.
89. Romeo R.D. Adolescence: a central event in shaping stress reactivity. Dev Psychobiol 2010, 52:244-253.
90. Pope H.G., Gruber A.J., Hudson J.I., Huestis M.A., Yurgelun-Todd D. Cognitive measures in long-term cannabis users. J Clin Pharmacol 2002, 42:41S-7S.