Gender-dependent behavioral and biochemical effects of adolescent delta-9-tetrahydrocannabinol in adult maternally deprived rats

Neuroscience

Volumn 204, Issue , 2012, Pages 245-257

  Zamberletti, E ^a   Prini, P ^a   Speziali, S ^a   Gabaglio, M ^a   Solinas, M ^a   Parolaro, D ^a,b   Rubino, T ^a  

^a UNIVERSITY OF INSUBRIA   (Italy)

^b Zardi Gori Foundation   (Italy)

Author keywords

Adolescence; Behavior; Cannabinoid; Dopamine; Glutamate; Maternal deprivation

Indexed keywords

CANNABINOID 1 RECEPTOR; DOPAMINE 1 RECEPTOR; DOPAMINE 2 RECEPTOR; N METHYL DEXTRO ASPARTIC ACID; TETRAHYDROCANNABINOL; TETRAHYDROCANNABINOLIC ACID;

AGGRESSION; ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR CHANGE; BEHAVIORAL STRESS; CONTROLLED STUDY; COPING BEHAVIOR; EARLY LIFE STRESS; FEMALE; FORCED SWIMMING TEST; LONG TERM EXPOSURE; MALE; MATERNAL DEPRIVATION; MEMORY CONSOLIDATION; NEUROMODULATION; NONHUMAN; PATTERN RECOGNITION; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; RAT; RISK FACTOR; SEX DIFFERENCE; SOCIAL INTERACTION;

ANIMALS; BEHAVIOR, ANIMAL; FEMALE; MALE; MATERNAL DEPRIVATION; MEMORY; RATS; RATS, SPRAGUE-DAWLEY; SEX FACTORS; SOCIAL BEHAVIOR; TETRAHYDROCANNABINOL;

EID: 84857128131     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.11.038     Document Type: Article

References (92)

1. Arseneault L., Cannon M., Fisher H.L., Polanczyk G., Moffitt T.E., Caspi A. Childhood trauma and children's emerging psychotic symptoms: a genetically sensitive longitudinal cohort study. Am J Psychiatry 2011, 168:65-72.
2. Arseneault L., Cannon M., Witton J., Murray R.M. Causal association between cannabis and psychosis: examination of the evidence. Br J Psychiatry 2004, 184:110-117.
3. Bambico F.R., Cassano T., Dominguez-Lopez S., Katz N., Walker C.D., Piomelli D., Gobbi G. Genetic deletion of fatty acid amide hydrolase alters emotional behavior and serotonergic transmission in the dorsal raphe, prefrontal cortex, and hippocampus. Neuropsychopharmacology 2010, 35:2083-2100.
4. Bayer T.A., Falkai P., Maier W. Genetic and non-genetic vulnerability factors in schizophrenia: the basis of the "two hit hypothesis". J Psychiatr Res 1999, 33:543-548.
5. Berghuis P., Dobszay M.B., Wang X., Spano S., Ledda F., Sousa K.M., Schulte G., Ernfors P., Mackie K., Paratcha G., Hurd Y.L., Harkany T. Endocannabinoids regulate interneuron migration and morphogenesis by transactivating the TrkB receptor. Proc Natl Acad Sci U S A 2005, 102:19115-19120.
6. Berghuis P., Rajnicek A.M., Morozov Y.M., Ross R.A., Mulder J., Urbán G.M., Monory K., Marsicano G., Matteoli M., Canty A., Irving A.J., Katona I., Yanagawa Y., Rakic P., Lutz B., Mackie K., Harkany T. Hardwiring the brain: endocannabinoids shape neuronal connectivity. Science 2007, 316:1212-1216.
7. Berrendero F., García-Gil L., Hernández M.L., Romero J., Cebeira M., de Miguel R., Ramos J.A., Fernández-Ruiz J.J. Localization of mRNA expression and activation of signal transduction mechanisms for cannabinoid receptor in rat brain during fetal development. Development 1998, 125:3179-3188.
8. Biegon A., Kerman I.A. Autoradiographic study of pre- and postnatal distribution of cannabinoid receptors in human brain. Neuroimage 2001, 14:1463-1468.
9. Biscaia M., Marín S., Fernández B., Marco E.M., Rubio M., Guaza C., Ambrosio E., Viveros M.P. 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.
10. Bloch M., Peleg I., Koren D., Aner H., Klein E. Long-term effects of early parental loss due to divorce on the HPA axis. Horm Behav 2007, 51:516-523.
11. Breslau N., Anthony J.C. Gender differences in the sensitivity to posttraumatic stress disorder: an epidemiological study of urban young adults. J Abnorm Psychol 2007, 116:607-611.
12. Caspi A., Moffitt T.E., Cannon M., McClay J., Murray R., Harrington H., Taylor A., Arseneault L., Williams B., Braithwaite A., Poulton R., Craig I.W. Moderation of the effect of adolescent-onset cannabis use on adult psychosis by a functional polymorphism in the catechol-O-methyltransferase gene: longitudinal evidence of a gene X environment interaction. Biol Psychiatry 2005, 57:1117-1127.
13. Castro J.E., Varea E., Márquez C., Cordero M.I., Poirier G., Sandi C. Role of the amygdala in antidepressant effects on hippocampal cell proliferation and survival and on depression-like behavior in the rat. PLoS One 2010, 5:e8618.
14. Catallani B., Palma B.D., Gil F.Z., Suchecki D. Brief and long maternal separations decrease corticosterone secretion in a lupus-prone strain: dissociation from disease-related parameters. Brain Behav Immun 2008, 22:367-374.
15. Crippa J.A., Zuardi A.W., Martín-Santos R., Bhattacharyya S., Atakan Z., McGuire P., Fusar-Poli P. Cannabis and anxiety: a critical review of the evidence. Hum Psychopharmacol 2009, 24:515-523.
16. de Jong I.E., van den Buuse M. SCH 23390 in the prefrontal cortex enhances the effect of apomorphine on prepulse inhibition of rats. Neuropharmacology 2006, 51:438-446.
17. Degenhardt L., Hall W. Is cannabis use a contributory cause of psychosis?. Can J Psychiatry 2006, 51:556-565.
18. Degenhardt L., Hall W., Lynskey M. 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 2001, 96:1603-1614.
19. Dekker N., Linszen D.H., De Haan L. Reasons for cannabis use and effects of cannabis use as reported by patients with psychotic disorders. Psychopathology 2009, 42:350-360.
20. Ellenbroek B.A., Cools A.R. The long-term effects of maternal deprivation depend on the genetic background. Neuropsychopharmacology 2000, 23:99-106.
21. Ellenbroek B.A., de Bruin N.M., van den Kroonenburg P.T., van Luijtelaar E.L., Cools A.R. The effects of early maternal deprivation on auditory information processing in adult Wistar rats. Biol Psychiatry 2004, 55:701-707.
22. Ellenbroek B.A., van den Kroonenberg P.T., Cools A.R. The effects of an early stressful life event on sensorimotor gating in adult rats. Schizophr Res 1998, 30:251-260.
23. Faturi C.B., Tiba P.A., Kawakami S.E., Catallani B., Kerstens M., Suchecki D. Disruptions of the mother-infant relationship and stress-related behaviours: altered corticosterone secretion does not explain everything. Neurosci Biobehav Rev 2010, 34:821-834.
24. Fergusson D.M., Boden J.M., Horwood L.J. Cannabis use and other illicit drug use: testing the cannabis gateway hypothesis. Addiction 2006, 101:556-569.
25. Fernandez-Espejo E., Viveros M.P., Núñez L., Ellenbroek B.A., Rodriguez de Fonseca F. Role of cannabis and endocannabinoids in the genesis of schizophrenia. Psychopharmacology (Berl) 2009, 206:531-549.
26. Garner B., Wood S.J., Pantelis C., van den Buuse M. Early maternal deprivation reduces prepulse inhibition and impairs spatial learning ability in adulthood: no further effect of post-pubertal chronic corticosterone treatment. Behav Brain Res 2007, 176:323-332.
27. Geyer M.A., Krebs-Thomson K., Braff D.L., Swerdlow N.R. Pharmacological studies of prepulse inhibition models of sensorimotor gating deficits in schizophrenia: a decade in review. Psychopharmacology (Berl) 2001, 156:117-154.
28. Gregg L., Barrowclough C., Haddock G. Reasons for increased substance use in psychosis. Clin Psychol Rev 2007, 27:494-510.
29. Guijarro J.Z., Tiba P.A., Ferreira T.L., Kawakami S.E., Oliveira M.G., Suchecki D. Effects of brief and long maternal separations on the HPA axis activity and the performance of rats on context and tone fear conditioning. Behav Brain Res 2007, 184:101-108.
30. Harkany T., Guzmán M., Galve-Roperh I., Berghuis P., Devi L.A., Mackie K. The emerging functions of endocannabinoid signaling during CNS development. Trends Pharmacol Sci 2007, 28:83-92.
31. Harkany T., Keimpema E., Barabás K., Mulder J. Endocannabinoid functions controlling neuronal specification during brain development. Mol Cell Endocrinol 2008, 286:S84-S90.
32. Harkany T., Mackie K., Doherty P. Wiring and firing neuronal networks: endocannabinoids take center stage. Curr Opin Neurobiol 2008, 18:338-345.
33. Henquet C., Rosa A., Krabbendam L., Papiol S., Fananás L., Drukker M., Ramaekers J.G., van Os J. An experimental study of catechol-o-methyltransferase Val158Met moderation of delta-9-tetrahydrocannabinol-induced effects on psychosis and cognition. Neuropsychopharmacology 2006, 31:2748-2757.
34. Houston J.E., Murphy J., Shevlin M., Adamson G. Cannabis use and psychosis: re-visiting the role of childhood trauma. Psychol Med 2011, 18:1-10.
35. Husum H., Termeer E., Mathé A.A., Bolwig T.G., Ellenbroek B.A. Early maternal deprivation alters hippocampal levels of neuropeptide Y and calcitonin-gene related peptide in adult rats. Neuropharmacology 2002, 42:798-806.
36. Kawakami S.E., Quadros I.M., Takahashi S., Suchecki D. Long maternal separation accelerates behavioural sensitization to ethanol in female, but not in male mice. Behav Brain Res 2007, 184:109-116.
37. Kelley A.E., Schochet T., Landry C.F. Risk taking and novelty seeking in adolescence: introduction to part I. Ann N Y Acad Sci 2004, 1021:27-32.
38. Knight L.D., Collins K.A. A 25-year retrospective review of deaths due to pediatric neglect. Am J Forensic Med Pathol 2005, 26:221-228.
39. Kolliakou A., Joseph C., Ismail K., Atakan Z., Murray R.M. Why do patients with psychosis use cannabis and are they ready to change their use?. Int J Dev Neurosci 2011, 29:335-346.
40. Kuepper R., Henquet C., Lieb R., Wittchen H.U., van Os J. Non-replication of interaction between cannabis use and trauma in predicting psychosis. Schizophr Res 2011, 131(1-3):262-263.
41. Lehmann J., Stöhr T., Feldon J. Long-term effects of prenatal stress experiences and postnatal maternal separation on emotionality and attentional processes. Behav Brain Res 2000, 107:133-144.
42. Léna I., Matthes H., Kieffer B., Kitchen I. Quantitative autoradiography of dopamine receptors in the brains of micro-opioid receptor knockout mice. Neurosci Lett 2004, 356:220-224.
43. Leweke F.M., Schneider M. Chronic pubertal cannabinoid treatment as a behavioural model for aspects of schizophrenia: effects of the atypical antipsychotic quetiapine. Int J Neuropsychopharmacol 2011, 14:43-51.
44. Llorente R., Arranz L., Marco E.M., Moreno E., Puerto M., Guaza C., De la Fuente M., Viveros M.P. Early maternal deprivation and neonatal single administration with a cannabinoid agonist induce long-term sex-dependent psychoimmunoendocrine effects in adolescent rats. Psychoneuroendocrinology 2007, 32:636-650.
45. Llorente R., Gallardo M.L., Berzal A.L., Prada C., Garcia-Segura L.M., Viveros M.P. Early maternal deprivation in rats induces gender-dependent effects on developing hippocampal and cerebellar cells. Int J Dev Neurosci 2009, 27:233-241.
46. Llorente R., Llorente-Berzal A., Petrosino S., Marco E.M., Guaza C., Prada C., López-Gallardo M., Di Marzo V., Viveros M.P. Gender-dependent cellular and biochemical effects of maternal deprivation on the hippocampus of neonatal rats: a possible role for the endocannabinoid system. Dev Neurobiol 2008, 68:1334-1347.
47. Llorente R., O'Shea E., Gutierrez-Lopez M.D., Llorente-Berzal A., Colado M.I., Viveros M.P. Sex-dependent maternal deprivation effects on brain monoamine content in adolescent rats. Neurosci Lett 2010, 479:112-117.
48. Llorente-Berzal A., Fuentes S., Gagliano H., López-Gallardo M., Armario A., Viveros M.P., Nadal R. Sex-dependent effects of maternal deprivation and adolescent cannabinoid treatment on adult rat behaviour. Addict Biol 2011, 16(4):624-637.
49. López-Gallardo M., Llorente R., Llorente-Berzal A., Marco E.M., Prada C., Di Marzo V., Viveros M.P. Neuronal and glial alterations in the cerebellar cortex of maternally deprived rats: gender differences and modulatory effects of two inhibitors of endocannabinoid inactivation. Dev Neurobiol 2008, 68:1429-1440.
50. López-Moreno J.A., González-Cuevas G., Moreno G., Navarro M. The pharmacology of the endocannabinoid system: functional and structural interactions with other neurotransmitter systems and their repercussions in behavioral addiction. Addict Biol 2008, 13:160-187.
51. Marco E.M., Adriani W., Canese R., Podo F., Viveros M.P., Laviola G. Enhancement of endocannabinoid signalling during adolescence: modulation of impulsivity and long-term consequences on metabolic brain parameters in early maternally deprived rats. Pharmacol Biochem Behav 2007, 86:334-345.
52. Mateos B, Borcel E, Loriga R, Luesu W, Bini V, Llorente R, Castelli M, Viveros MP (in press) 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 CB1 cannabinoid receptors. J Psychopharmacol.
53. Mato S., Del Olmo E., Pazos A. Ontogenetic development of cannabinoid receptor expression and signal transduction functionality in the human brain. Eur J Neurosci 2003, 17:1747-1754.
54. Morel L.J., Giros B., Daugé V. Adolescent exposure to chronic delta-9-tetrahydrocannabinol blocks opiate dependence in maternally deprived rats. Neuropsychopharmacology 2009, 34:2469-2476.
55. Mulder J., Aguado T., Keimpema E., Barabás K., Ballester Rosado C.J., Nguyen L., Monory K., Marsicano G., Di Marzo V., Hurd Y.L., Guillemot F., Mackie K., Lutz B., Guzmán M., Lu H.C., Galve-Roperh I., Harkany T. Endocannabinoid signaling controls pyramidal cell specification and long-range axon patterning. Proc Natl Acad Sci U S A 2008, 105. 8760-8755.
56. Newell K.A., Zavitsanou K., Huang X.F. Short and long term changes in NMDA receptor binding in mouse brain following chronic phencyclidine treatment. J Neural Transm 2007, 114:995-1001.
57. O'Shea M., McGregor I.S., Mallet P.E. Repeated cannabinoid exposure during perinatal, adolescent or early adult ages produces similar longlasting deficits in object recognition and reduced social interaction in rats. J Psychopharmacol 2006, 20:611-621.
58. 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.
59. Okubo Y., Suhara T., Suzuki K., Kobayashi K., Inoue O., Terasaki O., Someya Y., Sassa T., Sudo Y., Matsushima E., Iyo M., Tateno Y., Toru M. Decreased prefrontal dopamine D1 receptors in schizophrenia revealed by PET. Nature 1997, 385:634-636.
60. Quinn H.R., Matsumoto I., Callaghan P.D., Long L.E., Arnold J.C., Gunasekaran N., Thompson M.R., Dawson B., Mallet P.E., Kashem M.A., Matsuda-Matsumoto H., Iwazaki T., McGregor I.S. Adolescent rats find repeated Delta(9)-THC less aversive than adult rats but display greater residual cognitive deficits and changes in hippocampal protein expression following exposure. Neuropsychopharmacology 2008, 33:1113-1126.
61. Realini N., Vigano' D., Guidali C., Zamberletti E., Rubino T., Parolaro D. Chronic URB597 treatment at adulthood reverted most depressive-like symptoms induced by adolescent exposure to THC in female rats. Neuropharmacology 2011, 60:235-243.
62. Rebola N., Srikumar B.N., Mulle C. Activity-dependent synaptic plasticity of NMDA receptors. J Physiol 2010, 588:93-99.
63. Roceri M., Hendriks W., Racagni G., Ellenbroek B.A., Riva M.A. Early maternal deprivation reduces the expression of BDNF and NMDA receptor subunits in rat hippocampus. Mol Psychiatry 2002, 7:609-616.
64. Rodrigues A.J., Leão P., Carvalho M., Almeida O.F., Sousa N. Potential programming of dopaminergic circuits by early life stress. Psychopharmacology (Berl) 2011, 214:107-120.
65. Rubino T., Realini N., Braida D., Alberio T., Capurro V., Viganò D., Guidali C., Sala M., Fasano M., Parolaro D. 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. Neurotox Res 2009, 15:291-302.
66. Rubino T., Realini N., Braida D., Guidi S., Capurro V., Viganò D., Guidali C., Pinter M., Sala M., Bartesaghi R., Parolaro D. Changes in hippocampal morphology and neuroplasticity induced by adolescent THC treatment are associated with cognitive impairment in adulthood. Hippocampus 2009, 19:763-772.
67. Rubino T., Viganò D., Massi P., Parolaro D. Changes in the cannabinoid receptor binding, G protein coupling, and cyclic AMP cascade in the CNS of rats tolerant to and dependent on the synthetic cannabinoid compound CP55,940. J Neurochem 2000, 75:2080-2086.
68. Rubino T., Vigano' D., Realini N., Guidali C., Braida D., Capurro V., Castiglioni C., Cherubino F., Romualdi P., Candeletti S., Sala M., Parolaro D. 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.
69. Rubino T, Zamberletti E, Parolaro D (in press) Adolescent exposure to cannabis as a risk factor for psychiatric disorders. J Psychopharmacol.
70. 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.
71. Sherrill J.T., Anderson B., Frank E., Reynolds C.F., Tu X.M., Patterson D., Ritenour A., Kupfer D.J. Is life stress more likely to provoke depressive episodes in women than in men?. Depress Anxiety 1997, 6:95-105.
72. Simeon D., Knutelska M., Yehuda R., Putnam F., Schmeidler J., Smith L.M. Hypothalamic-pituitary-adrenal axis function in dissociative disorders, post-traumatic stress disorder, and healthy volunteers. Biol Psychiatry 2007, 61. 966-673.
73. Solowij N., Pesa N. Cognitive abnormalities and cannabis use. Rev Bras Psiquiatr 2010, 32:S31-S40.
74. Suárez J., Llorente R., Romero-Zerbo S.Y., Mateos B., Bermúdez-Silva F.J., de Fonseca F.R., Viveros M.P. Early maternal deprivation induces gender-dependent changes on the expression of hippocampal CB(1) and CB(2) cannabinoid receptors of neonatal rats. Hippocampus 2009, 19:623-632.
75. Suárez J., Rivera P., Llorente R., Romero-Zerbo S.Y., Bermúdez-Silva F.J., de Fonseca F.R., Viveros M.P. Early maternal deprivation induces changes on the expression of 2-AG biosynthesis and degradation enzymes in neonatal rat hippocampus. Brain Res 2010, 1349:162-173.
76. Swerdlow N.R., Caine S.B., Geyer M.A. Opiate-dopamine interactions in the neural substrates of acoustic startle gating in the rat. Prog Neuropsychopharmacol Biol Psychiatry 1991, 15:415-426.
77. Swerdlow N.R., Vaccarino F.J., Amalric M., Koob G.F. The neural substrates for the motor-activating properties of psychostimulants: a review of recent findings. Pharmacol Biochem Behav 1986, 25:233-248.
78. Szabo B., Schlicker E. Effects of cannabinoids on neurotransmission. Handb Exp Pharmacol 2005, 168:327-365.
79. Taylor E., Rogers J.W. Practitioner review: early adversity and developmental disorders. J Child Psychol Psychiatry 2005, 46:451-467.
80. Thompson K.N., Phillips L.J., Komesaroff P., Yuen H.P., Wood S.J., Pantelis C., Velakoulis D., Yung A.R., McGorry P.D. Stress and HPA-axis functioning in young people at ultra high risk for psychosis. J Psychiatr Res 2007, 41:561-569.
81. Tiba P.A., Oliveira M.G., Rossi V.C., Tufik S., Suchecki D. Glucocorticoids are not responsible for paradoxical sleep deprivation-induced memory impairments. Sleep 2008, 31:505-515.
82. Tiba P.A., Tufik S., Suchecki D. Effects of maternal separation on baseline sleep and cold stress-induced sleep rebound in adult Wistar rats. Sleep 2004, 27:1146-1153.
83. van Laar M., van Dorsselaer S., Monshouwer K., de Graaf R. Does cannabis use predict the first incidence of mood and anxiety disorders in the adult population?. Addiction 2007, 102:1251-1260.
84. van Os J., Krabbendam L., Myin-Germeys I., Delespaul P. The schizophrenia envirome. Curr Opin Psychiatry 2005, 18:141-145.
85. Viveros M.P., Llorente R., López-Gallardo M., Suarez J., Bermúdez-Silva F., De la Fuente M., Rodriguez de Fonseca F., Garcia-Segura L.M. Sex-dependent alterations in response to maternal deprivation in rats. Psychoneuroendocrinology 2009, 34:S217-S226.
86. Viveros MP, Llorente R, Suarez J, Llorente-Berzal A, Lopez-Gallardo M, Rodriguez de Fonseca F (in press), The endocannabinoid system in critical neurodevelopmental periods: sex differences and neuropsychiatric implications. J Psychopharmacol.
87. Wan F.J., Geyer M.A., Swerdlow N.R. Accumbens D2 modulation of sensorimotor gating in rats: assessing anatomical localization. Pharmacol Biochem Behav 1994, 49:155-163.
88. Wan F.J., Swerdlow N.R. Intra-accumbens infusion of quinpirole impairs sensorimotor gating of acoustic startle in rats. Psychopharmacology (Berl) 1993, 113:103-109.
89. Wang X., Dow-Edwards D., Keller E., Hurd Y.L. Preferential limbic expression of the cannabinoid receptor mRNA in the human fetal brain. Neuroscience 2003, 118:681-694.
90. Wegener N., Koch M. Neurobiology and systems physiology of the endocannabinoid system. Pharmacopsychiatry 2009, 42:S79-S86.
91. Weissman M.M., Klerman G.L. Sex differences and the epidemiology of depression. Arch Gen Psychiatry 1977, 34:98-111.
92. Wickramaratne P.J., Weissman M.M., Leaf P.J., Holford T.R. Age, period and cohort effects on the risk of major depression: results from five United States communities. J Clin Epidemiol 1989, 42:333-343.