Behavioral and neurochemical effects of repeated MDMA administration during late adolescence in the rat

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 48, Issue , 2014, Pages 229-235

  Cox, Brittney M ^a,d   Shah, Mrudang M ^b,c   Cichon, Teri ^a   Tancer, Manuel E ^a   Galloway, Matthew P ^a   Thomas, David M ^b,c,e   Perrine, Shane A ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WAYNE STATE UNIVERSITY   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^e OAKLAND UNIVERSITY WILLIAM BEAUMONT SCHOOL OF MEDICINE   (United States)

Author keywords

Amygdala; Anxiety; Conditioned place preference; Dorsal raphe; MDMA; Serotonin

Indexed keywords

3,4 METHYLENEDIOXYMETHAMPHETAMINE; 5 HYDROXYINDOLEACETIC ACID; SEROTONIN;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BRAIN DYSFUNCTION; BRAIN TISSUE; CONTROLLED STUDY; DORSAL RAPHE NUCLEUS; DRUG EFFECT; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HIPPOCAMPUS; JUVENILE ANIMAL; LOCOMOTION; MALE; NONHUMAN; OPEN FIELD TEST; PLACE PREFERENCE; RAT; SEROTONIN SYNDROME; SOCIAL AVOIDANCE BEHAVIOR;

3,4-METHYLENEDIOXYMETHAMPHETAMINE; 5-HIAA; 5-HT SEROTONIN; 5-HYDROXYINDOLEACETIC ACID; 5-HYDROXYTRYPTAMINE; AMYGDALA; ANALYSIS OF VARIANCE; ANOVA; ANXIETY; CONDITIONED PLACE PREFERENCE; DORSAL RAPHE; HIGH PRESSURE LIQUID CHROMATOGRAPHY; HPLC; INTRAPERITONEAL; IP; MDMA; PND; POSTNATAL DATE; SEM; SEROTONIN; SEROTONIN TRANSPORTER; SERT; STANDARD ERROR OF THE MEAN;

ADAPTATION, OCULAR; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; BRAIN; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CONDITIONING, OPERANT; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG ADMINISTRATION SCHEDULE; EXPLORATORY BEHAVIOR; HALLUCINOGENS; HYDROXYINDOLEACETIC ACID; MALE; N-METHYL-3,4-METHYLENEDIOXYAMPHETAMINE; RATS; RATS, SPRAGUE-DAWLEY; SEROTONIN; TIME FACTORS;

EID: 84887328302     PISSN: 02785846     EISSN: 18784216     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2013.09.021     Document Type: Article

References (60)

1. Adriani W., Macri S., Pacifici R., Laviola G. Peculiar vulnerability to nicotine oral self-administration in mice during early adolescence. Neuropsychopharmacology 2002, 27:212-224.
2. Azmitia E.C., Segal M. An autoradiographic analysis of the differential ascending projections of the dorsal and median raphe nuclei in the rat. J Comp Neurol 1978, 179:641-667.
3. Badanich K.A., Adler K.J., Kirstein C.L. Adolescents differ from adults in cocaine conditioned place preference and cocaine-induced dopamine in the nucleus accumbens septi. Eur J Pharmacol 2006, 550:95-106.
4. Bardo M.T., Bevins R.A. Conditioned place preference: what does it add to our preclinical understanding of drug reward?. Psychopharmacology (Berl) 2000, 153:31-43.
5. Battaglia G., Sharkey J., Kuhar M.J., de Souza E.B. Neuroanatomic specificity and time course of alterations in rat brain serotonergic pathways induced by MDMA (3,4-methylenedioxymethamphetamine): assessment using quantitative autoradiography. Synapse 1991, 8:249-260.
6. Baumann M.H., Rothman R.B. Neural and cardiac toxicities associated with 3,4-methylenedioxymethamphetamine (MDMA). Int Rev Neurobiol 2009, 88:257-296.
7. Biezonski D.K., Meyer J.S. The nature of 3,4-methylenedioxymethamphetamine (MDMA)-induced serotonergic dysfunction: evidence for and against the neurodegeneration hypothesis. Curr Neuropharmacol 2011, 9:84-90.
8. Bradberry C.W., Sprouse J.S., Aghajanian G.K., Roth R.H. 3,4-Methylenedioxymethamphetamine (MDMA)-induced release of endogenous serotonin from the rat dorsal raphe nucleus in vitro: effects of fluoxetine and tryptophan. Neurochem Int 1990, 17:509-513.
9. Broening H.W., Bacon L., Slikker W. Age modulates the long-term but not the acute effects of the serotonergic neurotoxicant 3,4-methylenedioxymethamphetamine. J Pharmacol Exp Ther 1994, 271:285-293.
10. Catlow B.J., Badanich K.A., Sponaugle A.E., Rowe A.R., Song S., Rafalovich I., et al. Effects of MDMA ("ecstasy") during adolescence on place conditioning and hippocampal neurogenesis. Eur J Pharmacol 2010, 628:96-103.
11. Cerrito F., Raiteri M. Serotonin release is modulated by presynaptic autoreceptors. Eur J Pharmacol 1979, 57:427-430.
12. Clemens K.J., Cornish J.L., Hunt G.E., McGregor I.S. Repeated weekly exposure to MDMA, methamphetamine or their combination: long-term behavioural and neurochemical effects in rats. Drug Alcohol Depend 2007, 86:183-190.
13. Daza-Losada M., Ribeiro Do Couto B., Manzanedo C., Aguilar M.A., Rodriguez-Arias M., Minarro J. Rewarding effects and reinstatement of MDMA-induced CPP in adolescent mice. Neuropsychopharmacology 2007, 32:1750-1759.
14. Faria R., Magalhaes A., Monteiro P.R., Gomes-Da-Silva J., Amélia Tavares M., Summavielle T. MDMA in adolescent male rats: decreased serotonin in the amygdala and behavioral effects in the elevated plus-maze test. Ann N Y Acad Sci 2006, 1074:643-649.
15. Fone K.C., Beckett S.R., Topham I.A., Swettenham J., Ball M., Maddocks L. Long-term changes in social interaction and reward following repeated MDMA administration to adolescent rats without accompanying serotonergic neurotoxicity. Psychopharmacology (Berl) 2002, 159:437-444.
16. Gordon J.A., Hen R. The serotonergic system and anxiety. Neuromolecular Med 2004, 5:27-40.
17. Gurtman C.G., Morley K.C., Li K.M., Hunt G.E., McGregor I.S. Increased anxiety in rats after 3,4-methylenedioxymethamphetamine: association with serotonin depletion. Eur J Pharmacol 2002, 446:89-96.
18. Harris G.C., Aston-Jones G. Altered motivation and learning following opiate withdrawal: evidence for prolonged dysregulation of reward processing. Neuropsychopharmacology 2003, 28:865-871.
19. Hascoet M., Bourin M. A new approach to the light/dark test procedure in mice. Pharmacol Biochem Behav 1998, 60:645-653.
20. Heisler L.K., Zhou L., Bajwa P., Hsu J., Tecott L.H. Serotonin 5-HT(2C) receptors regulate anxiety-like behavior. Genes Brain Behav 2007, 6:491-496.
21. Higgins G.A., Jones B.J., Oakley N.R., Tyers M.B. Evidence that the amygdala is involved in the disinhibitory effects of 5-HT3 receptor antagonists. Psychopharmacology (Berl) 1991, 104:545-551.
22. Hodges H., Green S., Glenn B. Evidence that the amygdala is involved in benzodiazepine and serotonergic effects on punished responding but not on discrimination. Psychopharmacology (Berl) 1987, 92:491-504.
23. Izenwasser S. Differential effects of psychoactive drugs in adolescents and adults. Crit Rev Neurobiol 2005, 17:51-67.
24. Jacobs B.L., Azmitia E.C. Structure and function of the brain serotonin system. Physiol Rev 1992, 72:165-229.
25. Johnston L.D., O'Malley P.M., Bachman J.G., Schulenberg J.E. Marijuana use is rising; ecstasy use is beginning to rise; and alcohol use is declining among U.S. teens 2010, University of Michigan News Service, Ann Arbor, MI.
26. Kelly P.A., Ritchie I.M., Quate L., McBean D.E., Olverman H.J. Functional consequences of perinatal exposure to 3,4-methylenedioxymethamphetamine in rat brain. Br J Pharmacol 2002, 137:963-970.
27. Kindlundh-Hogberg A.M., Schioth H.B., Svenningsson P. Repeated intermittent MDMA binges reduce DAT density in mice and SERT density in rats in reward regions of the adolescent brain. Neurotoxicology 2007, 28:1158-1169.
28. Koch S., Galloway M.P. MDMA induced dopamine release in vivo: role of endogenous serotonin. J Neural Transm 1997, 104:135-146.
29. Kolyaduke O.V., Hughes R.N. Increased anxiety-related behavior in male and female adult rats following early and late adolescent exposure to 3,4-methylenedioxymethamphetamine (MDMA). Pharmacol Biochem Behav 2013, 103:742-749.
30. LaPlant Q., Vialou V., Covington H.E., Dumitriu D., Feng J., Warren B.L., et al. Dnmt3a regulates emotional behavior and spine plasticity in the nucleus accumbens. Nat Neurosci 2010, 13:1137-1143.
31. Liechti M.E., Baumann C., Gamma A., Vollenweider F.X. Acute psychological effects of 3,4-methylenedioxymethamphetamine (MDMA, "Ecstasy") are attenuated by the serotonin uptake inhibitor citalopram. Neuropsychopharmacology 2000, 22:513-521.
32. Lin H.Q., Burden P.M., Christie M.J., Johnston G.A. The anxiogenic-like and anxiolytic-like effects of MDMA on mice in the elevated plus-maze: a comparison with amphetamine. Pharmacol Biochem Behav 1999, 62:403-408.
33. Llorente-Berzal A., Manzanedo C., Daza-Losada M., Valero M., Lopez-Gallardo M., Aguilar M.A., et al. Sex-dependent effects of early maternal deprivation on MDMA-induced conditioned place preference in adolescent rats: possible neurochemical correlates. Toxicology 2013, 311:78-86.
34. MacInnes N., Handley S.L., Harding G.F. Former chronic methylenedioxymethamphetamine (MDMA or ecstasy) users report mild depressive symptoms. J Psychopharmacol 2001, 15:181-186.
35. Marona-Lewicka D., Rhee G.S., Sprague J.E., Nichols D.E. Reinforcing effects of certain serotonin-releasing amphetamine derivatives. Pharmacol Biochem Behav 1996, 53:99-105.
36. Martin J.R., Ballard T.M., Higgins G.A. Influence of the 5-HT2C receptor antagonist, SB-242084, in tests of anxiety. Pharmacol Biochem Behav 2002, 71:615-625.
37. McGregor I.S., Clemens K.J., Van der Plasse G., Li K.M., Hunt G.E., Chen F., et al. Increased anxiety 3 months after brief exposure to MDMA ("Ecstasy") in rats: association with altered 5-HT transporter and receptor density. Neuropsychopharmacology 2003, 28:1472-1484.
38. McNamara M.G., Kelly J.P., Leonard B.E. Some behavioural and neurochemical aspects of subacute (+/-)3,4-methylenedioxymethamphetamine administration in rats. Pharmacol Biochem Behav 1995, 52:479-484.
39. Meyer A., Mayerhofer A., Kovar K.A., Schmidt W.J. Rewarding effects of the optical isomers of 3,4-methylenedioxy-methylamphetamine ('Ecstasy') and 3,4-methylenedioxy-ethylamphetamine ('Eve') measured by conditioned place preference in rats. Neurosci Lett 2002, 330:280-284.
40. Meyer J.S., Grande M., Johnson K., Ali S.F. Neurotoxic effects of MDMA ("ecstasy") administration to neonatal rats. Int J Dev Neurosci 2004, 22:261-271.
41. Morley K.C., Gallate J.E., Hunt G.E., Mallet P.E., McGregor I.S. Increased anxiety and impaired memory in rats 3 months after administration of 3,4-methylenedioxymethamphetamine ("ecstasy"). Eur J Pharmacol 2001, 433:91-99.
42. Morley-Fletcher S., Bianchi M., Gerra G., Laviola G. Acute and carryover effects in mice of MDMA ("ecstasy") administration during periadolescence. Eur J Pharmacol 2002, 448:31-38.
43. Navarro J.F., Rivera A., Maldonado E., Cavas M., de la Calle A. Anxiogenic-like activity of 3,4-methylenedioxy-methamphetamine ("Ecstasy") in the social interaction test is accompanied by an increase of c-fos expression in mice amygdala. Prog Neuropsychopharmacol Biol Psychiatry 2004, 28:249-254.
44. Niculescu M., Perrine S.A., Miller J.S., Ehrlich M.E., Unterwald E.M. Trk: a neuromodulator of age-specific behavioral and neurochemical responses to cocaine in mice. J Neurosci 2008, 28:1198-1207.
45. Parrott A.C., Sisk E., Turner J.J. Psychobiological problems in heavy 'ecstasy' (MDMA) polydrug users. Drug Alcohol Depend 2000, 60:105-110.
46. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 2007, Elsevier, Amsterdam; Boston. 6th ed.
47. Perrine S.A., Ghoddoussi F., Michaels M.S., Hyde E.M., Kuhn D.M., Galloway M.P. MDMA administration decreases serotonin but not N-acetylaspartate in the rat brain. Neurotoxicology 2010, 31:654-661.
48. Pineyro G., Blier P. Autoregulation of serotonin neurons: role in antidepressant drug action. Pharmacol Rev 1999, 51:533-591.
49. Piper B.J. A developmental comparison of the neurobehavioral effects of ecstasy (MDMA). Neurotoxicol Teratol 2007, 29:288-300.
50. Piper B.J., Ali S.F., Daniels L.G., Meyer J.S. Repeated intermittent methylenedioxymethamphetamine exposure protects against the behavioral and neurotoxic, but not hyperthermic, effects of an MDMA binge in adult rats. Synapse 2010, 64:421-431.
51. Pompeiano M., Palacios J.M., Mengod G. Distribution and cellular localization of mRNA coding for 5-HT1A receptor in the rat brain: correlation with receptor binding. J Neurosci 1992, 12:440-453.
52. Prut L., Belzung C. The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur J Pharmacol 2003, 463:3-33.
53. Ribeiro Do Couto B., Rodriguez-Arias M., Fuentes S., Gagliano H., Armario A., Minarro J., et al. Adolescent pre-exposure to ethanol or MDMA prolongs the conditioned rewarding effects of MDMA. Physiol Behav 2011, 103:585-593.
54. Ribeiro Do Couto B., Daza-Losada M., Rodriguez-Arias M., Nadal R., Guerri C., Summavielle T., et al. Adolescent pre-exposure to ethanol and 3,4-methylenedioxymethylamphetamine (MDMA) increases conditioned rewarding effects of MDMA and drug-induced reinstatement. Addict Biol 2012, 17:588-600.
55. Robledo P., Trigo J.M., Panayi F., de la Torre R., Maldonado R. Behavioural and neurochemical effects of combined MDMA and THC administration in mice. Psychopharmacology (Berl) 2007, 195:255-264.
56. Salzmann J., Marie-Claire C., Le Guen S., Roques B.P., Noble F. Importance of ERK activation in behavioral and biochemical effects induced by MDMA in mice. Br J Pharmacol 2003, 140:831-838.
57. SAMHSA Results from the 2001 national household survey on drug abuse: volume I. Summary of national findings. Series H-17 2002, Office of Applied Studies, Rockville, MD. NHSDA (Ed.).
58. Tancer M., Johanson C.E. Reinforcing, subjective, and physiological effects of MDMA in humans: a comparison with d-amphetamine and mCPP. Drug Alcohol Depend 2003, 72:33-44.
59. Verkes R.J., Gijsman H.J., Pieters M.S., Schoemaker R.C., de Visser S., Kuijpers M., et al. Cognitive performance and serotonergic function in users of ecstasy. Psychopharmacology (Berl) 2001, 153:196-202.
60. Weisstaub N.V., Zhou M., Lira A., Lambe E., Gonzalez-Maeso J., Hornung J.P., et al. Cortical 5-HT2A receptor signaling modulates anxiety-like behaviors in mice. Science 2006, 313:536-540.