Partial lesion of the serotonergic system by a single dose of MDMA results in behavioural disinhibition and enhances acute MDMA-induced social behaviour on the social interaction test

Neuropharmacology

Volumn 50, Issue 7, 2006, Pages 884-896

  Ando, Romeo D ^a   Benko, Anita ^a   Ferrington, Linda ^b   Kirilly, Eszter ^a   Kelly, Paul A T ^b   Bagdy, Gyorgy ^a,c  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c SEMMELWEIS UNIVERSITY   (Hungary)

Author keywords

3,4 Methylenedioxymethamphetamine (MDMA, ecstasy); Anxiety; Depression; Impulsivity; Local cerebral glucose utilization; Social behaviour

Indexed keywords

3,4 METHYLENEDIOXYMETHAMPHETAMINE; DEOXYGLUCOSE; GLUCOSE; PAROXETINE; SEROTONIN;

AGGRESSION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; CONTROLLED STUDY; EXPLORATORY BEHAVIOR; GLUCOSE BRAIN LEVEL; LIGAND BINDING; LOCOMOTION; MALE; METABOLIC ACTIVATION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; RAT; SEROTONINERGIC SYSTEM; SOCIAL BEHAVIOR; SOCIAL INTERACTION; TASK PERFORMANCE;

ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; BRAIN; MALE; N-METHYL-3,4-METHYLENEDIOXYAMPHETAMINE; PAROXETINE; RATS; SEROTONIN AGENTS; SOCIAL BEHAVIOR;

EID: 33646725110     PISSN: 00283908     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2005.12.010     Document Type: Article

References (61)

1. Bagdy G., Graf M., Anheuer Z.E., Modos E.A., and Kantor S. Anxiety-like effects induced by acute fluoxetine, sertraline or m-CPP treatment are reversed by pretreatment with the 5-HT2C receptor antagonist SB-242084 but not the 5-HT1A receptor antagonist WAY-100635. Int. J. Neuropsychopharmacol. 4 (2001) 399-408
2. Balogh B., Molnar E., Jakus R., Quate L., Olverman H.J., Kelly P.A., Kantor S., and Bagdy G. Effects of a single dose of 3,4-methylenedioxymethamphetamine on circadian patterns, motor activity and sleep in drug-naive rats and rats previously exposed to MDMA. Psychopharmacology (Berl) 173 (2004) 296-309
3. Beveridge T.J., Mechan A.O., Sprakes M., Pei Q., Zetterstrom T.S., Green A.R., and Elliott J.M. Effect of 5-HT depletion by MDMA on hyperthermia and Arc mRNA induction in rat brain. Psychopharmacology (Berl) 173 (2004) 346-352
4. Bhattacharya S., Bhattacharya A., and Ghosal S. Anxiogenic activity of methylenedioxymethamphetamine (Ecstasy): an experimental study. Biog. Amines 14 (1998) 217-237
5. Briley M., Chopin P., and Moret C. Effect of serotonergic lesion on "anxious" behaviour measured in the elevated plus-maze test in the rat. Psychopharmacology (Berl) 101 (1990) 187-189
6. Buchert R., Obrocki J., Thomasius R., Vaterlein O., Petersen K., Jenicke L., Bohuslavizki K.H., and Clausen M. Long-term effects of 'ecstasy' abuse on the human brain studied by FDG PET. Nucl. Med. Commun. 22 (2001) 889-897
7. Bull E.J., Hutson P.H., and Fone K.C. Reduced social interaction following 3,4-methylenedioxymethamphetamine is not associated with enhanced 5-HT 2C receptor responsivity. Neuropharmacology 44 (2003) 439-448
8. Bull E.J., Hutson P.H., and Fone K.C. Decreased social behaviour following 3,4-methylenedioxymethamphetamine (MDMA) is accompanied by changes in 5-HT2A receptor responsivity. Neuropharmacology 46 (2004) 202-210
9. Butler G.K., and Montgomery A.M. Impulsivity, risk taking and recreational 'ecstasy' (MDMA) use. Drug Alcohol Depend. 76 (2004) 55-62
10. Charney D.S., and Deutch A. A functional neuroanatomy of anxiety and fear: implications for the pathophysiology and treatment of anxiety disorders. Crit. Rev. Neurobiol. 10 (1996) 419-446
11. Colado M.I., Williams J.L., and Green A.R. The hyperthermic and neurotoxic effects of 'Ecstasy' (MDMA) and 3,4 methylenedioxyamphetamine (MDA) in the Dark Agouti (DA) rat, a model of the CYP2D6 poor metabolizer phenotype. Br. J. Pharmacol. 115 (1995) 1281-1289
12. Davison D., and Parrott A.C. Ecstasy (MDMA) in recreational users: self-reported psychological and physiological effects. Hum. Psychopharmacol. 12 (1997) 221-226
13. 3H]-paroxetine-labeled serotonin uptake sites in rat brain. Synapse 1 (1987) 488-496
14. Ferrington, L., McBean, D.E., Olverman, H.J., Leith, J.L., Kelly, P.A.T. Previous exposure to 3,4-methylenedioxymethamphetamine (MDMA) alters cerebral metabolic response to 8-OH-DPAT in Dark Agouti rats. pA2 online, in press.
15. Fone K.C., Beckett S.R., Topham I.A., Swettenham J., Ball M., and Maddocks L. Long-term changes in social interaction and reward following repeated MDMA administration to adolescent rats without accompanying serotonergic neurotoxicity. Psychopharmacology (Berl) 159 (2002) 437-444
16. Green A.R. MDMA: fact and fallacy, and the need to increase knowledge in both the scientific and popular press. Psychopharmacology (Berl) 173 (2004) 231-233
17. Green A.R., Cross A.J., and Goodwin G.M. Review of the pharmacology and clinical pharmacology of 3,4-methylenedioxymethamphetamine (MDMA or "Ecstasy"). Psychopharmacology (Berl) 119 (1995) 247-260
18. Green A.R., and McGregor I.S. On the anxiogenic and anxiolytic nature of long-term cerebral 5-HT depletion following MDMA. Psychopharmacology (Berl) 162 (2002) 448-450
19. Green A.R., Mechan A.O., Elliott J.M., O'Shea E., and Colado M.I. The pharmacology and clinical pharmacology of 3,4-methylenedioxymethamphetamine (MDMA, "ecstasy"). Pharmacol. Rev. 55 (2003) 463-508
20. Griebel G. 5-Hydroxytryptamine-interacting drugs in animal models of anxiety disorders: more than 30 years of research. Pharmacol. Ther. 65 (1995) 319-395
21. Haidkind R., Eller M., Kask A., Harro M., Rinken A., Oreland L., and Harro J. Increased behavioural activity of rats in forced swimming test after partial denervation of serotonergic system by parachloroamphetamine treatment. Neurochem. Int. 45 (2004) 721-732
22. Hall F.S., Devries A.C., Fong G.W., Huang S., and Pert A. Effects of 5,7-dihydroxytryptamine depletion of tissue serotonin levels on extracellular serotonin in the striatum assessed with in vivo microdialysis: relationship to behavior. Synapse 33 (1999) 16-25
23. Harro J. Long-term partial 5-HT depletion: interference of anxiety and impulsivity?. Psychopharmacology (Berl) 164 (2002) 433-434
24. Harro J., Tonissaar M., Eller M., Kask A., and Oreland L. Chronic variable stress and partial 5-HT denervation by parachloroamphetamine treatment in the rat: effects on behavior and monoamine neurochemistry. Brain Res. 899 (2001) 227-239
25. Ho Y.J., Pawlak C.R., Guo L., and Schwarting R.K. Acute and long-term consequences of single MDMA administration in relation to individual anxiety levels in the rat. Behav. Brain Res. 149 (2004) 135-144
26. Iversen S.D. 5-HT and anxiety. Neuropharmacology 23 (1984) 1553-1560
27. Kalivas P.W., Duffy P., and White S.R. MDMA elicits behavioral and neurochemical sensitization in rats. Neuropsychopharmacology 18 (1998) 469-479
28. Kantor S., Anheuer Z.E., and Bagdy G. High social anxiety and low aggression in Fawn-Hooded rats. Physiol. Behav. 71 (2000) 551-557
29. Kelly P.A., Ritchie I.M., and Collins F.M. Cerebrovascular consequences of repeated exposure to NG-nitro-l-arginine methyl ester. Br. J. Pharmacol. 116 (1995) 2771-2777
30. Kirilly E., Benko A., Ferrington L., Ando R.D., Kelly P.A., and Bagdy G. Acute and long-term effects of a single dose of MDMA on aggression in Dark Agouti rats. Int. J. Neuropsychopharmacol. 9 (2006) 63-76
31. Kirilly, E., Tóth, Z.E., Gerber, G., Palkovits, M., Bagdy, G., 2005. 3,4-Methylenedioxymethamphetamine (MDMA) modulates serotonin transporter mRNA expression in the rat brainstem. Society for Neuroscience 35th Annual Meeting, November 12-16 2005, Washington DC, P111.12.
32. Maldonado E., and Navarro J.F. Effects of 3,4-methylenedioxy-methamphetamine (MDMA) on anxiety in mice tested in the light-dark box. Prog. Neuropsychopharmacol. Biol. Psychiatry 24 (2000) 463-472
33. Maldonado E., and Navarro J.F. MDMA ("ecstasy") exhibits an anxiogenic-like activity in social encounters between male mice. Pharmacol. Res. 44 (2001) 27-31
34. McGregor I.S., Clemens K.J., Van der Plasse G., Li K.M., Hunt G.E., Chen F., and Lawrence A.J. Increased anxiety 3 months after brief exposure to MDMA ("Ecstasy") in rats: association with altered 5-HT transporter and receptor density. Neuropsychopharmacology 28 (2003) 1472-1484
35. McGregor I.S., Gurtman C.G., Morley K.C., Clemens K.J., Blokland A., Li K.M., Cornish J.L., and Hunt G.E. Increased anxiety and "depressive" symptoms months after MDMA ("ecstasy") in rats: drug-induced hyperthermia does not predict long-term outcomes. Psychopharmacology (Berl) 168 (2003) 465-474
36. Mechan A.O., Moran P.M., Elliott M., Young A.J., Joseph M.H., and Green R. A comparison between Dark Agouti and Sprague-Dawley rats in their behaviour on the elevated plus-maze, open-field apparatus and activity meters, and their response to diazepam. Psychopharmacology (Berl) 159 (2002) 188-195
37. Mechan A.O., Moran P.M., Elliott M., Young A.J., Joseph M.H., and Green R. A study of the effect of a single neurotoxic dose of 3,4-methylenedioxymethamphetamine (MDMA; "ecstasy") on the subsequent long-term behaviour of rats in the plus maze and open field. Psychopharmacology (Berl) 159 (2002) 167-175
38. Mittman S.M., and Geyer M.A. Dissociation of multiple effects of acute LSD on exploratory behavior in rats by ritanserin and propranolol. Psychopharmacology (Berl) 105 (1991) 69-76
39. Morley K.C., Arnold J.C., and McGregor I.S. Serotonin (1A) receptor involvement in acute 3,4-methylenedioxymethamphetamine (MDMA) facilitation of social interaction in the rat. Prog. Neuropsychopharmacol. Biol. Psychiatry (2005)
40. Morley K.C., Gallate J.E., Hunt G.E., Mallet P.E., and McGregor I.S. Increased anxiety and impaired memory in rats 3 months after administration of 3,4-methylenedioxymethamphetamine ("ecstasy"). Eur. J. Pharmacol. 433 (2001) 91-99
41. Morley K.C., and McGregor I.S. (+/-)-3,4-methylenedioxymethamphetamine (MDMA, 'Ecstasy') increases social interaction in rats. Eur. J. Pharmacol. 408 (2000) 41-49
42. Navarro J.F., and Maldonado E. Behavioral profile of 3,4-methylenedioxy-methamphetamine (MDMA) in agonistic encounters between male mice. Prog. Neuropsychopharmacol. Biol. Psychiatry 23 (1999) 327-334
43. O'Shea E., Granados R., Esteban B., Colado M.I., and Green A.R. The relationship between the degree of neurodegeneration of rat brain 5-HT nerve terminals and the dose and frequency of administration of MDMA ('ecstasy'). Neuropharmacology 37 (1998) 919-926
44. Pallanti S., and Mazzi D. MDMA (Ecstasy) precipitation of panic disorder. Biol. Psychiatry 32 (1992) 91-95
45. Parrott A.C. Human research on MDMA (3,4-methylene- dioxymethamphetamine) neurotoxicity: cognitive and behavioural indices of change. Neuropsychobiology 42 (2000) 17-24
46. Parrott A.C. Human psychopharmacology of ecstasy (MDMA): a review of 15 years of empirical research. Hum. Psychopharmacol. 16 (2001) 557-577
47. Parrott A.C., Sisk E., and Turner J.J. Psychobiological problems in heavy 'ecstasy' (MDMA) polydrug users. Drug Alcohol Depend. 60 (2000) 105-110
48. Piper B.J., and Meyer J.S. Memory deficit and reduced anxiety in young adult rats given repeated intermittent MDMA treatment during the periadolescent period. Pharmacol. Biochem. Behav. (2004)
49. Quate L., McBean D.E., Ritchie I.M., Olverman H.J., and Kelly P.A. Acute methylenedioxymethamphetamine administration: effects on local cerebral blood flow and glucose utilisation in the Dark Agouti rat. Psychopharmacology (Berl) 173 (2004) 287-295
50. Sharkey J., McBean D.E., and Kelly P.A. Alterations in hippocampal function following repeated exposure to the amphetamine derivative methylenedioxymethamphetamine ("Ecstasy"). Psychopharmacology (Berl) 105 (1991) 113-118
51. Singewald N., Salchner P., and Sharp T. Induction of c-Fos expression in specific areas of the fear circuitry in rat forebrain by anxiogenic drugs. Biol. Psychiatry 53 (2003) 275-283
52. Sokoloff L., Reivich M., Kennedy C., Des Rosiers M.H., Patlak C.S., Pettigrew K.D., Sakurada O., and Shinohara M. The [14C]deoxyglucose method for the measurement of local cerebral glucose utilization: theory, procedure, and normal values in the conscious and anesthetized albino rat. J. Neurochem. 28 (1977) 897-916
53. Sprague J.E., Everman S.L., and Nichols D.E. An integrated hypothesis for the serotonergic axonal loss induced by 3,4-methylenedioxymethamphetamine. Neurotoxicology 19 (1998) 427-441
54. Sumnall H.R., O'Shea E., Marsden C.A., and Cole J.C. The effects of MDMA pretreatment on the behavioural effects of other drugs of abuse in the rat elevated plus-maze test. Pharmacol. Biochem. Behav. 77 (2004) 805-814
55. Thompson M.R., Li K.M., Clemens K.J., Gurtman C.G., Hunt G.E., Cornish J.L., and McGregor I.S. Chronic fluoxetine treatment partly attenuates the long-term anxiety and depressive symptoms induced by MDMA ('Ecstasy') in rats. Neuropsychopharmacology 29 (2004) 694-704
56. To C.T., Anheuer Z.E., and Bagdy G. Effects of acute and chronic fluoxetine treatment of CRH-induced anxiety. Neuroreport 10 (1999) 553-555
57. de la Torre R., and Farre M. Neurotoxicity of MDMA (ecstasy): the limitations of scaling from animals to humans. Trends Pharmacol. Sci. 25 (2004) 505-508
58. de la Torre R., Farre M., Mathuna B.O., Roset P.N., Pizarro N., Segura M., Torrens M., Ortuno J., Pujadas M., and Cami J. MDMA (ecstasy) pharmacokinetics in a CYP2D6 poor metaboliser and in nine CYP2D6 extensive metabolisers. Eur. J. Clin. Pharmacol. 61 (2005) 551-554
59. Vollenweider F.X., Gamma A., Liechti M., and Huber T. Psychological and cardiovascular effects and short-term sequelae of MDMA ("ecstasy") in MDMA-naive healthy volunteers. Neuropsychopharmacology 19 (1998) 241-251
60. Vollenweider F.X., Liechti M.E., Gamma A., Greer G., and Geyer M. Acute psychological and neurophysiological effects of MDMA in humans. J. Psychoactive Drugs 34 (2002) 171-184
61. Whitaker-Azmitia P.M., and Aronson T.A. "Ecstasy" (MDMA)-induced panic. Am. J. Psychiatry 146 (1989) 119