Hippocampal serotonergic damage induced by MDMA (ecstasy): Effects on spatial learning

Physiology and Behavior

Volumn 79, Issue 2, 2003, Pages 281-287

  Sprague, Jon E ^a   Preston, Amanda S ^a   Leifheit, Michael ^a   Woodside, Brian ^b  

^a OHIO NORTHERN UNIVERSITY   (United States)

^b BOWLING GREEN STATE UNIVERSITY   (United States)

Author keywords

Ecstasy; MDMA; Memory; Morris water maze; Spatial learning

Indexed keywords

3,4 METHYLENEDIOXYMETHAMPHETAMINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; HIPPOCAMPUS; LEARNING; MALE; MAZE TEST; MEMORY; MEMORY DISORDER; NERVE ENDING; NERVE INJURY; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; RAT; SEROTONIN BRAIN LEVEL; SEROTONINERGIC NERVE CELL;

EID: 0038819903     PISSN: 00319384     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0031-9384(03)00092-1     Document Type: Article

References (46)

1. Johnston L.D., O'Malley P.M., Bachman J.G. Monitoring the future national survey results on drug use, 1975-2001. Secondary School Students. vol. I:2002;National Institute on Drug Abuse, Bethesda, MD. (NIH Publication No. 02-5106).
2. Morgan M.J. Memory deficits associated with recreational use of "ecstasy" (MDMA). Psychopharmacology. 141:1999;30-36.
3. Parrott A.C., Lees A., Garnham N.J., Jones M., Wesnes K. Cognitive performance in recreational users of MDMA of 'ecstasy': evidence for memory deficits. J. Psychopharmacol. (Oxf.). 2(1):1998;79-83.
4. Reneman L., Majoie C., Schmand B., Brink W., Heeten G. Prefrontal N-acetylaspartate is strongly associated with memory performance in (abstinent) ecstasy users: preliminary report. Soc. Biol. Psych. 50:2001;550-554.
5. Wareing M., Fisk J.E., Murphy P.N. Working memory deficits in current and previous users of MDMA. Br. J. Psychol. 91:2000;181-188.
6. Heffernan T.M., Jarvis H., Rodgers J., Scholey A.B., Ling J. Prospective memory, everyday cognitive failure and central executive function in recreational users of ecstasy. Hum. Psychopharmacol. Clin. Exp. 16(8):2001;607-612.
7. Rodgers J., Buchanan T., Scholey A.B., Heffernan T.M., Ling J., Parrott A. Differential effects of ecstasy and cannabis on self-reports of memory ability: a web-based study. Hum. Psychopharmacol. Clin. Exp. 16(8):2001;619-625.
8. Bolla K.I., McCann U.D., Ricaurte G.A. Memory impairment in abstinent MDMA ('ecstasy') users. Neurology. 51(6):1998;1532-1537.
9. Reneman L., Booij J., Schmand B., van den Brink W., Gunning B. Memory disturbances in 'ecstasy' users are correlated with an altered brain serotonin neurotransmission. Psychopharmacology (Berl.). 148(3):2000;322-324.
10. Taffe M.A., Weed M.R., Davis S., Huitron-Resendiz S., Schroeder R., Parsons L.H.et al. Functional consequences of repeated (±)3,4-methylenedioxymethamphetamine (MDMA) treatment in rhesus monkeys. Neuropsychopharmacology. 24:2001;230-239.
11. Winsauer P.J., McCann U.D., Yuan J., Delatte M.S., Stevenson M.W., Ricaurte G.A.et al. Effects of fenfluramine, m-CPP and triazolam on repeated-acquisition in squirrel monkeys before and after neurotoxic MDMA administration. Psychopharmacology. 159:2002;388-396.
12. Frederick D.L., Ali S.F., Gillam M.P., Gossett J., Slikker W., Paule M.G. Acute effects of dexfenfluramine (D-FEN) and methylenedioxymethamphetamine (MDMA) before and after short-course, high-dose treatment. Ann. N.Y. Acad. Sci. 844:1998;183-190.
13. Frederick D.L., Ali S.F., Slikker W., Gillam M.P., Allen R.R., Paule M.G. Behavioral and neurochemical effects of chronic methylenedioxymethamphetamine (MDMA) treatment in rhesus monkeys. Neurotoxicol. Teratol. 17:1995;531-543.
14. Byrne T., Baker L.E., Poling A. MDMA and learning: effects of acute and neurotoxic exposure in the rat. Pharmacol. Biochem. Behav. 66(3):2000;501-508.
15. Broening H.W., Morford L.L., Inman-Wood S.L., Fukumura M., Vorhees C.V. 3,4-Methylenedioxymethamphetamine (ecstasy)-induced learning and memory impairments depend on the age of exposure during early development. J. Neurosci. 21:2001;3228-3235.
16. Ricaurte G.A., Markowska A.L., Wenk G.L., Hatzidimitriou G., Wlos J. 3,4-Methylenedioxymethamphetamine, serotonin, and memory. J. Pharmacol. Exp. Ther. 266:1993;1097-1105.
17. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods. 11:1984;47-60.
18. Whishaw I.Q., Mittleman G., Bunch S.T., Dunnett S.B. Impairments in the aquisition, retention and selection of spatial navigation strategies after medial caudate-putamen lesions in rats. Behav. Brain Res. 24:1987;125-138.
19. Brandeis R., Brandys Y., Yehuda S. The use of the Morris water maze in the study of memory and learning. Int. J. Neurosci. 48:1989;26-29.
20. Brandner C., Schenk F. Septal lesions impair the acquisition of a cued place navigation task: attentional or memory deficit? Neurobiol. Learn. Mem. 69:1998;106-125.
21. Waite J.J., Chen A.D., Wardlow M.L., Thal L.J. Behavioral and biochemical consequences of combined lesions of the medial septum/diagonal band and nucleus basalis in the rat when ibotenic acid, quisqualic acid, and AMPA are used. Exp. Neurol. 130:1994;214-229.
22. Petrosini L., Molinari M., Dell'Anna M.E. Cerebellar contribution to spatial event processing: Morris water maze and T-maze. Eur. J. Neurosci. 8:1996;1882-1896.
23. Mogensen J., Pedersen T.K., Holm S., Bang L.E. Prefrontal cortical mediation of rats' place learning in a modified water maze. Brain Res. Bull. 38:1995;425-434.
24. Morris R.G.M., Garrud P., Rawlins J.N.P., O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature. 297:1982;681-683.
25. Sprague J.E., Nichols D.E. The monoamine oxidase-B inhibitor L-deprenyl protects against 3,4-methylenedioxymethamphetamine-induced lipid peroxidation and long term serotonergic deficits. J. Pharmacol. Exp. Ther. 273(3):1995;667-673.
26. Gallagher M., Burwell R., Burchinal M. Severity of spatial learning impairment in aging: development of a learning index for performance in the Morris water maze. Behav. Neurosci. 107:1993;618-626.
27. Chapin D.S., Lookingland K.J., Moore K.E. Effects of LC mobile phase composition on retention times for biogenic amines, and their precursors and metabolites. Curr. Sep. 7:1994;68-70.
28. Bannerman D.M., Good M.A., Butcher S.P., Ramsay M., Morris R.G.M. Distinct components of spatial learning revealed by prior training and NMDA receptor blockade. Nature. 378:1995;182-186.
29. Saucier D., Cain D.P. Spatial learning without NMDA receptor-dependent long-term potentiation. Nature. 378:1995;186-189.
30. Hoh T.E., Cain D.P. Fractionating the nonspatial pretraining effect in the water maze task. Behav. Neurosci. 111:1997;285-1291.
31. Cain D.P., Saucier D., Hall J., Hargreaves E.L., Boon F. Detailed behavioral analysis of water maze acquisition under APV or CNQX: contribution of sensorimotor disturbances to drug-induced acquisition deficits. Behav. Neurosci. 110:1996;86-102.
32. Saucier D., Hargreaves E.L., Boon F., Vanderwolf C.H., Cain D.P. Detailed behavioral analysis of water maze acquisition under systemic NMDA or muscarinic antagonism: nonspatial pretraining eliminates spatial learning deficits. Behav. Neurosci. 110:1996;103-116.
33. Schenk F., Morris R.G.M. Dissociation between components of spatial memory in rats after recovery from the effects of retrohippocampal lesions. Exp. Brain Res. 58:1985;11-28.
34. Whishaw I.Q. Cholinergic receptor blockade in the rat impairs locale but not taxon strategies for place navigation in a swimming pool. Behav. Neurosci. 99:1985;979-1005.
35. Jarrard J.E. What does the hippocampus really do? Behav. Brain Res. 71(1-2):1995;1-10.
36. Sprague J.E., Everman S.L., Nichols D.E. An integrated hypothesis for the serotonergic axonal loss induced by 3,4-methylenedioxymethamphetamine. Neurotoxicology. 19:1998;427-442.
37. Aguirre N., Barrionuevo M., Lasheras B., Del Rio J. The role of dopaminergic systems in the perinatal sensitivity to 3,4-methylenedioxymethamphetamine-induced neurotoxicity in rats. J. Pharmacol. Exp. Ther. 286:1998;1159-1165.
38. Oliveria M.G.M., Bueno O.F.A., Pomarico A.C., Gugliano E.B. Strategies used by hippocampal and caudate putamen lesioned rats in a learning task. Neurobiol. Learn. Mem. 68:1997;32-41.
39. Gurtman C.G., Morley K.C., Kong M.L., Hunt G.E., McGregor I.S. Increased anxiety in rats after 3,4-methylenedioxymethamphetamine: association with serotonin depletion. Eur. J. Pharmacol. 446:2002;89-96.
40. Morley K.C., McGregor I.S. (±)-3,4-Methylenedioxymethamphetamine (MDMA, ecstasy) increases social interactions in rats. Eur. J. Pharmacol. 408:2000;41-49.
41. 1A receptors in the hippocampus. Behav. Brain. Res. 67:1995;67-74.
42. Kulla A., Manahan-Vaughan D. Modulation by serotonin 5-HT(4) receptors of long-term potentiation and depotentiation in the dentate gyrus of freely moving rats. Cereb. Cortex. 12(2):2002;150-162.
43. Shakesby A.C., Anwyl R., Rowan M.J. Overcoming the effects of stress on synaptic plasticity in the intact hippocampus: rapid actions of serotonergic and antidepressant agents. J. Neurosci. 22(9):2002;3638-3644.
44. Lehmann O., Jeltsch H., Lazarus C., Tritschler L., Bertrand F., Cassel J.C. Combined 192 IgG-saporin and 5,7-dihydroxytryptamine lesions in the male rat brain: a neurochemical and behavioral study. Pharmacol. Biochem. Behav. 72:2002;899-912.
45. Acquas E., Marrocu P., Pisanu A., Cadoni C., Zernig G., Saria A.et al. Intravenous (3,4-methylenedioxymethamphetamine) enhances cortical and striatal acetylcholine release in vivo. Eur. J. Pharmacol. 418(3):2001;207-211.
46. Zakzanis K.K., Young D.A. Memory impairment in abstinent MDMA ("ecstasy") users: a longitudinal investigation. Neurology. 56:2001;966-969.