Prague Med. Rep. 2014, 115, 43-59

Effect of Amphetamine on Adult Male and Female Rats Prenatally Exposed to Methamphetamine

Romana Šlamberová*, Eva Macúchová, Kateryna Nohejlová, Andrea Štofková, Jana Jurčovičová

Department of Normal, Pathological and Clinical Physiology, Third Faculty of Medicine, Charles University in Prague, Prague, Czech Republic


1. Acuff-Smith, K. D., Schilling, M. A., Fisher, J. E., Vorhees, C. V. (1996) Stage-specific effects of prenatal d-methamphetamine exposure on behavioral and eye development in rats. Neurotoxicol. Teratol. 18, 199–215. <>
2. Ago, Y., Arikawa, S., Yata, M., Yano, K., Abe, M., Takuma, K., Matsuda, T. (2008) Antidepressant-like effects of the glucocorticoid receptor antagonist RU-43044 are associated with changes in prefrontal dopamine in mouse models of depression. Neuropharmacology 55, 1355–1363. <>
3. Akirav, I., Sandi, C., Richter-Levin, G. (2001) Differential activation of hippocampus and amygdala following spatial learning under stress. Eur. J. Neurosci. 14, 719–725. <>
4. Armstrong, J. N., McIntyre, D. C., Neubort, S., Sloviter, R. S. (1993) Learning and memory after adrenalectomy-induced hippocampal dentate granule cell degeneration in the rat. Hippocampus 3, 359–371. <>
5. Bartoletti, M., Gaiardi, M., Gubellini, C., Bacchi, A., Babbini, M. (1985) Cross-sensitization to the excitatory effect of morphine in post-dependent rats. Neuropharmacology 24, 889–893. <>
6. Bernášková, K., Matějovská, I., Šlamberová, R. (2011) Postnatal challenge dose of methamphetamine amplifies anticonvulsant effects of prenatal methamphetamine exposure on epileptiform activity induced by electrical stimulation in adult male rats. Exp. Neurol. 229, 282–287. <>
7. Bisagno, V., Ferguson, D., Luine, V. N. (2003) Chronic D-amphetamine induces sexually dimorphic effects on locomotion, recognition memory, and brain monoamines. Pharmacol. Biochem. Behav. 74, 859–867. <>
8. Bubeníková-Valešová, V., Kačer, P., Syslová, K., Rambousek, L., Janovský, M., Schutová, B., Hrubá, L., Šlamberová, R. (2009) Prenatal methamphetamine exposure affects the mesolimbic dopaminergic system and behavior in adult offspring. Int. J. Dev. Neurosci. 27, 525–530. <>
9. Camp, D. M., Robinson, T. E. (1988) Susceptibility to sensitization. II. The influence of gonadal hormones on enduring changes in brain monoamines and behavior produced by the repeated administration of D-amphetamine or restraint stress. Behav. Brain Res. 30, 69–88. <>
10. Cao, G., Zhu, J., Zhong, Q., Shi, C., Dang, Y., Han, W., Liu, X., Xu, M., Chen, T. (2013) Distinct roles of methamphetamine in modulating spatial memory consolidation, retrieval, reconsolidation and the accompanying changes of ERK and CREB activation in hippocampus and prefrontal cortex. Neuropharmacology 67, 144–154. <> <PubMed>
11. Carey, R., Gui, J. (1997) A simple and reliable method for the positive identification of Pavlovian conditioned cocaine effects in open-field behavior. J. Neurosci. Methods 73, 1–8. <>
12. Carey, R. J., Damianopoulos, E. N. (2006) Cocaine conditioning and sensitization: the habituation factor. Pharmacol. Biochem. Behav. 84, 128–133. <>
13. Cho, D. H., Lyu, H. M., Lee, H. B., Kim, P. Y., Chin, K. (1991) Behavioral teratogenicity of methamphetamine. J. Toxicol. Sci. 16, 37–49 (Suppl. 1). <>
14. Chu, Y., Mouat, M. F., Harris, R. B., Coffield, J. A., Grider, A. (2003) Water maze performance and changes in serum corticosterone levels in zinc-deprived and pair-fed rats. Physiol. Behav. 78, 569–578. <>
15. Deroche, V., Piazza, P. V., Casolini, P., Maccari, S., Le Moal, M., Simon, H. (1992) Stress-induced sensitization to amphetamine and morphine psychomotor effects depend on stress-induced corticosterone secretion. Brain Res. 598, 343–348. <>
16. Estelles, J., Rodriguez-Arias, M., Maldonado, C., Aguilar, M. A., Minarro, J. (2006) Gestational exposure to cocaine alters cocaine reward. Behav. Pharmacol. 17, 509–515. <>
17. Fattore, L., Deiana, S., Spano, S. M., Cossu, G., Fadda, P., Scherma, M., Fratta, W. (2005) Endocannabinoid system and opioid addiction: behavioural aspects. Pharmacol. Biochem. Behav. 81, 343–359. <>
18. Fleckenstein, A. E., Gibb, J. W., Hanson, G. R. (2000) Differential effects of stimulants on monoaminergic transporters: pharmacological consequences and implications for neurotoxicity. Eur. J. Pharmacol. 406, 1–13. <>
19. Forgie, M. L., Stewart, J. (1993) Sex differences in amphetamine-induced locomotor activity in adult rats: role of testosterone exposure in the neonatal period. Pharmacol. Biochem. Behav. 46, 637–645. <>
20. Gagin, R., Kook, N., Cohen, E., Shavit, Y. (1997) Prenatal morphine enhances morphine-conditioned place preference in adult rats. Pharmacol. Biochem. Behav. 58, 525–528. <>
21. Gralewicz, S., Lutz, P., Swiercz, R., Grzelinska, Z., Wiaderna, D. (2011) Neuroendocrine and behavioral response to amphetamine challenge after exposure to an organophosphorus pesticide. Int. J. Occup. Med. Environ. Health 24, 283–291. <>
22. Handa, R. J., Burgess, L. H., Kerr, J. E., O’Keefe, J. A. (1994) Gonadal steroid hormone receptors and sex differences in the hypothalamo-pituitary-adrenal axis. Horm. Behav. 28, 464–476. <>
23. He, S., Grasing, K. (2004) Chronic opiate treatment enhances both cocaine-reinforced and cocaine-seeking behaviors following opiate withdrawal. Drug Alcohol Depend. 75, 215–221. <>
24. Heyser, C. J., Goodwin, G. A., Moody, C. A., Spear, L. P. (1992) Prenatal cocaine exposure attenuates cocaine-induced odor preference in infant rats. Pharmacol. Biochem. Behav. 42, 169–173. <>
25. Hrubá, L., Schutová, B., Šlamberová, R. (2012) Sex differences in anxiety-like behavior and locomotor activity following prenatal and postnatal methamphetamine exposure in adult rats. Physiol. Behav. 105, 364–370. <>
26. Jarvik, L. F. (1975) Human intelligence: sex differences. Acta Genet. Med. Gemellol. (Roma) 24, 189–211. <>
27. Johnson, B. N., Yamamoto, B. K. (2010) Chronic stress enhances the corticosterone response and neurotoxicity to +3,4-methylenedioxymethamphetamine (MDMA): the role of ambient temperature. J. Pharmacol. Exp. Ther. 335, 180–189. <> <PubMed>
28. Kitaichi, K., Morishita, Y., Doi, Y., Ueyama, J., Matsushima, M., Zhao, Y. L., Takagi, K., Hasegawa, T. (2003) Increased plasma concentration and brain penetration of methamphetamine in behaviorally sensitized rats. Eur. J. Pharmacol. 464, 39–48. <>
29. Lee, B., Sur, B., Shim, I., Lee, H., Hahm, D. H. (2014) Baicalin improves chronic corticosterone-induced learning and memory deficits via the enhancement of impaired hippocampal brain-derived neurotrophic factor and cAMP response element-binding protein expression in the rat. J. Nat. Med. 68, 132–143. <>
30. Macúchová, E., Nohejlová-Deykun, K., Šlamberová, R. (2013) Effect of methamphetamine on cognitive functions of adult female rats prenatally exposed to the same drug. Physiol. Res. 62, S89–S98.
31. Malanga, C. J., Kosofsky, B. E. (2003) Does drug abuse beget drug abuse? Behavioral analysis of addiction liability in animal models of prenatal drug exposure. Brain Res. Dev. Brain Res. 147, 47–57. <>
32. Martin, J. C., Martin, D. C., Radow, B., Sigman, G. (1976) Growth, development and activity in rat offspring following maternal drug exposure. Exp. Aging Res. 2, 235–251. <>
33. Marwick, C. (2000) NIDA seeking data on effect of fetal exposure to methamphetamine. JAMA 283, 2225–2226. <>
34. Matějovská, I., Bernášková, K., Šlamberová, R. (2014) Effect of prenatal methamphetamine exposure and challenge dose of the same drug in adulthood on epileptiform activity induced by electrical stimulation in female rats. Neuroscience 257, 130–138. <>
35. Milesi-Halle, A., McMillan, D. E., Laurenzana, E. M., Byrnes-Blake, K. A., Owens, S. M. (2007) Sex differences in (+)-amphetamine- and (+)-methamphetamine-induced behavioral response in male and female Sprague-Dawley rats. Pharmacol. Biochem. Behav. 86, 140–149. <> <PubMed>
36. Morris, R. (1984) Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods 11, 47–60. <>
37. Páleníček, T., Votava, M., Bubeníková, V., Horáček, J. (2005) Increased sensitivity to the acute effects of MDMA (“ecstasy”) in female rats. Physiol. Behav. 86, 546–553. <>
38. Polanecký, V., Šejda, J., Studničková, B. (1996) Prevalence study of serious substance abusers in the Czech Republic. Cent. Eur. J. Public Health 4, 176–184.
39. Rocha, B. A., Mead, A. N., Kosofsky, B. E. (2002) Increased vulnerability to self-administer cocaine in mice prenatally exposed to cocaine. Psychopharmacology (Berl.) 163, 221–229. <>
40. Roozendaal, B., Bohus, B., McGaugh, J. L. (1996) Dose-dependent suppression of adrenocortical activity with metyrapone: effects on emotion and memory. Psychoneuroendocrinology 21, 681–693. <>
41. Rothman, R. B., Baumann, M. H., Dersch, C. M., Romero, D. V., Rice, K. C., Carroll, F. I., Partilla, J. S. (2001) Amphetamine-type central nervous system stimulants release norepinephrine more potently than they release dopamine and serotonin. Synapse 39, 32–41. <<32::AID-SYN5>3.0.CO;2-3>
42. Schutová, B., Hrubá, L., Pometlová, M., Deykun, K., Šlamberová, R. (2008) Impact of methamphetamine administered prenatally and in adulthood on cognitive functions of male rats tested in Morris water maze. Prague Med. Rep. 109, 62–70.
43. Schutová, B., Hrubá, L., Pometlová, M., Deykun, K., Šlamberová, R. (2009a) Cognitive functions and drug sensitivity in adult male rats prenatally exposed to methamphetamine. Physiol. Res. 58, 741–750.
44. Schutová, B., Hrubá, L., Pometlová, M., Šlamberová, R. (2009b) Impact of prenatal and acute methamphetamine exposure on behaviour of adult male rats. Prague Med. Rep. 110, 67–78.
45. Schutová, B., Hrubá, L., Pometlová, M., Rokyta, R., Šlamberová, R. (2010) Responsiveness to methamphetamine in adulthood is altered by prenatal exposure in rats. Physiol. Behav. 99, 381–387. <>
46. Schutová, B., Hrubá, L., Rokyta, R., Šlamberová, R. (2013) Gender differences in behavioral changes elicited by prenatal methamphetamine exposure and application of the same drug in adulthood. Dev. Psychobiol. 55, 232–242. <>
47. Šejda, J., Studničková, B., Polanecký, V. (1998) Trends in the incidence of problematic drug addicts in the Czech Republic, 1995–1996. Cent. Eur. J. Public Health 6, 18–24.
48. Sherwin, B. B. (1997) Estrogen effects on cognition in menopausal women. Neurology 48, S21–S26. <>
49. Shoblock, J. R., Maisonneuve, I. M., Glick, S. D. (2003a) Differences between d-methamphetamine and d-amphetamine in rats: working memory, tolerance, and extinction. Psychopharmacology (Berl.) 170, 150–156. <>
50. Shoblock, J. R., Sullivan, E. B., Maisonneuve, I. M., Glick, S. D. (2003b) Neurochemical and behavioral differences between d-methamphetamine and d-amphetamine in rats. Psychopharmacology (Berl.) 165, 359–369. <>
51. Šlamberová, R., Charousová, P., Pometlová, M. (2005) Methamphetamine administration during gestation impairs maternal behavior. Dev. Psychobiol. 46, 57–65. <>
52. Šlamberová, R., Pometlová, M., Charousová, P. (2006) Postnatal development of rat pups is altered by prenatal methamphetamine exposure. Prog. Neuropsychopharmacol. Biol. Psychiatry 30, 82–88. <>
53. Šlamberová, R., Schutová, B., Matějovská, I., Bernášková, K., Rokyta, R. (2009) Effects of a single postnatal methamphetamine administration on NMDA-induced seizures are sex- and prenatal exposure-specific. Naunyn Schmiedebergs Arch. Pharmacol. 380, 109–114. <>
54. Šlamberová, R., Yamamotová, A., Schutová, B., Hrubá, L., Pometlová, M. (2011) Impact of prenatal methamphetamine exposure on the sensitivity to the same drug in adult male rats. Prague Med. Rep. 112, 102–114.
55. Šlamberová, R., Pometlová, M., Schutová, B., Hrubá, L., Macúchová, E., Nová, E., Rokyta, R. (2012a) Do prenatally methamphetamine-exposed adult male rats display general predisposition to drug abuse in the conditioned place preference test? Physiol. Res. 61, S129–S138 (Suppl. 2).
56. Šlamberová, R., Yamamotová, A., Pometlová, M., Schutová, B., Hrubá, L., Nohejlová-Deykun, K., Nová, E., Macúchová, E. (2012b) Does prenatal methamphetamine exposure induce cross-sensitization to cocaine and morphine in adult male rats? Prague Med. Rep. 113, 189–205. <>
57. Turner, C. D., Bagnara, J. T. (1976) Endocrinology of the ovary. In: General Endocrinology, eds. Turner, C. D., Bagnara, J. T., pp. 450–495, W. B. Saunders Company, Philadelphia.
58. Tzschentke, T. M. (1998) Measuring reward with the conditioned place preference paradigm: a comprehensive review of drug effects, recent progress and new issues. Prog. Neurobiol. 56, 613–672. <>
59. Tzschentke, T. M., Schmidt, W. J. (1998) The development of cocaine-induced behavioral sensitization is affected by discrete quinolinic acid lesions of the prelimbic medial prefrontal cortex. Brain Res. 795, 71–76. <>
60. Valvassori, S. S., Frey, B. N., Martins, M. R., Reus, G. Z., Schimidtz, F., Inacio, C. G., Kapczinski, F., Quevedo, J. (2007) Sensitization and cross-sensitization after chronic treatment with methylphenidate in adolescent Wistar rats. Behav. Pharmacol. 18, 205–212. <>
61. Vela, G., Martin, S., Garcia-Gil, L., Crespo, J. A., Ruiz-Gayo, M., Javier Fernandez-Ruiz, J., Garcia-Lecumberri, C., Pelaprat, D., Fuentes, J. A., Ramos, J. A., Ambrosio, E. (1998) Maternal exposure to delta9-tetrahydrocannabinol facilitates morphine self-administration behavior and changes regional binding to central mu opioid receptors in adult offspring female rats. Brain Res. 807, 101–109. <>
62. Williams, M. T., Blankenmeyer, T. L., Schaefer, T. L., Brown, C. A., Gudelsky, G. A., Vorhees, C. V. (2003) Long-term effects of neonatal methamphetamine exposure in rats on spatial learning in the Barnes maze and on cliff avoidance, corticosterone release, and neurotoxicity in adulthood. Brain Res. Dev. Brain Res. 147, 163–175. <>
63. Won, L., Bubula, N., McCoy, H., Heller, A. (2001) Methamphetamine concentrations in fetal and maternal brain following prenatal exposure. Neurotoxicol. Teratol. 23, 349–354. <>
64. Yamamotová, A., Šlamberová, R. (2012) Behavioral and antinociceptive effects of different psychostimulant drugs in prenatally methamphetamine-exposed rats. Physiol. Res. 61, S139–S147 (Suppl. 2).
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