The effects of co-administration of opium and morphine with nicotine during pregnancy on spatial learning and memory of adult male offspring rats

Document Type: Original Article

Authors

1 Neuroscience Research Center, Institute of Neuropharmacology, Kerman University of Medical Sciences Kerman, Iran

2 Mashhad Cognitive Neuroscience Research Center and Dept. of Physiology, School of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran

3 Neuroscience Research Center, Institute of Neuropharmacology, Kerman University of Medical Sciences Kerman, IranReproductive Biology and Anatomy Department, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran

4 Department of physiology, Arsanjan Branch, Islamic Azad University, Fars, Iran

5 NPRC and Physiology Dept., School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, IranNeuroscience Research Center, Institute of Neuropharmacology, Kerman University of Medical Sciences Kerman, Iran

Abstract

Objective(s): Smoking opium/cigarette is a global health concern. The aim of this study was to examine learning and memory of rat male offsprings whose mothers had been exposed to either opium or morphine with nicotine during pregnancy.
Materials and Methods: Wistar rats were used for the experiments. In the female rats, opium, morphine and nicotine dependencies were induced by daily injections of drug solution for 10 days before mating. Spatial memory was tested by Morris water maze test in male pups at the postnatal day 60. The duration that took until the rats found the platform in the maze and also their swimming speed were recorded.
Results: An increase in the platform finding duration was observed for the pups of dependent mothers in comparison with the control in the training trial (P<0.05). Prenatal exposure to opium/morphine and nicotine significantly decreased the time spent in the trigger zone to find the hidden platform (P<0.05) but had no significant effect on the swimming speed in the probe test. However, no significant difference was observed in the learning and memory behavior of offspring whose mothers received morphine, opium, nicotine or the co-administration of either morphine or opium with nicotine.
Conclusion: The present study showed that the opium, morphine and nicotine abuse and co-administration of opium/morphine with nicotine during pregnancy may cause deficits in spatial learning of male rat offspring. Based on our data, no synergistic effects of co-drug administration were observed on learning and memory in male rat offspring.

Keywords


1. Jacobs DR Jr, Adachi H, Mulder I, Kromhout D, Menotti A, Nissinen A, et al. Cigarette smoking and mortality risk: twenty-five-year follow-up of the Seven Countries Study. Arch Intern Med 1999; 159: 733-740.

2. Peto R, Lopez AD, Boreham J, Thun M, Heath C Jr, Doll R. Mortality from smoking worldwide. Br Med Bull 1996; 52: 12-21.

3. Brody AL, Olmstead RE, London ED, Farahi J, Meyer JH, Grossman P, et al. Smoking-induced ventral striatum dopamine release. Am J Psychiatry 2004; 161: 1211-1218.

4. Rose JE, Behm FM, Westman EC, Mathew RJ, London ED, Hawk TC, et al. PET studies of the influences of nicotine on neural systems in cigarette smokers. Am J Psychiatry 2003; 160: 323-333.

5. Benowitz NL. Cigarette smoking and nicotine addiction.Med Clin North Am 1992; 76:415-437.

6. Lam SK, To WK, Duthie SJ, Ma HK. Narcotic addiction in pregnancy with adverse maternal and perinatal outcome.Aust N Z J ObstetGynaecol 1992; 32: 216-221.

7. Lam SK, To WK, Duthie SJ, Ma HK. The effect of smoking during pregnancy on the incidence of low birth weight among Chinese parturients.Aust N Z J ObstetGynaecol 1992; 32: 125-128.

8. Slotkin TA. Fetal nicotine or cocaine exposure: which one is worse?.J PharmacolExpTher 1998; 285: 931-945.

9. Balfour DJ. The effects of nicotine on brain neurotransmitter systems. PharmacolTher 1982; 16: 269-282.

10. Gold AB, Keller AB, Perry DC. Prenatal exposure of rats to nicotine causes persistent alterations of nicotinic cholinergic receptors. Brain Res 2009; 1250: 88-100.

11. Goodman FR. Effects of nicotine on distribution and release of 14C-norepinephrine and 14C-dopamine in rat brain striatum and hypothalamus slices. Neuropharmacology 1974; 13: 1025-1032.

12. Eppolito AK, Smith RF. Long-term behavioral and developmental consequences of pre- and perinatal nicotine. PharmacolBiochemBehav 2006; 85: 835-841.

13. Singer M. Drugs and development: the global impact of drug use and trafficking on social and economic development. Int J Drug Policy 2008; 19: 467-478.

14. Finnegan LP, Reeser DS, Connaughton JF Jr.The effects of maternal drug dependence on neonatal mortality. Drug Alcohol Depend 1977; 2: 131-140.

15. Joffe JM, Peruzovic M, Milkovic K. Progeny of male rats treated with methadone: physiological and behavioural effects. Mutat Res 1990; 229: 201-211.

16. Sarkaki A, Assaei R, Motamedi F, Badavi M, Pajouhi N. Effect of parental morphine addiction on hippocampal long-term potentiation in rats offspring. Behav Brain Res 2008; 186: 72-77.

17. Hauser KF, McLaughlin PJ, Zagon IS. Endogenous opioids regulate dendritic growth and spine formation in developing rat brain. Brain Res 1987; 416: 157-161.

18. Steingart RA, Barg J, Maslaton J, Nesher M, Yanai J. Pre- and postsynaptic alterations in the septohippocampal cholinergic innervations after prenatal exposure to drugs. Brain Res Bull 1998; 46: 203-209.

19. Schrott LM, Franklin LTM, Serrano PA. Prenatal opiate exposure impairs radial arm maze performance and reduces levels of BDNF precursor following training. Brain Res 2008; 1198: 132-140. 

20. Slamberova R, Schindler CJ, Pometlova M, Urkuti C, Purow-Sokol JA, Vathy I. Prenatal morphine exposure differentially alters learning and memory in male and female rats. PhysiolBehav 2001; 73:93-103.

21. Hammer RP Jr, Seatriz JV, Ricalde AR. Regional dependence of morphine-induced mu-opiate receptor down-regulation in perinatal rat brain. Eur J Pharmacol 1991; 209: 253-256.

22. SaberiMoghadam A, Sepehri G, Sheibani V, Haghpanah T, Divsalar K, Hajzadeh MA, et al. The effect of opium dependency of parent (s) on offspring’s spatial learning & memory in adult male rats. Iran J Basic Med Sci 2013; 16(5): 694-699.

23. Zarrindast MR, Barghi-Lashkari S, Shafizadeh M. The possible cross-tolerance between morphine- and nicotine-induced hypothermia in mice.PharmacolBiochemBehav 2001; 68: 283-289.

24. Zarrindast MR, Faraji N, Rostami P, Sahraei H, Ghoshouni H. Cross-tolerance between morphine- and nicotine-induced conditioned place preference in mice. PharmacolBiochemBehav 2003; 74: 363-369.

25. Zarrindast MR, Farzin D. Nicotine attenuates naloxone-induced jumping behaviour in morphine-dependent mice. Eur J Pharmacol 1996; 298: 1-6.

26. Mello NK, Lukas SE, Mendelson JH. Buprenorphine effects on cigarette smoking. Psychopharmacology (Berl) 1985; 86: 417-425.

27. Yoo JH, Lee SY, Loh HH, Ho IK, Jang CG. Loss of nicotine-induced behavioral sensitization in micro-opioid receptor knockout mice. Synapse 2004; 51: 219-223.

28. Malanga CJ, KosofskyBE. Does drug abuse beget drug abuse? Behavioral analysis of addiction liability in animal models of prenatal drug exposure. Brain Res Dev Brain Res 2003; 147: 47-57.

29. Salmanzadeh F, Fathollahi Y, Semnanian S, Shafizadeh M, Kazemnejad A. Dependence on morphine leads to a prominent sharing among the different mechanisms of long-term potentiation in the CA1 region of rat hippocampus. Brain Res 2003; 963: 93-100.

30. Afarinesh MR, Sheibani V, Arabzadeh S, Shamsizadeh A. Effect of chronic morphine exposure on response properties of rat barrel cortex neurons. Addict Biol 2008; 13: 31-39.

31. Fan GH, Wang LZ, Qiu HC, Ma L, Pei G. Inhibition of calcium/calmodulin-dependent protein kinase II in rat hippocampus attenuates morphine tolerance and dependence. MolPharmacol1999; 56: 39-45.

32. Trujillo KA, Akil H. Inhibition of morphine tolerance and dependence by the NMDA receptor antagonist MK-801. Science 1991; 251: 85-87.

33. Pompili A, Tomaz C, Arnone B, Tavares MC, Gasbarri A. Working and reference memory across the estrous cycle of rat: a long-term study in gonadally intact females. Behav Brain Res 2010; 213: 10-18.

34. Warren SG, Juraska JM. Sex differences and estropausal phase effects on water maze performance in aged rats. Neurobiol Learn Mem 2000; 74: 229-240.

35. Warren SG, Juraska JM. Spatial and nonspatial learning across the rat estrous cycle.BehavNeurosci 1997; 111: 259-266.

36. Fowden AL, Forhead AJ, Coan PM, Burton GJ. The placenta and intrauterine programming. J Neuroendocrinol 2008; 20: 439-450. 

37. Luck W, Nau H, Hansen R, Steldinger R. Extent of nicotine and cotinine transfer to the human fetus, placenta and amniotic fluid of smoking mothers. DevPharmacolTher 1985; 8: 384-395.

38. Bandstra ES, Morrow CE, Mansoor E, Accornero VH. Prenatal drug exposure: infant and toddler outcomes. J Addict Dis 2010; 29: 245-258.

39. Hutchings DE. Methadone and heroin during pregnancy: a review of behavioral effects in human and animal offspring. NeurobehavToxicolTeratol 1982; 4: 429-434.

40. Vaglenova J, Parameshwaran K, Suppiramaniam V, Breese C, Pandiella N, Birru S. Long-lasting teratogenic effects of nicotine on cognition: gender specificity and role of AMPA receptor function. Neurobiol Learn Mem 2008; 90: 527-536. 

41. Wang Y, Han TZ. Prenatal exposure to heroin in mice elicits memory deficits that can be attributed to neuronal apoptosis. Neuroscience 2009; 160: 330-338.

42. Sinha C, Ohadike P, Carrick P, Pairaudeau P, Armstrong D, Lindow SW. Neonatal outcome following maternal opiate use in late pregnancy. Int J GynaecolObstet 2001; 74: 241-246.

43. Friedler G. Paternal exposures: impact on reproductive and developmental outcome. An overview.PharmacolBiochemBehav 1996; 55: 691-700.

44. Zhu JH, Stadlin A. Prenatal heroin exposure. Effects on development, acoustic startle response, and locomotion in weanling rats. NeurotoxicolTeratol 2000; 22: 193-203.

45. Siddiqui A, Haq S, Shaharyar S, Haider SG. Morphine induces reproductive changes in female rats and their male offspring. ReprodToxicol 1995; 9: 143-151.

46. Hyman SE, Malenka RC, Nestler EJ. Neural mechanisms of addiction: the role of reward-related learning and memory. Annu Rev Neurosci 2006; 29: 565-598.

47. Nasiraei-Moghadam S, Sahraei H, Bahadoran H, Sadooghi M, Salimi S, Kaka G, et al. Effects of maternal oral morphine consumption on neural tube development in Wistar rats. Dev Brain Res 2005; 159: 12-17.

48. Niu L, Cao B, Zhu H, Mei B, Wang M, Yang Y, et al. Impaired in vivo synaptic plasticity in dentate gyrus and spatial memory in juvenile rats induced by prenatal morphine exposure. Hippocampus 2009; 19:649-657.

49. Ghafari S, Golalipour MJ. Prenatal morphine exposure reduces pyramidal neurons in CA1, CA2 and CA3 subfields of mice hippocampus. Iran J Basic Med Sci. 2014; 17: 155-161.

50. Park S, Knopick C, McGurk S, Meltzer HY. Nicotine impairs spatial working memory while leaving spatial attention intact. Neuropsychopharmacology 2000; 22: 200-209.

51. Houdi AA, Pierzchala K, Marson L, Palkovits M, Van Loon GR. Nicotine-induced alteration in Tyr-Gly-Gly and Met-enkephalin in discrete brain nuclei reflects altered enkephalin neuron activity. Peptides 1991; 12: 161-166.

52. Zarrindast MR, Pazouki M, Nassiri-Rad S. Involvement of cholinergic and opioid receptor mechanisms in nicotine-induced antinociception. PharmacolToxicol 1997; 81: 209-213.

53. Asadi E, Jahanshahi M, Golalipour MJ. Effect of vitamin e on oocytes apoptosis in nicotine-treated mice. Iran J Basic Med Sci 2012; 15: 880-884.

54. Che Y, Sun H, Tan H, Peng Y, Zeng T, Ma Y. The effect of prenatal morphine exposure on memory consolidation in the chick.NeurosciLett 2005; 380: 300-304.

55. Davis CP, Franklin LTM, Johnson GS, Schrott LM. Prenatal oxycodone exposure impairs spatial learning and/or memory in rats. Behav Brain Res 2010; 212: 27-34.