Mid- to late gestational morphine exposure does not alter the rewarding properties of morphine in adult male rats

Neuropharmacology

Volumn 51, Issue 2, 2006, Pages 295-304

  Riley, Michelle A ^a   Vathy, Ilona ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

CPP; Development; Drugs of abuse; Prenatal morphine exposure; Prenatal stress; Self administration

Indexed keywords

MORPHINE; MU OPIATE RECEPTOR; SODIUM CHLORIDE;

AMYGDALOID NUCLEUS; ANALGESIA; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; CONTROLLED STUDY; DRUG SELF ADMINISTRATION; FEMALE; GESTATION PERIOD; INJECTION; MALE; MESOLIMBIC DOPAMINERGIC SYSTEM; NONHUMAN; NUCLEUS ACCUMBENS; PLACE PREFERENCE; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROGENY; RAT; RECEPTOR DENSITY; REWARD; STATISTICAL SIGNIFICANCE;

ANALGESICS, OPIOID; ANIMALS; CONDITIONING (PSYCHOLOGY); FEMALE; GESTATIONAL AGE; MALE; MATERNAL EXPOSURE; MORPHINE; NARCOTICS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, SPRAGUE-DAWLEY; REWARD; SELF ADMINISTRATION;

EID: 33746225402     PISSN: 00283908     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2006.03.022     Document Type: Article

References (67)

1. Alderson H.L., Robbins T.W., and Everitt B.J. Heroin self-administration under a second-order schedule of reinforcement: acquisition and maintenance of heroin-seeking behaviour in rats. Psychopharmacology (Berl.) 153 (2000) 120-133
2. Baer J.S., Sampson P.D., Barr H.M., Connor P.D., and Streissguth A.P. A 21-year longitudinal analysis of the effects of prenatal alcohol exposure on young adult drinking. Arch. Gen. Psychiatry 60 (2003) 377-385
3. Buka S.L., Shenassa E.D., and Niaura R. Elevated risk of tobacco dependence among offspring of mothers who smoked during pregnancy: a 30-year prospective study. Am. J. Psychiatry 160 (2003) 1978-1984
4. Calatayud F., Coubard S., and Belzung C. Emotional reactivity in mice may not be inherited but influenced by parents. Physiol. Behav. 80 (2004) 465-474
5. Carta J.J., Atwater J.B., Greenwood C.R., McConnell S.R., McEvoy M.A., and Williams R. Effects of cumulative prenatal substance exposure and environmental risks on children's developmental trajectories. J. Clin. Child Psychol. 30 (2001) 327-337
6. Choi S.J., Mazzio E.A., Reams R.R., and Soliman K.F. Gestational cocaine exposure alters postnatal pituitary-adrenal axis activity and stress endurance in rats. Ann. NY Acad. Sci. 844 (1998) 336-345
7. Cicero T.J., Nock B., and Meyer E.R. Sex-related differences in morphine's antinociceptive activity: relationship to serum and brain morphine concentrations. J. Pharmacol. Exp. Ther. 282 (1997) 939-944
8. Clarke A.S., and Schneider M.L. Prenatal stress has long-term effects on behavioral responses to stress in juvenile rhesus monkeys. Dev. Psychobiol. 26 (1993) 293-304
9. Dutriez-Casteloot I., Bernet F., Dedieu J.F., Croix D., Laborie C., Montel V., Lesage J., Beauvillain J.C., and Dupouy J.P. Hypothalamic-pituitary-adrenocortical and gonadal axes and sympathoadrenal activity of adult male rats prenatally exposed to morphine. Neurosci. Lett. 263 (1999) 1-4
10. Fischer G., Jagsch R., Eder H., Gombas W., Etzersdorfer P., Schmidl-Mohl K., Schatten C., Weninger M., and Aschauer H.N. Comparison of methadone and slow-release morphine maintenance in pregnant addicts. Addiction 94 (1999) 231-239
11. Fuchs R.A., Tran-Nguyen L.T., Specio S.E., Groff R.S., and Neisewander J.L. Predictive validity of the extinction/reinstatement model of drug craving. Psychopharmacology (Berl.) 135 (1998) 151-160
12. Gagin R., Kook N., Cohen E., and Shavit Y. Prenatal morphine enhances morphine-conditioned place preference in adult rats. Pharmacol. Biochem. Behav. 58 (1997) 525-528
13. Glatt S.J., Bolanos C.A., Trksak G.H., Crowder-Dupont C., and Jackson D. Prenatal cocaine exposure alters behavioral and neurochemical sensitization to amphetamine in adult rats. Neuropharmacology 39 (2000) 599-610
14. Gue M., Bravard A., Meunier J., Veyrier R., Gaillet S., Recasens M., and Maurice T. Sex differences in learning deficits induced by prenatal stress in juvenile rats. Behav. Brain Res. 150 (2004) 149-157
15. Hall F.S., Li X.F., Goeb M., Roff S., Hoggatt H., Sora I., and Uhl G.R. Congenic C57BL/6 mu opiate receptor (MOR) knockout mice: baseline and opiate effects. Genes Brain Behav. 2 (2003) 114-121
16. Handler A., Kistin N., Davis F., and Ferre C. Cocaine use during pregnancy: perinatal outcomes. Am. J. Epidemiol 133 (1991) 818-825
17. Hiroi N., Brown J.R., Haile C.N., Ye H., Greenberg M.E., and Nestler E.J. FosB mutant mice: loss of chronic cocaine induction of Fos-related proteins and heightened sensitivity to cocaine's psychomotor and rewarding effects. Proc. Natl Acad. Sci. USA 94 (1997) 10397-10402
18. Holson R.R., and Pearce B. Principles and pitfalls in the analysis of prenatal treatment effects in multiparous species. Neurotoxicol. Teratol 14 (1992) 221-228
19. Huizink A.C., Mulder E.J., and Buitelaar J.K. Prenatal stress and risk for psychopathology: specific effects or induction of general susceptibility?. Psychol. Bull. 130 (2004) 115-142
20. Huizink A.C., Mulder E.J., Robles de Medina P.G., Visser G.H., and Buitelaar J.K. Is pregnancy anxiety a distinctive syndrome?. Early Hum. Dev. 79 (2004) 81-91
21. Keller F., and Alexopoulou T. Phonology competes with syntax: experimental evidence for the interaction of word order and accent placement in the realization of Information Structure. Cognition 79 (2001) 301-372
22. Koehl M., Lemaire V., Mayo W., Abrous D.N., Maccari S., Piazza P.V., Le Moal M., and Vallee M. Individual vulnerability to substance abuse and affective disorders: role of early environmental influences. Neurotox. Res. 4 (2002) 281-296
23. Kofman O. The role of prenatal stress in the etiology of developmental behavioural disorders. Neurosci. Biobehav. Rev. 26 (2002) 457-470
24. Koob G.F., and Le Moal M. Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacology 24 (2001) 97-129
25. Krinke G.J. The Laboratory Rat (2000), Academic Press, San Diego
26. Malanga C.J., and Kosofsky B.E. Does drug abuse beget drug abuse? Behavioral analysis of addiction liability in animal models of prenatal drug exposure. Brain Res. Dev. Brain Res. 147 (2003) 47-57
27. Markou A., Weiss F., Gold L.H., Caine S.B., Schulteis G., and Koob G.F. Animal models of drug craving. Psychopharmacology (Berl.) 112 (1993) 163-182
28. Matthes H.W., Maldonado R., Simonin F., Valverde O., Slowe S., Kitchen I., Befort K., Dierich A., Le Meur M., Dolle P., Tzavara E., Hanoune J., Roques B.P., and Kieffer B.L. Loss of morphine-induced analgesia, reward effect and withdrawal symptoms in mice lacking the mu-opioid-receptor gene. Nature 383 (1996) 819-823
29. Nair P., Schuler M.E., Black M.M., Kettinger L., and Harrington D. Cumulative environmental risk in substance abusing women: early intervention, parenting stress, child abuse potential and child development. Child Abuse Negl. 27 (2003) 997-1017
30. Piazza P.V., and Le Moal M.L. Pathophysiological basis of vulnerability to drug abuse: role of an interaction between stress, glucocorticoids, and dopaminergic neurons. Annu. Rev. Pharmacol. Toxicol. 36 (1996) 359-378
31. Piazza P.V., Deroche V., Rouge-Pont F., and Le Moal M. Behavioral and biological factors associated with individual vulnerability to psychostimulant abuse. NIDA Res. Monogr. 169 (1998) 105-133
32. Ramsey N.F., Niesink R.J., and Van Ree J.M. Prenatal exposure to morphine enhances cocaine and heroin self-administration in drug-naive rats. Drug Alcohol. Depend. 33 (1993) 41-51
33. Richardson G.A. Prenatal cocaine exposure. A longitudinal study of development. Ann. NY Acad. Sci. 846 (1998) 144-152
34. Rimanóczy A., and Vathy I. Prenatal exposure to morphine alters brain μ opioid receptor characteristics in rats. Brain Res. 690 (1995) 245-248
35. Rimanóczy A., Šlamberová R., Riley M.A., and Vathy I. Adrenocorticotropin stress response but not glucocorticoid-negative feedback is altered by prenatal morphine exposure in adult male rats. Neuroendocrinology 78 (2003) 312-320
36. Rocha B.A., Mead A.N., and Kosofsky B.E. Increased vulnerability to self-administer cocaine in mice prenatally exposed to cocaine. Psychopharmacology (Berl.) 163 (2002) 221-229
37. Rubio P., Rodriguez de Fonseca F., Martin-Calderon J.L., Del Arco I., Bartolome S., Villanua M.A., and Navarro M. Maternal exposure to low doses of delta9-tetrahydrocannabinol facilitates morphine-induced place conditioning in adult male offspring. Pharmacol. Biochem. Behav. 61 (1998) 229-238
38. Saal D., Dong Y., Bonci A., and Malenka R.C. Drugs of abuse and stress trigger a common synaptic adaptation in dopamine neurons. Neuron 37 (2003) 577-582
39. Scher M.S., Richardson G.A., Robles N., Geva D., Goldschmidt L., Dahl R.E., Sclabassi R.J., and Day N.L. Effects of prenatal substance exposure: altered maturation of visual evoked potentials. Pediatr. Neurol. 18 (1998) 236-243
40. Schindler C.J., Šlamberová R., Rimanóczy A., Hnactzuk O.C., Riley M.A., and Vathy I. Field-specific changes in hippocampal opioid mRNA, peptides, and receptors due to prenatal morphine exposure in adult male rats. Neuroscience 126 (2004) 355-364
41. Schneider M.L. Prenatal stress exposure alters postnatal behavioral expression under conditions of novelty challenge in rhesus monkey infants. Dev. Psychobiol. 25 (1992) 529-540
42. Schneider M.L., Clarke A.S., Kraemer G.W., Roughton E.C., Lubach G.R., Rimm-Kaufman S., Schmidt D., and Ebert M. Prenatal stress alters brain biogenic amine levels in primates. Dev. Psychopathol. 10 (1998) 427-440
43. Schuler M.E., Nair P., and Harrington D. Developmental outcome of drug-exposed children through 30 months: a comparison of Bayley and Bayley-II. Psychol. Assess 15 (2003) 435-438
44. Shenassa E.D., McCaffery J.M., Swan G.E., Khroyan T.V., Shakib S., Lerman C., Lyons M., Mouttapa M., Niaura R.S., Buka S.L., Leslie F., and Santangelo S.L. Intergenerational transmission of tobacco use and dependence: a transdisciplinary perspective. Nicotine Tob. Res. 5 Suppl 1 (2003) S55-S69
45. Singer L.T., Salvator A., Arendt R., Minnes S., Farkas K., and Kliegman R. Effects of cocaine/polydrug exposure and maternal psychological distress on infant birth outcomes. Neurotoxicol. Teratol. 24 (2002) 127-135
46. Šlamberová R., Rimanóczy A., Riley M.A., Schindler C.J., and Vathy I. Mu-opioid receptors in seizure-controlling brain structures are altered by prenatal morphine exposure and by male and female gonadal steroids in adult rats. Brain Res. Bull. 58 (2002) 391-400
47. Šlamberová R., Hnatczuk O.C., and Vathy I. Expression of proopiomelanocortin and proenkephalin mRNA in sexually dimorphic brain regions are altered in adult male and female rats treated prenatally with morphine. J. Pept. Res. 63 (2004) 399-408
48. Šlamberová R., Rimanóczy A., Riley M.A., and Vathy I. Hypothalamo-pituitary-adrenal axis-regulated stress response and negative feedback sensitivity is altered by prenatal morphine exposure in adult female rats. Neuroendocrinology 80 (2004) 192-200
49. Stefanis L., and Burke R.E. Transneuronal degeneration in substantia nigra pars reticulata following striatal excitotoxic injury in adult rat: time-course, distribution and morphology of cell death. Neuroscience 74 (1996) 997-1008
50. Takahashi L.K., Haglin C., and Kalin N.H. Prenatal stress potentiates stress-induced behavior and reduces the propensity to play in juvenile rats. Physiol. Behav. 51 (1992) 319-323
51. Tzschentke T.M. Measuring reward with the conditioned place preference paradigm: a comprehensive review of drug effects, recent progress and new issues. Prog. Neurobiol. 56 (1998) 613-672
52. Tzschentke T.M., and Schmidt W.J. Blockade of morphine- and amphetamine-induced conditioned place preference in the rat by riluzole. Neurosci. Lett. 242 (1998) 114-116
53. Vathy I. Effects of prenatal morphine and cocaine on postnatal behaviors and brain neurotransmitters. [Review] [118 refs]. NIDA Res. Monogr. 158 (1995) 88-114
54. Vathy I. Effects of prenatal morphine exposure on rat heterotypical sexual behavior. Physiol. Behav. 66 (1999) 667-671
55. Vathy I. Prenatal opiate exposure: long-term CNS consequences in the stress system of the offspring. Psychoneuroendocrinology 27 (2002) 273-283
56. Vathy I., and Kátay L. Effects of prenatal morphine on adult sexual behavior and brain catecholamines in rats. Dev. Brain Res. 73 (1992) 115-122
57. Vathy I.U., Etgen A.M., and Barfield R.J. Effects of prenatal exposure to morphine on the development of sexual behavior in rats. Pharmacol. Biochem. Behav. 22 (1985) 227-232
58. Vathy I., Rimanóczy A., Eaton R.C., and Kátay L. Sex dimorphic alterations in postnatal brain catecholamines after gestational morphine. Brain Res. Bull. 36 (1995) 185-193
59. Vathy I., Šlamberová R., Rimanóczy A., Riley M.A., and Bar N. Autoradiographic evidence that prenatal morphine exposure sex-dependently alters mu-opioid receptor densities in brain regions that are involved in the control of drug abuse and other motivated behaviors. Prog. Neuropsychopharmacol. Biol. Psychiatry 27 (2003) 381-393
60. 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., and Ambrosio E. 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 (1998) 101-109
61. Weinstock M. Does prenatal stress impair coping and regulation of hypothalamic-pituitary-adrenal axis?. Neurosci. Biobehav. Rev. 21 (1997) 1-10
62. Weinstock M. Alterations induced by gestational stress in brain morphology and behaviour of the offspring. Prog. Neurobiol. 65 (2001) 427-451
63. Weiss F., and Koob G.F. Drug addiction: functional neurotoxicity of the brain reward systems. Neurotox. Res. 3 (2001) 145-156
64. Wilson G.S. Clinical studies of infants and children exposed prenatally to heroin. Ann. NY Acad. Sci. 562 (1989) 183-194
65. Wise R.A. Opiate reward: sites and substrates. Neurosci. Biobehav. Rev. 13 (1989) 129-133
66. Wood R.D., and Spear L.P. Prenatal cocaine alters social competition of infant, adolescent, and adult rats. Behav. Neurosci. 112 (1998) 419-431
67. Yates W.R., Cadoret R.J., Troughton E.P., Stewart M., and Giunta T.S. Effect of fetal alcohol exposure on adult symptoms of nicotine, alcohol, and drug dependence. Alcohol Clin. Exp. Res. 22 (1998) 914-920