Gestational ethanol and nicotine exposure: Effects on maternal behavior, oxytocin, and offspring ethanol intake in the rat

Neurotoxicology and Teratology

Volumn 30, Issue 6, 2008, Pages 475-486

  McMurray, M S ^a   Williams, S K ^a   Jarrett, T M ^a   Cox, E T ^a   Fay, E E ^a   Overstreet, D H ^a   Walker, C H ^a   Johns, J M ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

Alcohol drinking; Development; Maternal behavior; Oxytocin; Prenatal alcohol; Prenatal nicotine

Indexed keywords

ALCOHOL; NICOTINE; OXYTOCIN;

ADOLESCENT; ALCOHOL BLOOD LEVEL; ALCOHOL CONSUMPTION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CONTROLLED STUDY; DRINKING BEHAVIOR; ENVIRONMENTAL EXPOSURE; FEMALE; FETUS DEVELOPMENT; GESTATION PERIOD; MALE; MATERNAL BEHAVIOR; MATERNAL CARE; NESTING; NONHUMAN; OSMOTIC MINIPUMP; OXYTOCIN BLOOD LEVEL; PRENATAL DRUG EXPOSURE; PRENATAL PERIOD; PREOPTIC AREA; PRIORITY JOURNAL; PROGENY; PUP (RODENT); RAT; REARING; REWARD; SMOKING; SNIFFING; SOCIAL BEHAVIOR; SPRAGUE DAWLEY RAT; TOUCH; VENTRAL TEGMENTUM;

AGE FACTORS; ALCOHOL DRINKING; ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; BIRTH WEIGHT; BODY WEIGHT; CHI-SQUARE DISTRIBUTION; ETHANOL; FEMALE; FOOD PREFERENCES; MALE; MATERNAL BEHAVIOR; NICOTINE; OXYTOCIN; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RADIOIMMUNOASSAY; RATS; RATS, SPRAGUE-DAWLEY; SEX FACTORS;

RATTUS;

EID: 53349164676     PISSN: 08920362     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ntt.2008.07.001     Document Type: Article

References (87)

1. [Anonymous]. No safe haven: children of substance-abusing parents. Columbia University: National Center on Addiction and Substance Abuse (Jan 1999)
2. Almeida O.F., Shoaib M., Deicke J., Fischer D., Darwish M.H., and Patchev V.K. Gender differences in ethanol preference and ingestion in rats. The role of the gonadal steroid environment. J. Clin. Invest. 101 (1998) 2677-2685
3. Amir L.H. Maternal smoking and reduced duration of breastfeeding: a review of possible mechanisms. Early Hum. Dev. 64 (2001) 45-67
4. Barron S., and Gilbertson R. Neonatal ethanol exposure but not neonatal cocaine selectively reduces specific isolation-induced vocalization waveforms in rats. Behav. Genet. 35 (2005) 93-102
5. Blake C.A., and Sawyer C.H. Nicotine blocks the suckling-induced rise in circulating prolactin in lactating rats. Science 177 (1972) 619-621
6. Burt A. Textbook of Neuroanatomy (1993), WB Saunders, Philadelphia
7. Byrnes E.M., Rigero B.A., and Bridges R.S. Dopamine antagonists during parturition disrupt maternal care and the retention of maternal behavior in rats. Pharmacol. Biochem. Behav. 73 (2002) 869-875
8. Cailhol S., and Mormede P. Sex and strain differences in ethanol drinking: effects of gonadectomy. Alcohol Clin. Exp. Res. 25 (2001) 594-599
9. Centers for Disease Control and Prevention. Alcohol consumption among women who are pregnant or who might become pregnant - United States, 2002. Morb. Mort. Wkly. Rep. 53 (2004) 1178-1181
10. Chen W.J., Parnell S.E., and West J.R. Nicotine decreases blood alcohol concentration in neonatal rats. Alcohol Clin. Exp. Res. 25 (2001) 1072-1077
11. Chotro M.G., Arias C., and Laviola G. Increased ethanol intake after prenatal ethanol exposure: Studies with animals. Neurosci. Biobehav. Rev. 31 (2007) 181-191
12. Damsma G., Day J., and Fibiger H.C. Lack of tolerance to nicotine-induced dopamine release in the nucleus accumbens. Eur. J. Pharmacol. 168 (1989) 363-368
13. Devaud L.L., and Chadda R. Sex differences in rats in the development of and recovery from ethanol dependence assessed by changes in seizure susceptibility. Alcohol Clin. Exp. Res. 25 (2001) 1689-1696
14. Doremus T.L., Brunell S.C., Rajendran P., and Spear L.P. Factors influencing elevated ethanol consumption in adolescent relative to adult rats. Alcohol Clin. Exp. Res. 29 (2005) 1796-1808
15. Dube S.R., Felitti V.J., Dong M., Chapman D.P., Giles W.H., and Anda R.F. Childhood abuse, neglect, and household dysfunction and the risk of illicit drug use: the adverse childhood experiences study. Pediatrics 111 (2003) 564-572
16. Falk D.E., Yi H.Y., and Hiller-Sturmhofel S. An epidemiologic analysis of co-occurring alcohol and tobacco use and disorders: findings from the National Epidemiologic Survey on Alcohol and Related Conditions. Alcohol Res. Health 29 (2006) 162-171
17. Finer L.B., and Henshaw S.K. Disparities in rates of unintended pregnancy in the United States, 1994 and 2001. Perspect. Sex Reprod. Health 38 (2006) 90-96
18. Fish E.W., Shahrokh D., Bagot R., Caldji C., Bredy T., Szyf M., and Meaney M.J. Epigenetic programming of stress responses through variations in maternal care. Ann. N.Y. Acad. Sci. 1036 (2004) 167-180
19. Francis D.D., Champagne F.C., and Meaney M.J. Variations in maternal behaviour are associated with differences in oxytocin receptor levels in the rat. J. Neuroendocrinol. 12 (2000) 1145-1148
20. Funk D., Marinelli P.W., and Le A.D. Biological processes underlying co-use of alcohol and nicotine: neuronal mechanisms, cross-tolerance, and genetic factors. Alcohol Res. Health 29 (2006) 186-192
21. Goodlett C.R., Horn K.H., and Zhou F.C. Alcohol teratogenesis: mechanisms of damage and strategies for intervention. Exp. Biol. Medicine (Maywood) 230 (2005) 394-406
22. Guyer B., Hoyert D.L., Martin J.A., Ventura S.J., MacDorman M.F., and Strobino D.M. Annual summary of vital statistics-1998. Pediatrics 104 (1999) 1229-1246
23. Hawley T.L., Halle T.G., Drasin R.E., and Thomas N.G. Children of addicted mothers: effects of the 'crack epidemic' on the caregiving environment and the development of preschoolers. Am. J. Orthopsychiatr. 65 (1995) 364-379
24. Huizink A.C., and Mulder E.J. Maternal smoking, drinking or cannabis use during pregnancy and neurobehavioral and cognitive functioning in human offspring. Neurosci. Biobehav. Rev. 30 (2006) 24-41
25. Hussey J.M., Chang J.J., and Kotch J.B. Child maltreatment in the United States: prevalence, risk factors, and adolescent health consequences. Pediatrics 118 (2006) 933-942
26. Johns J.M., Elliott D.L., Hofler V.E., Joyner P.W., McMurray M.S., Jarrett T.M., Haslup A.M., Middleton C.L., Elliott J.C., and Walker C.H. Cocaine treatment and prenatal environment interact to disrupt intergenerational maternal behavior in rats. Behav. Neurosci. 119 (2005) 1605-1618
27. Johns J.M., Lubin D.A., Walker C.H., Meter K.E., and Mason G.A. Chronic gestational cocaine treatment decreases oxytocin levels in the medial preoptic area, ventral tegmental area and hippocampus in Sprague-Dawley rats. Neuropeptides 31 (1997) 439-443
28. Johns J.M., Nelson C.J., Meter K.E., Lubin D.A., Couch C.D., Ayers A., and Walker C.H. Dose-dependent effects of multiple acute cocaine injections on maternal behavior and aggression in Sprague-Dawley rats. Dev. Neurosci. 20 (1998) 525-532
29. Johns J.M., Noonan L.R., Zimmerman L.I., Li L., and Pedersen C.A. Effects of chronic and acute cocaine treatment on the onset of maternal behavior and aggression in Sprague-Dawley rats. Behav. Neurosci. 108 (1994) 107-112
30. Kinsley C.H., Turco D., Bauer A., Beverly M., Wellman J., and Graham A.L. Cocaine alters the onset and maintenance of maternal behavior in lactating rats. Pharmacol. Biochem. Behav. 47 (1994) 857-864
31. Konig J.F.R., and Klippel R.A. The Rat Brain: A Stereotaxic Atlas of the Forebrain and Lower Parts of the Brain Stem (1963), Krieger, New York
32. Koob G.F., and Le Moal M. Neurobiology of Addiction (2006), Elsevier, London
33. Kovacs G.L., Faludi M., Falkay G., and Telegdy G. Peripheral oxytocin treatment modulates central dopamine transmission in the mouse limbic structures. Neurochem. Int. 9 (1986) 481-485
34. Kovacs G.L., Sarnyai Z., and Szabo G. Oxytocin and addiction: a review. Psychoneuroendocrinology 23 (1998) 945-962
35. Lallemand F., Ward R.J., and De Witte P. Nicotine increases ethanol preference but decreases locomotor activity during the initial stages of chronic ethanol withdrawal. Alcohol Alcohol. 42 (2007) 207-218
36. Lee A., Clancy S., and Fleming A.S. Mother rats bar-press for pups: effects of lesions of the MPOA and limbic sites on maternal behavior and operant responding for pup-reinforcement [corrected and republished article originally printed in Behav Brain Res 1999 Apr;100(1-2):15-31]. Behav. Brain Res. 108 (2000) 215-231
37. Letson G.W., Rosenberg K.D., and Wu L. Association between smoking during pregnancy and breastfeeding at about 2 weeks of age. J. Hum. Lact. 18 (2002) 368-372
38. Levine S. Developmental determinants of sensitivity and resistance to stress. Psychoneuroendocrinology 30 (2005) 939-946
39. Lichtensteiger W., and Schlumpf M. Prenatal nicotine affects fetal testosterone and sexual dimorphism of saccharin preference. Pharmacol. Biochem. Behav. 23 (1985) 439-444
40. Lubin D.A., Couch C.D., Meter K.E., Nelson C.J., and Johns J.M. Acute cocaine administration dose dependently disrupts maternal behavior in Sprague-Dawley rats [abstract]. Neuroscience (1998)
41. Lubin D.A., Elliott J.C., Black M.C., and Johns J.M. An oxytocin antagonist infused into the central nucleus of the amygdala increases maternal aggressive behavior. Behav. Neurosci. 117 (2003) 195-201
42. Marino M.D., Cronise K., Lugo Jr. J.N., and Kelly S.J. Ultrasonic vocalizations and maternal-infant interactions in a rat model of fetal alcohol syndrome. Dev. Psychobiol. 41 (2002) 341-351
43. Matta S.G., and Elberger A.J. Combined exposure to nicotine and ethanol throughout full gestation results in enhanced acquisition of nicotine self-administration in young adult rat offspring. Psychopharmacology (Berl) 193 (2007) 199-213
44. May P.A., and Gossage J.P. Estimating the prevalence of fetal alcohol syndrome. A summary. Alcohol Res. Health 25 (2001) 159-167
45. Mayer A.D., and Rosenblatt J.S. A method for regulating the duration of pregnancy and the time of parturition in Sprague-Dawley rats (Charles River CD strain). Dev. Psychobiol. 32 (1998) 131-136
46. McGivern R.F., Handa R.J., and Redei E. Decreased postnatal testosterone surge in male rats exposed to ethanol during the last week of gestation. Alcohol Clin. Exp. Res. 17 (1993) 1215-1222
47. Means L.W., and Goy H.B. Reduced preference for alcohol during pregnancy and following lactation in rats. Pharmacol. Biochem. Behav. 17 (1982) 1097-1101
48. Mercelina-Roumans P.E., Ubachs J.M., and van Wersch J.W. Smoking and pregnancy. Eur. J. Obstet. Gynecol. Reprod. Biol. 75 (1997) 113-114
49. Millstein R.A., and Holmes A. Effects of repeated maternal separation on anxiety- and depression-related phenotypes in different mouse strains. Neurosci. Biobehav. Rev. 31 (2007) 3-17
50. Moffett M.C., Vicentic A., Kozel M., Plotsky P., Francis D.D., and Kuhar M.J. Maternal separation alters drug intake patterns in adulthood in rats. Biochem. Pharmacol. 73 (2007) 321-330
51. Niccols A. Fetal alcohol syndrome and the developing socio-emotional brain. Brain Cogn. 65 (2007) 135-142
52. Numan M., and Insel T.R. The Neurobiology of Parental Behavior (2003), Springer-Verlag, New York
53. Office of Applied Studies. Results from the 2006 National Survey on Drug Use and Health: National findings (DHHS Publication No. SMA 07-4293, NSDUH Series H-32) (2007), Substance Abuse and Mental Health Services Administration, Rockville, MD
54. Overstreet D.H., Knapp D.J., and Breese G.R. Similar anxiety-like responses in male and female rats exposed to repeated withdrawals from ethanol. Pharmacol. Biochem. Behav. 78 (2004) 459-464
55. Overton P.G., and Clark D. Burst firing in midbrain dopaminergic neurons. Brain Res. Brain Res. Rev. 25 (1997) 312-334
56. Parnell S.E., West J.R., and Chen W.J. Nicotine decreases blood alcohol concentrations in adult rats: a phenomenon potentially related to gastric function. Alcohol Clin. Exp. Res. 30 (2006) 1408-1413
57. Pedersen C.A., Ascher J.A., Monroe Y.L., and Prange A.J. Oxytocin induces maternal behavior in virgin female rats. Science 216 (1982) 648-650
58. Pedersen C.A., and Boccia M.L. Oxytocin links mothering received, mothering bestowed and adult stress responses. Stress 5 (2002) 259-267
59. Pedersen C.A., and Boccia M.L. Oxytocin antagonism alters rat dams' oral grooming and upright posturing over pups. Physiol. Behav. 80 (2003) 233-241
60. Pedersen C.A., Caldwell J.D., Peterson G., Walker C.H., and Mason G.A. Oxytocin activation of maternal behavior in the rat. Ann. N.Y. Acad. Sci. 652 (1992) 58-69
61. Pedersen C.A., Caldwell J.D., Walker C., Ayers G., and Mason G.A. Oxytocin activates the postpartum onset of rat maternal behavior in the ventral tegmental and medial preoptic areas. Behav. Neurosci. 108 (1994) 1163-1171
62. Pedersen C.A., and Prange Jr. A.J. Induction of maternal behavior in virgin rats after intracerebroventricular administration of oxytocin. Proc. Natl. Acad. Sci. U. S. A. 76 (1979) 6661-6665
63. Pepino M.Y., Abate P., Spear N.E., and Molina J.C. Disruption of maternal behavior by alcohol intoxication in the lactating rat: a behavioral and metabolic analysis. Alcohol Clin. Exp. Res. 26 (2002) 1205-1214
64. Philpot R., and Kirstein C. Developmental differences in the accumbal dopaminergic response to repeated ethanol exposure. Ann. N.Y. Acad. Sci. 1021 (2004) 422-426
65. Ristuccia R.C., and Spear L.P. Adolescent ethanol sensitivity: hypothermia and acute tolerance. Ann. N.Y. Acad. Sci. 1021 (2004) 445-447
66. Sarnyai Z., Biro E., Babarczy E., Vecsernyes M., Laczi F., Szabo G., Krivan M., Kovacs G.L., and Telegdy G. Oxytocin modulates behavioural adaptation to repeated treatment with cocaine in rats. Neuropharmacology 31 (1992) 593-598
67. Sarnyai Z., and Kovacs G.L. Role of oxytocin in the neuroadaptation to drugs of abuse. Psychoneuroendocrinology 19 (1994) 85-117
68. Sarnyai Z., Szabo G., Kovacs G.L., and Telegdy G. Oxytocin attenuates the cocaine-induced exploratory hyperactivity in mice. Neuroreport 1 (1990) 200-202
69. Sarnyai Z., Viski S., Krivan M., Szabo G., Kovacs G.L., and Telegdy G. Endogenous oxytocin inhibits morphine tolerance through limbic forebrain oxytocin receptors. Brain Res. 463 (1988) 284-288
70. Sobrian S.K., Jones B.L., James H., Kamara F.N., and Holson R.R. Prenatal ethanol preferentially enhances reactivity of the dopamine D1 but not D2 or D3 receptors in offspring. Neurotoxicol. Teratol. 27 (2005) 73-93
71. Spear L.P. The adolescent brain and age-related behavioral manifestations. Neurosci. Biobehav. Rev. 24 (2000) 417-463
72. Subramanian M.G. Alcohol inhibits suckling-induced oxytocin release in the lactating rat. Alcohol 19 (1999) 51-55
73. Szabo G., Kovacs G.L., Szekeli S., and Telegdy G. The effects of neurohypophyseal hormones on tolerance to the hypothermic effect of ethanol. Alcohol 2 (1985) 567-574
74. Szabo G., Kovacs G.L., and Telegdy G. Effects of neurohypophyseal peptide hormones on alcohol dependence and withdrawal. Alcohol Alcohol. 22 (1987) 71-74
75. Truxell E.M., Molina J.C., and Spear N.E. Ethanol intake in the juvenile, adolescent, and adult rat: effects of age and prior exposure to ethanol. Alcohol Clin. Exp. Res. 31 (2007) 755-765
76. Tyler R., Howard J., Espinosa M., and Doakes S.S. Placement with substance-abusing mothers vs. placement with other relatives: infant outcomes. Child Abuse Negl. 21 (1997) 337-349
77. Vaglenova J., Birru S., Pandiella N.M., and Breese C.R. An assessment of the long-term developmental and behavioral teratogenicity of prenatal nicotine exposure. Behav. Brain Res. 150 (2004) 159-170
78. Varlinskaya E.I., and Spear L.P. Acute effects of ethanol on social behavior of adolescent and adult rats: role of familiarity of the test situation. Alcohol Clin. Exp. Res. 26 (2002) 1502-1511
79. Varlinskaya E.I., and Spear L.P. Acute ethanol withdrawal (hangover) and social behavior in adolescent and adult male and female Sprague-Dawley rats. Alcohol Clin. Exp. Res. 28 (2004) 40-50
80. Vernotica E.M., Lisciotto C.A., Rosenblatt J.S., and Morrell J.I. Cocaine transiently impairs maternal behavior in the rat. Behav. Neurosci. 110 (1996) 315-323
81. Vernotica E.M., Rosenblatt J.S., and Morrell J.I. Acute cocaine alters all components of established postpartum maternal behavior in the rat [abstract]. Soc. Neurosci. Abstr. (1996)
82. Vernotica E.M., Rosenblatt J.S., and Morrell J.I. Microinfusion of cocaine into the medial preoptic area or nucleus accumbens transiently impairs maternal behavior in the rat. Behav. Neurosci. 113 (1999) 377-390
83. E.M. Vernotica, J.S. Rosenblatt, J.I. Morrell. A Single Injection of Cocaine Impairs Postpartum Maternal Behavior in the Rat [dissertation]. 2007.
84. Vorhees C.V. A fostering/crossfostering analysis of the effects of prenatal ethanol exposure in a liquid diet on offspring development and behavior in rats. Neurotoxicol. Teratol. 11 (1989) 115-120
85. Wasserman D.R., and Leventhal J.M. Maltreatment of children born to cocaine-dependent mothers. Am. J. Dis. Child. 147 (1993) 1324-1328
86. Yoshimoto K., McBride W.J., Lumeng L., and Li T.K. Alcohol stimulates the release of dopamine and serotonin in the nucleus accumbens. Alcohol 9 (1992) 17-22
87. Zimmerberg B., and Gray M.S. The effects of cocaine on maternal behaviors in the rat. Physiol. Behav. 52 (1992) 379-384