Nursing from an ethanol-intoxicated dam induces short- and long-term disruptions in motor performance and enhances later self-administration of the drug.

RATIONALE During interactions with an ethanol-intoxicated dam, preweanling rats encode ethanol-related chemosensory information. These experiences have been observed to enhance subsequent recognition of ethanol's chemosensory properties and to modulate learning about ethanol. OBJECTIVE The present study tested the effects of ethanol-related nursing experiences on motor function in later infancy and adolescence and on ethanol intake during adolescence. METHODS Wistar-derived rats were reared by dams intragastrically administered with ethanol (2.5 g/kg) or with water during postnatal days (PDs) 3, 5, 7, 9, 11, and 13. Later in infancy or in adolescence, these rats were tested on a motor coordination task (Accelerod) while either sober or acutely intoxicated with ethanol (1 g/kg). During adolescence, animals had simultaneous access to varying ethanol concentrations (3, 4, 5, or 6% v/v) and water. RESULTS Both infants and adolescents that had been reared by ethanol-intoxicated dams exhibited dramatic behavioral impairments in the Accelerod task when compared with the offspring of water control dams. Ethanol intoxication disrupted motor performance in both age groups, but this effect was independent of prior maternal treatment. When tested for voluntary ethanol intake as adolescents, those with prior nursing experiences with an intoxicated dam ingested more ethanol than adolescents reared by sober dams. CONCLUSIONS Early experiences with alcohol comprising interactions with an alcohol-intoxicated dam result in motor impairment and enhanced ethanol intake later in life.

[1]  M. Chotro,et al.  Prenatal exposure to ethanol increases ethanol consumption: a conditioned response? , 2003, Alcohol.

[2]  J. West,et al.  Alcohol and nutritional control treatments during neurogenesis in rat brain reduce total neuron number in locus coeruleus, but not in cerebellum or inferior olive. , 2003, Alcohol.

[3]  Robert F. Smith Animal models of periadolescent substance abuse. , 2003, Neurotoxicology and teratology.

[4]  R. Philpot,et al.  Place conditioning: age-related changes in the rewarding and aversive effects of alcohol. , 2003, Alcoholism, clinical and experimental research.

[5]  P. Connor,et al.  A 21-year longitudinal analysis of the effects of prenatal alcohol exposure on young adult drinking , 2003 .

[6]  V. Duffy,et al.  Chemosensory factors influencing alcohol perception, preferences, and consumption. , 2003, Alcoholism, clinical and experimental research.

[7]  L. Spear,et al.  Nicotine-induced conditioned place preference in adolescent and adult rats , 2002, Physiology & Behavior.

[8]  P. Plotsky,et al.  Long-lasting changes in stress-induced corticosterone response and anxiety-like behaviors as a consequence of neonatal maternal separation in Long–Evans rats , 2002, Pharmacology Biochemistry and Behavior.

[9]  N. Spear,et al.  Disruption of maternal behavior by alcohol intoxication in the lactating rat: a behavioral and metabolic analysis. , 2002, Alcoholism, clinical and experimental research.

[10]  R. Little,et al.  Alcohol, breastfeeding, and development at 18 months. , 2002, Pediatrics.

[11]  Michael J Meaney,et al.  Environmental regulation of the development of mesolimbic dopamine systems: a neurobiological mechanism for vulnerability to drug abuse? , 2002, Psychoneuroendocrinology.

[12]  P. Plotsky,et al.  Early adverse experience as a developmental risk factor for later psychopathology: Evidence from rodent and primate models , 2001, Development and Psychopathology.

[13]  M. Silveri,et al.  Acute, rapid, and chronic tolerance during ontogeny: observations when equating ethanol perturbation across age. , 2001, Alcoholism, clinical and experimental research.

[14]  M. Meaney,et al.  Development of adult ethanol preference and anxiety as a consequence of neonatal maternal separation in Long Evans rats and reversal with antidepressant treatment , 2001, Psychopharmacology.

[15]  E. M. Scordalakes,et al.  Social interaction with an intoxicated sibling can result in increased intake of ethanol by periadolescent rats. , 2001, Developmental psychobiology.

[16]  M. Meaney,et al.  Variations in maternal care in infancy regulate the development of stress reactivity , 2000, Biological Psychiatry.

[17]  S. Levine Influence of psychological variables on the activity of the hypothalamic-pituitary-adrenal axis. , 2000, European journal of pharmacology.

[18]  L. Spear The adolescent brain and age-related behavioral manifestations , 2000, Neuroscience & Biobehavioral Reviews.

[19]  S. Heil,et al.  Chronic alcohol exposure and lactation: extended observations. , 2000, Alcohol.

[20]  M. Champoux,et al.  Rearing experiences and stress-induced plasma cortisol as early risk factors for excessive alcohol consumption in nonhuman primates. , 2000, Alcoholism, clinical and experimental research.

[21]  N. Spear,et al.  The infant rat learns about alcohol through interaction with an intoxicated mother. , 2000, Alcoholism, clinical and experimental research.

[22]  K. Berridge Measuring hedonic impact in animals and infants: microstructure of affective taste reactivity patterns , 2000, Neuroscience & Biobehavioral Reviews.

[23]  M. Subramanian Alcohol inhibits suckling-induced oxytocin release in the lactating rat. , 1999, Alcohol.

[24]  N. Spear,et al.  Infant rats respond differently to alcohol after nursing from an alcohol-intoxicated dam. , 1999, Alcohol.

[25]  J. C. Molina,et al.  Chronic alcohol administration in the rat pup: effects upon later consumption of alcohol and other palatable solutions , 1999, Addiction biology.

[26]  W. P. Smotherman,et al.  Sustained attachment to the nipple in the newborn rat depends on experience with the nipple, milk, and the expression of oral grasping. , 1999, Behavioral neuroscience.

[27]  M. Meaney,et al.  Maternal care and the development of stress responses , 1999, Current Opinion in Neurobiology.

[28]  F. Bookstein,et al.  Prenatal alcohol exposure and family history of alcoholism in the etiology of adolescent alcohol problems. , 1998, Journal of studies on alcohol.

[29]  J. C. Molina,et al.  Neonatal responsiveness to alcohol odor and infant alcohol intake as a function of alcohol experience during late gestation. , 1998, Alcohol.

[30]  R. Cadoret,et al.  Effect of fetal alcohol exposure on adult symptoms of nicotine, alcohol, and drug dependence. , 1998, Alcoholism: Clinical and Experimental Research.

[31]  N. Spear,et al.  Behavioral detection of low concentrations of ethanol in milk in the preweanling rat. , 1998, Alcohol.

[32]  J. Mennella,et al.  Effects of exposure to alcohol in mother's milk on infant sleep. , 1998, Pediatrics.

[33]  Shakti Sharma,et al.  Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[34]  H. Kalant,et al.  Research on tolerance: what can we learn from history? , 1998, Alcoholism, clinical and experimental research.

[35]  Shakti Sharma,et al.  Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. , 1997, Science.

[36]  M. Subramanian Evaluation of lactational parameters after alcohol administration for four days during early or midlactation in the rat. , 1997, Alcoholism, clinical and experimental research.

[37]  W. P. Smotherman,et al.  Oral grasping of a surrogate nipple by the newborn rat. , 1997, Developmental psychobiology.

[38]  J. Mennella Infants' suckling responses to the flavor of alcohol in mothers' milk. , 1997, Alcoholism, clinical and experimental research.

[39]  A. T. Eilers,et al.  Alcohol-induced Purkinje cell loss with a single binge exposure in neonatal rats: a stereological study of temporal windows of vulnerability. , 1997, Alcoholism, clinical and experimental research.

[40]  M. Subramanian Effects of chronic alcohol administration on lactational performance in the rat. , 1995, Alcohol.

[41]  S. Kiefer Alcohol, palatability, and taste reactivity , 1995, Neuroscience & Biobehavioral Reviews.

[42]  N. Haghighat,et al.  Alcohol consumption by nursing rats and its effect on the cerebellum of the offspring. , 1994, Alcohol and alcoholism.

[43]  G. Beauchamp,et al.  Beer, breast feeding, and folklore. , 1993, Developmental psychobiology.

[44]  N. Spear,et al.  Enhanced ethanol intake in preweanling rats following exposure to ethanol in a nursing context. , 1993, Developmental psychobiology.

[45]  C. Cunningham,et al.  Species difference in sensitivity to ethanol's hedonic effects. , 1993, Alcohol.

[46]  K. Singletary,et al.  Effect of moderate ethanol consumption on mammary gland structural development and DNA synthesis in the female rat. , 1992, Alcohol.

[47]  G. Beauchamp,et al.  The transfer of alcohol to human milk. Effects on flavor and the infant's behavior. , 1991, The New England journal of medicine.

[48]  J. Volpicelli,et al.  The bidirectional effects of shock on alcohol preference in rats. , 1990, Alcoholism, clinical and experimental research.

[49]  B. Scatton,et al.  Differential Effects of Forced Locomotion, Tail‐Pinch, Immobilization, and Methyl‐β‐Carboline Carboxylate on Extracellular 3,4‐Dihydroxyphenylacetic Acid Levels in the Rat Striatum, Nucleus Accumbens, and Prefrontal Cortex: An In Vivo Voltammetric Study , 1990, Journal of neurochemistry.

[50]  J. C. Molina,et al.  Perinatal undernutrition reduced ethanol intake preference in adult recovered rats , 1990, Physiology and Behavior.

[51]  C. Goodlett,et al.  A single day of alcohol exposure during the brain growth spurt induces brain weight restriction and cerebellar Purkinje cell loss. , 1990, Alcohol.

[52]  E. Riley,et al.  Alterations in gait following ethanol exposure during the brain growth spurt in rats. , 1990, Alcoholism, clinical and experimental research.

[53]  R. Little,et al.  Maternal Alcohol Use during Breast-Feeding and Infant Mental and Motor Development at One Year , 1989 .

[54]  C. Goodlett,et al.  Differential neuronal loss following early postnatal alcohol exposure. , 1989, Teratology.

[55]  S. Vilaró,et al.  Altered ultrastructure of lactating rat mammary epithelial cells induced by chronic ethanol ingestion. , 1989, Alcoholism, clinical and experimental research.

[56]  S. Vilaró,et al.  Effects of chronic ethanol consumption on lactational performance in rat: Mammary gland and milk composition and pups' growth and metabolism , 1987, Pharmacology Biochemistry and Behavior.

[57]  G. Kirouac,et al.  Effects of Unavoidable Electric Shocks on Voluntary Alcohol Consumption in the Rat , 1987, Perceptual and motor skills.

[58]  N. Spear,et al.  Alcohol drinking patterns of young adult rats as a function of infantile aversive experiences with alcohol odor. , 1986, Behavioral and neural biology.

[59]  G. Dombrowski,et al.  The inefficient transfer of maternally fed alcohol to nursing rats. , 1986, Alcohol.

[60]  M. Caplan,et al.  Stress and conflict conditions leading to and maintaining voluntary alcohol consumption in rats , 1986, Pharmacology Biochemistry and Behavior.

[61]  M. Lawton,et al.  Alcohol in Breast Milk , 1985, The Australian & New Zealand journal of obstetrics & gynaecology.

[62]  P. S. Lasiter,et al.  Shock facilitation of taste aversion learning. , 1981, Behavioral and neural biology.

[63]  L. Pohorecky The interaction of alcohol and stress A review , 1981, Neuroscience & Biobehavioral Reviews.

[64]  J. Dobbing,et al.  Comparative aspects of the brain growth spurt. , 1979, Early human development.

[65]  J. Altman,et al.  The effect of ethanol chronically administered to preweanling rats on cerebellar development: A morphological study , 1977, Brain Research.

[66]  M. Eckardt The role of orosensory stimuli from ethanol and blood-alcohol levels in producing conditioned taste aversion in the rat , 1975, Psychopharmacologia.

[67]  J. Dobbing,et al.  Quantitative growth and development of human brain , 1973, Archives of disease in childhood.

[68]  F. Gudé,et al.  Influence of alcohol consumption on serum immunoglobulin E levels in atopic and nonatopic adults. , 2002, Alcoholism, clinical and experimental research.

[69]  N. Spear,et al.  Nursing experiences with an alcohol-intoxicated rat dam counteract appetitive conditioned responses toward alcohol. , 2001, Alcoholism, clinical and experimental research.

[70]  E. Riley,et al.  Hyperactivity in preweanling rats following postnatal alcohol exposure. , 1994, Alcohol.

[71]  L. Lumeng,et al.  Comparison of alcohol-preferring (P) and nonpreferring (NP) rats on tests of anxiety and for the anxiolytic effects of ethanol. , 1993, Alcohol.

[72]  E. Riley,et al.  Neonatal ethanol exposure: functional alterations associated with cerebellar growth retardation. , 1990, Neurotoxicology and teratology.

[73]  W. House,et al.  The effects of post-stress exposure to alcohol upon the development of alcohol consumption in rats. , 1989, Behaviour research and therapy.

[74]  N. Spear,et al.  Weanlings' transfer of conditioned ethanol aversion from olfaction to ingestion depends on the unconditioned stimulus. , 1986, Behavioral and neural biology.

[75]  S. Vilaró,et al.  Effects of chronic ethanol ingestion on circulating metabolites and liver composition in the lactating rat. , 1986, General pharmacology.