Abstract
Pubescent (30 day old) male rats were maintained on an alcohol liquid diet containing 35% ethanol-derived calories (ALC) for 39 days or were pairfed an isocaloric control diet (PF). The concentration of alcohol in the diet was gradually increased to permit adaptation, then stabilized and then gradually tapered to prevent an alcohol withdrawal syndrome. Following a drug-free period (2 weeks), the males were mated with nontreated females. Offspring were evaluated on several developmental indices and on various learning/memory tasks to assess functional deficits in adulthood. Offspring sired by ALC-treated males did not differ from the offspring of PF males on several developmental parameters including body weights, when developmental landmarks appeared, or on tests of sensorimotor development. As adults, male offspring groups did not differ on tests of activity or on an object exploration/recognition task. However, male offspring of ALC-treated males demonstrated impaired acquisition performance (days and errors to criterion) on a win-shift spatial discrimination in an eight-arm radial maze and on a win-stay discrimination (days to criterion) conducted in a T-maze at a later age. The radial maze results were replicated in a subsequent experiment using different groups of rats.
References
Abel EL (1984) Fetal alcohol syndrome/fetal alcohol effects. Plenum Press, New York
Abel EL (1989) Paternal and maternal alcohol consumption: effects on offspring in two strains of rats. Alcohol Clin Exp Res 13:533–541
Abel EL, Bilitzke P (1990) Paternal alcohol exposure: paradoxical effect in mice and rats. Psychopharmacology 100:159–164
Abel EL, Lee JA (1988) Paternal alcohol exposure affects offspring behavior but not body or organ weights in mice. Alcohol Clin Exp Res 12:349–355
Abel EL, Moore C (1987) Effects of paternal alcohol consumption in mice. Alcohol Clin Exp Res 11:533–535
Abel EL, Tan SE (1988) Effects of paternal alcohol consumption on pregnancy outcome in rats. Neurotoxicol Teratol 10:187–192
Adams J, Buelke-Sam J, Kimmel CA, Nelson CJ, Reiter LW, Sobotka TJ, Tilson HA, Nelson BK (1985) Collaborative behavioral teratology study: protocol design and testing procedures. Neurobehav Toxicol Teratol 7:579–586
Adams P, Fabricant J, Legator MS (1981) Cyclophosphamide-induced spermatogenic effects detected in the F1 generation by behavioral testing. Science 211:80–82
Al-Rabini S, Miller MW (1989) Effect of prenatal exposure to ethanol on the ultrastructure of layer V of mature rat somatosensory cortex. J Neurocytol 18:711–729
Anderson RA, Furby JE, Oswald C, Zaneveld LJD (1981) Teratological evaluation of mouse fetuses after paternal alcohol ingestion. Neurobehav Toxicol Teratol 3:117–120
Anderson RA, Willis BR, Oswald C, Zaneveld LJD (1983) Ethanol-induced male infertility: impairment of spermatozoa. J Pharmacol Exp Ther 225:479–486
Barnes DE, Walker DW (1981) Prenatal ethanol exposure permanently reduces the number of pyramidal neurons in rat hippocampus. Dev Brain Res 1:333–340
Beatty WW (1979) Gonadal hormones and sex differences in non-reproductive behaviors in rodents: organizational and activational influences. Horm Behav 12:112–163
Beatty WW (1984) Hormonal organization of sex differences in play fighting and spatial behavior. Prog Brain Res 61:320–324
Brady K, Herrera Y, Zenick H (1975) Influence of paternal lead exposure on subsequent learning ability of offspring. Pharmacol Biochem Behav 3:561–565
Buelke-Sam J, Kimmel CA, Adams J, Nelson CJ, Vorhees CV, Wright DC, St. Omer V, Korol BA, Butcher RE, Geyer MA, Holson JF, Kutscher CL, Wayner MJ (1985) Collaborative behavioral teratology study: results. Neurobehav Toxicol Teratol 7:591–624
Burd L, Martsolf JT (1989) Fetal alcohol syndrome: diagnosis and syndromal variability. Physiol Behav 46:39–43
Campbell JH, Zimmerman EG (1982) Automodulation of genes: a proposed mechanism for persisting effects of drugs and hormones in mammals. Neurobehav Toxicol Teratol 4:435–439
Cantwell D (1972) Psychiatric illness in the families of hyperactive children. Arch Gen Psychiatry 27:414–417
Cicero TJ, Adams ML, O'Connor L, Nock B, Meyer ER, Wozniak D (1990) Influence of chronic alcohol on representative indices of puberty and sexual maturation in male rats and the development of their progeny. J Pharmacol Exp Ther 255:707–715
Clarren SK, Smith DW (1978) The fetal alcohol syndrome. N Engl J Med 298:1063–1067
Cohen FL (1986) Paternal contributions to birth defects. Nurs Clin North Am 21:49–64
Dawson JLM, Cheung YM, Lau RTS (1973) Effects of neonatal sex hormones on sex-based cognitive abilities in the white rat. Psychologia 16:17–24
Ennaceur A, Delacour J (1988) A new one-trial test for neurobiological studies of memory in rats. 1: behavioral data. Behav Brain Res 31:47–59
Ervin CS, Little RE, Streissguth AP, Beck DE (1984) Alcoholic fathering and its relation to child's intellectual development: a pilot investigation. Alcohol Clin Exp Res 8:362–365
Fabricant JD, Legator MS, Adams PM (1983) Post-meiotic cell mediation of behavior in progeny of male rats treated with cyclophosphamide. Mutat Res 119:185–190
Friedler G (1985) Effects of limited paternal exposure to xenobiotic agents on development of progeny. Neurobehav Toxicol Teratol 7:739–743
Friedler G, Cicero TJ (1987) Paternal pregestational opiate exposure in male mice: neuroendocrine deficits in their offspring. Res Commun Subst Abuse 8:109–116
Hegedüs AM, Alterman AI, Tarter RE (1984) Learning achievement in sons of alcoholics. Alcohol Clin Exp Res 8:330–333
Hepler DJ, Wenk GL, Cribbs BL, Olton DS, Coyle JT (1985) Memory impairments following basal forebrain lesions. Brain Res 346:8–14
Joffe JM, Soyka LF (1982) Paternal drug exposure: Effects on reproduction and progeny. Semina Perinatol 6:116–124
Jones KL, Smith DW (1973) Recognition of the fetal alcohol syndrome in early infancy.Lancet II:999–1001
Joseph R, Hess S, Birecree E (1978) Effect of hormone manipulations and exploration on sex differences in maze learning. Behav Biol 24:364–377
Keppel G (1973) Design and analysis: a researcher's handbook. Prentice Hall, Englewood Cliffs, NJ, pp 512–513
Miller MW, Dow-Edwards DL (1988) Structural and metabolic alterations in rat cerebral cortex induced by prenatal exposure to ethanol. Brain Res 474:316–326
Morrison J, Stewart M (1971) A family study of the hyperactive child syndrome. Biol Psychiatry 3:189–195
Morrison J, Stewart M (1973) The psychiatric status of the legal families of adopted hyperactive children. Arch Gen Psychiatry 28:888–891
Neidengard L, Carter TE (1978) Klippel-Feil malformation complex in fetal alcohol syndrome. Am J Dis Child 132:929–930
Nelson BK, Brightwell WS, Burg JR, Massari VJ (1984) Behavioral and neurochemical alterations in the offspring of rats after maternal or paternal inhalation exposure to the industrial solvent 2-methoxyethanol. Pharmacol Biochem Behav 20:269–279
Nylander I (1960) Children of alcoholic fathers. Acta Pediatr 49:134
Reyes E, Wolfe J, Savage DD (1989) The effects of prenatal alcohol exposure on radial arm maze performance in adult rats. Physiol Behav 46:45–48
Shaywitz BA, Griffith GG, Warshaw JB (1979) Hyperactivity and cognitive deficits in developing rat pups born to alcoholic mothers: an experimental model of the expanded fetal alcohol syndrome. Neurobehav Toxicol 1:113–122
Tarter RE, Hegedüs AM, Goldstein S, Shelly C, Alterman AI (1974) Adolescent sons of alcoholics: neuropsychological and personality characteristics. Alcohol Clin Exp Res 8:216–222
van Haaren F, Wouters M, van de Poll NE (1987) Absence of behavioral differences between male female rats in different radial-maze procedures. Physiol Behav 39:409–412
West JR, Hodges CA, Black AC Jr (1981) Prenatal exposure to ethanol alters the organization of hippocampal mossy fibers in rats. Science 211:957–959
Wilkinson L (1987) SYSTAT: The system for statistics. Evanston, IL: SYSTAT
Williams CL, Barnett AM, Meck WH (1990) Organizational effects of early gonadal secretions on sexual differentiation in spatial memory. Behav Neurosci 104:84–97
Wozniak DF, Stewart GR, Finger S, Olney JW (1989) Comparison of behavioral effects of nucleus basalis magnocellularis lesions and somatosensory cortex ablation in the rat. Neuroscience 32:685–700
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Wozniak, D.F., Cicero, T.J., Kettinger, L. et al. Paternal alcohol consumption in the rat impairs spatial learning performance in male offspring. Psychopharmacology 105, 289–302 (1991). https://doi.org/10.1007/BF02244324
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DOI: https://doi.org/10.1007/BF02244324