Skip to main content
Log in

Paternal alcohol consumption in the rat impairs spatial learning performance in male offspring

  • Rapid Communication
  • Published:
Psychopharmacology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

References

  • Abel EL (1984) Fetal alcohol syndrome/fetal alcohol effects. Plenum Press, New York

    Google Scholar 

  • Abel EL (1989) Paternal and maternal alcohol consumption: effects on offspring in two strains of rats. Alcohol Clin Exp Res 13:533–541

    PubMed  Google Scholar 

  • Abel EL, Bilitzke P (1990) Paternal alcohol exposure: paradoxical effect in mice and rats. Psychopharmacology 100:159–164

    Article  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Abel EL, Moore C (1987) Effects of paternal alcohol consumption in mice. Alcohol Clin Exp Res 11:533–535

    PubMed  Google Scholar 

  • Abel EL, Tan SE (1988) Effects of paternal alcohol consumption on pregnancy outcome in rats. Neurotoxicol Teratol 10:187–192

    Article  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Adams P, Fabricant J, Legator MS (1981) Cyclophosphamide-induced spermatogenic effects detected in the F1 generation by behavioral testing. Science 211:80–82

    PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Anderson RA, Furby JE, Oswald C, Zaneveld LJD (1981) Teratological evaluation of mouse fetuses after paternal alcohol ingestion. Neurobehav Toxicol Teratol 3:117–120

    PubMed  Google Scholar 

  • Anderson RA, Willis BR, Oswald C, Zaneveld LJD (1983) Ethanol-induced male infertility: impairment of spermatozoa. J Pharmacol Exp Ther 225:479–486

    PubMed  Google Scholar 

  • Barnes DE, Walker DW (1981) Prenatal ethanol exposure permanently reduces the number of pyramidal neurons in rat hippocampus. Dev Brain Res 1:333–340

    Article  Google Scholar 

  • Beatty WW (1979) Gonadal hormones and sex differences in non-reproductive behaviors in rodents: organizational and activational influences. Horm Behav 12:112–163

    Article  PubMed  Google Scholar 

  • Beatty WW (1984) Hormonal organization of sex differences in play fighting and spatial behavior. Prog Brain Res 61:320–324

    Google Scholar 

  • Brady K, Herrera Y, Zenick H (1975) Influence of paternal lead exposure on subsequent learning ability of offspring. Pharmacol Biochem Behav 3:561–565

    Article  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Burd L, Martsolf JT (1989) Fetal alcohol syndrome: diagnosis and syndromal variability. Physiol Behav 46:39–43

    Article  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Cantwell D (1972) Psychiatric illness in the families of hyperactive children. Arch Gen Psychiatry 27:414–417

    PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Clarren SK, Smith DW (1978) The fetal alcohol syndrome. N Engl J Med 298:1063–1067

    PubMed  Google Scholar 

  • Cohen FL (1986) Paternal contributions to birth defects. Nurs Clin North Am 21:49–64

    PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Friedler G (1985) Effects of limited paternal exposure to xenobiotic agents on development of progeny. Neurobehav Toxicol Teratol 7:739–743

    PubMed  Google Scholar 

  • Friedler G, Cicero TJ (1987) Paternal pregestational opiate exposure in male mice: neuroendocrine deficits in their offspring. Res Commun Subst Abuse 8:109–116

    Google Scholar 

  • Hegedüs AM, Alterman AI, Tarter RE (1984) Learning achievement in sons of alcoholics. Alcohol Clin Exp Res 8:330–333

    PubMed  Google Scholar 

  • Hepler DJ, Wenk GL, Cribbs BL, Olton DS, Coyle JT (1985) Memory impairments following basal forebrain lesions. Brain Res 346:8–14

    Article  PubMed  Google Scholar 

  • Joffe JM, Soyka LF (1982) Paternal drug exposure: Effects on reproduction and progeny. Semina Perinatol 6:116–124

    Google Scholar 

  • Jones KL, Smith DW (1973) Recognition of the fetal alcohol syndrome in early infancy.Lancet II:999–1001

    Article  Google Scholar 

  • Joseph R, Hess S, Birecree E (1978) Effect of hormone manipulations and exploration on sex differences in maze learning. Behav Biol 24:364–377

    Article  PubMed  Google Scholar 

  • Keppel G (1973) Design and analysis: a researcher's handbook. Prentice Hall, Englewood Cliffs, NJ, pp 512–513

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Morrison J, Stewart M (1971) A family study of the hyperactive child syndrome. Biol Psychiatry 3:189–195

    PubMed  Google Scholar 

  • Morrison J, Stewart M (1973) The psychiatric status of the legal families of adopted hyperactive children. Arch Gen Psychiatry 28:888–891

    PubMed  Google Scholar 

  • Neidengard L, Carter TE (1978) Klippel-Feil malformation complex in fetal alcohol syndrome. Am J Dis Child 132:929–930

    PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Nylander I (1960) Children of alcoholic fathers. Acta Pediatr 49:134

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Wilkinson L (1987) SYSTAT: The system for statistics. Evanston, IL: SYSTAT

    Google Scholar 

  • Williams CL, Barnett AM, Meck WH (1990) Organizational effects of early gonadal secretions on sexual differentiation in spatial memory. Behav Neurosci 104:84–97

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02244324

Key words

Navigation