Postnatal environmental or experiential amelioration of neurobehavioral effects of perinatal alcohol exposure in rats

Neuroscience and Biobehavioral Reviews

Volumn 31, Issue 2, 2007, Pages 202-211

  Hannigan, John H ^a,b   O'Leary Moore, Shonagh K ^a,c   Berman, Robert F ^d  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c WAYNE STATE UNIVERSITY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Alcohol related neurodevelopmental disorders (ARND); Animal models; Environmental enrichment; Fetal alcohol syndrome (FAS); Treatment (Therapy)

Indexed keywords

ADAPTIVE BEHAVIOR; ALCOHOL CONSUMPTION; BRAIN DEVELOPMENT; COGNITION; ENVIRONMENTAL ENRICHMENT; ENVIRONMENTAL EXPOSURE; FETAL ALCOHOL SYNDROME; LEARNING DISORDER; NERVE CELL PLASTICITY; NEUROENDOCRINE SYSTEM; NEWBORN ASSESSMENT; NONHUMAN; PRENATAL EXPOSURE; PRIORITY JOURNAL; REVIEW;

ANIMALS; BEHAVIOR, ANIMAL; COGNITIVE THERAPY; DISEASE MODELS, ANIMAL; ENVIRONMENT; FEMALE; FETAL ALCOHOL SYNDROME; HANDLING (PSYCHOLOGY); HUMANS; PREGNANCY; RATS;

EID: 33846047856     PISSN: 01497634     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neubiorev.2006.06.019     Document Type: Review

References (104)

1. Abel E.L. An update on the incidence of FAS: FAS is not an equal opportunity birth defect. Neurotoxicology and Teratology 17 (1995) 437-443
2. Abel E.L., and Hannigan J.H. Maternal risk factors in fetal alcohol syndrome: provocative and permissive influences. Neurotoxicology and Teratology 17 (1995) 445-462
3. Abel E.L., and Sokol R.J. A revised conservative estimate of the incidence of FAS and its economic impact. Alcoholism- Clinical and Experimental Research 15 (1991) 514-524
4. Ader R. Effects of early experiences on emotional and physiological reactivity in the rat. Journal of Computational Physiology and Psychology 66 (1968) 264-268
5. Barnes D.E., and Walker D.N. Prenatal ethanol exposure permanently reduces the number of pyramidal neurons in rat hippocampus. Developmental Brain Research 1 (1981) 3-24
6. Beblo B., Stark K., Murthy M., Janisse J., Rockett R., Whitty J.E., Buda-Abela M., Martier S.S., Sokol R.J., Hannigan J.H., and Salem Jr. N. Effects of alcohol intake during pregnancy on docosahexaenoic acid and arachidonic acid in umbilical cord vessels of Black women. Pediatrics 115 (2005) 194-203
7. Berman R.F., and Hannigan J.H. Effects of prenatal alcohol exposure in rats on the hippocampus: spatial behavior, electrophysiology and neuroanatomy. Hippocampus 10 (2000) 94-110
8. Berman R.F., Hannigan J.H., Sperry M.A., and Zajac C.S. Prenatal alcohol exposure eliminates the effects of environmental enrichment on hippocampal dendritic spine density. Alcohol 13 (1996) 209-216
9. Bertrand J., Floyd R.L., Weber M.K., Connor M., Riley E.P., Johnson K.A., and Cohen D.E. National Task Force on FAS/FAE. Fetal Alcohol Syndrome: Guidelines for Referral and Diagnosis (2004), Center for Disease Control and Prevention, Atlanta, GA
10. Bonthius D.J., and West J.R. Permanent neuronal deficits in rats exposed to alcohol during the brain growth spurt. Teratology 44 (1991) 147-163
11. Camp D.M., Robinson T.E., and Becker J.B. Sex differences in the effects of early experience on the development behavioral and brain asymmetries in rats. Physiology and Behavior 33 (1984) 433-439
12. Clausing P. Interaction of prenatal ethanol exposure (PEE) and preweaning environmental enrichment on conditioned taste aversion and other endpoints in mice. Neurotoxicology and Teratology 2 (2000) 113-123
13. Clausing P., Mothes H.K., Opitz B., and Kormann S. Differential effects of communal rearing and preweaning handling on open field behavior and hot plate latencies in mice. Behavioural Brain Research 82 (1997) 179-184
14. DeNelsky G.Y., and Denenberg V.H. Infantile stimulation and adult exploratory behavior: effects of handling upon tactual variation seeking. Journal of Computational Physiological and Psychology 63 (1967) 309-312
15. Denenberg V.H. Critical periods, stimulus input, and emotional reactivity: a theory of infantile stimulation. Psychological Review 71 (1964) 335-351
16. Denenberg V.H., Woodcock, and Rosenberg K.M. Long-term effects of preweaning and postweaning free-environment experience on rats problem solving behavior. Journal of Computational Physiology and Psychology 66 (1968) 533-535
17. Dewey S.L., and West J.R. Evidence for altered lesion-induced sprouting in the dentate gyrus of adult rats exposed to ethanol in utero. Alcohol 1 (1984) 81-88
18. Dobbing J., and Sands J. Comparative aspects of the brain growth spurt. Early Human Development 3 1 (1979) 79-83
19. Dong W.K., and Greenough W.T. Plasticity of nonneuronal brain tissue: roles in developmental disorders. Mental Retardation and Developmental Disabilities Research Review 10 (2004) 85-90
20. Ferrer I., Galofre F., Lopez-Tejero D., and Llobera M. Morphological recovery of hippocampal pyramidal neurons in the adult rat exposed in utero to ethanol. Toxicology 48 (1988) 191-197
21. Fiala B.A., Joyce J.N., and Greenough W.T. Environmental complexity modulates growth of granule cell dendrites in developing but not adult hippocampus of rats. Experimental Neurology 59 (1978) 372-383
22. Gabriel K.I., and Weinberg J. Effects of prenatal ethanol exposure and postnatal handling on conditioned taste aversion. Neurotoxicology and Teratology 23 (2001) 167-176
23. Gabriel K.I., Johnston S., and Weinberg J. Prenatal ethanol exposure and spatial navigation: effects of postnatal handling and aging. Developmental Psychobiology 40 (2002) 345-357
24. Gabriel K.I., Glavas M.M., Ellis L., and Weinberg J. Postnatal handling doesnot normalize hypothalamic corticotropin-releasing factor nRNA levels in animals prenatally exposed to ethanol. Developmental Brain Research 157 (2005) 74-82
25. Gadow K.D. Children on Medication vol. I (1986), Little, Brown, and Co, Boston
26. Gallo P.V., and Weinberg J. Neuromotor development and response inhibition following prenatal ethanol exposure. Neurobehavioral Toxicology and Teratology 4 (1982) 505-513
27. Gillespie R.A., Eriksen J., Hao H.L., and Druse M.J. Effects of maternal ethanol consumption and buspirone treatment on dopamine and norepinephrine reuptake sites and D1 receptors in offspring. Alcoholism-Clinical and Experimental Research 21 (1997) 452-459
28. Gottesfield Z., Garcia C.J., Lingham R.B., and Chronister R.B. Prenatal ethanol exposure impairs lesion-induced plasticity in a dopaminergic synapse after maturity. Neuroscience 29 (1989) 715-723
29. Greenough W.T. Enduring brain effects of differential experience and training. In: Rosenzweig M.R., and Bennett E.L. (Eds). Neural Mechanisms of Learning and Memory (1976), MIT Press, Cambridge, MA 255-278
30. Hannigan J.H. What research with animals is telling us about alcohol-related neurodevelopmental disorders. Pharmacology and Biochemical Behaviour 55 (1996) 489-500
31. Hannigan J.H., and Armant D.R. Alcohol in pregnancy and neonatal outcome. Seminal Neonatology 5 (2000) 243-254
32. Hannigan J.H., and Berman R.F. Amelioration of fetal alcohol-related neurodevelopmental disorders in rats. Exploring pharmacological and environmental treatments. Neurotoxicology and Teratology 22 (2000) 103-111
33. Hannigan J.H., and Randall S. Behavioral pharmacology in animals exposed prenatally to alcohol. In: Abel E.L. (Ed). Fetal Alcohol Syndrome: From Mechanism to Prevention (1996), CRC Press, Boca Raton 191-213
34. Hannigan J.H., and Riley E.P. Prenatal ethanol exposure alters gait in rats. Alcohol 5 (1988) 451-454
35. Hannigan J.H., Berman R.F., and Zajac C.S. Environmental enrichment and the behavioral effects of prenatal exposure to alcohol in rats. Neurotoxicology and Teratology 15 (1993) 261-266
36. Heaton M.B., Mitchell J.J., and Paiva M. Overexpression of NGF ameliorates ethanol neurotoxicity in the developing cerebellum. Journal of Neurobiology 45 (2000) 95-104
37. Hess J.L., Denenberg V.H., Zarrow M.X., and Pfeifer W.D. Modification of the corticosterone response curve as a function of handling in infancy. Physiology & Behavior 4 (1969) 109-112
38. Hinde J. Early interventions for alcohol-affected children. In: Kleinfeld J., and Wescott S. (Eds). Fantastic Antone Succeeds: Experiences in Educating Children with Fetal Alcohol Syndrome (1993), University of Alaska Press, Fairbanks 131-147
39. ICCFAS (Interagency Coordinating Committee on Fetal Alcohol Syndrome), 2000. Early childhood neurobehavioral assessment for the differential diagnosis of fetal alcohol syndrome and alcohol-related neurodevelopmental disorder, NIAAA, 〈http://www.niaaa.nih.gov/fas/report/early_childhood.html〉.
40. Jacobson J.L., and Jacobson S.W. Prenatal alcohol exposure and neurobehavioral development: where is the threshold?. Alcohol Health & Research World 18 (1994) 30-36
41. Jones K.L., and Smith D.W. Recognition of fetal alcohol syndrome in early infancy. Lancet 2 (1973) 999-1001
42. Juraska J.M., Fitch J.M., and Washburne D.L. The dendritic morphology of pyramidal neurons in the rat hippocampal CA3 area. II. Effects of gender and the environment. Brain Research 479 (1989) 115-119
43. Kempermann G., Wiskott L., and Gage F.H. Functional significance of adult neurogenesis. Current Opinion in Neurobiology 14 (2004) 186-191
44. In: Kleinfeld J., Morse B., and Wescott S. (Eds). Fantastic Antone Grows Up: Adolescents and Adults with Fetal Alcohol Syndrome (2000), University of Alaska Press, Fairbanks
45. Klintsova A.Y., Matthews J.T., Goodlett C.R., Napper R.M., and Greenough .T. Therapeutic motor training increases parallel fiber synapse number per Purkinje neuron in cerebellar cortex of rats given postnatal binge alcohol exposure: preliminary report. Alcoholism-Clinical and Experimental Research 21 (1997) 1257-1262
46. Klintsova A.Y., Cowell R.M., Swain R.A., Napper R.M.A., Goodlett C.R., and Greenough W.T. Therapeutic effects of complex motor training on motor performance deficits induced by neonatal binge-like alcohol exposure in rats: I. Behavioral results. Brain Research 800 (1998) 48-61
47. Klintsova A.Y., Goodlett C.R., Napper R.M.A., and Greenough W.T. Therapeutic motor training ameliorates cerebellar effects of postnatal binge alcohol. Neurotoxicology and Teratology 22 (2000) 125-132
48. Klintsova A.Y., Scamra C., Hoffman M., Napper R.M., Goodlett C.R., and Greenough W.T. Therapeutic effects of complex motor training on motor performance deficits induced by neonatal binge-like alcohol exposure in rats: II. a quantitative stereological study of synaptic plasticity in female rat cerebellum. Brain Research 937 (2002) 83-93
49. Krahl S.E., and Berman R.F. Neurophysiological correlates of fetal alcohol syndrome. In: Abel E.L. (Ed). Fetal Alcohol Syndrome: From Mechanisms to Prevention (1996), CRC Press, Boca Raton, FL 69-84
50. 1 neurons after prenatal ethanol exposure. Alcohol 17 (1999) 125-131
51. Lee M.H., and Rabe A. Infantile handling eliminates reversal learning deficits in rats prenatally exposed to alcohol. Alcohol 18 (1999) 49-53
52. Levine S. Infantile experience and resistance to physiological stress. Science 126 (1957) 405-406
53. Levine S. Maternal and environmental influences on the adrenocortical response to stress in weanling rats. Science 156 (1967) 258-260
54. Levine S. Developmental determinants of sensitivity and resistance to stress. Psychoneuroendocrinology 30 (2005) 939-946
55. Levine S., Haltmeyer G.C., Karas G.G., and Denenberg V.H. Physiological and behavioral effects of infantile stimulation. Physiology & Behavior 2 (1967) 55-59
56. Lewis M.H. Environmental complexity and central nervous system development and function. Mental Retardation Development Disabilities and Research Review 10 (2004) 91-95
57. Lutke J. Parental advocacy for alcohol-affected children. In: Kleinfeld J., and Wescott S. (Eds). Fantastic Antone Succeeds: Experiences in Educating Children with Fetal Alcohol Syndrome (1993), University of Alaska Press, Fairbanks 71-95
58. Mattson S.N., and Riley E.P. A review of the neurobehavioral deficits in children with fetal alcohol syndrome or prenatal exposure to alcohol. Alcoholism-Clinical and Experimental Research 22 (1998) 279-294
59. Mattson S.N., Riley E.P., Gramling L., Delis D.C., and Jones K.L. Neuropsychological comparison of alcohol-exposed children with or without physical features of fetal alcohol syndrome. Neuropsychology 12 (1998) 146-153
60. Mattson S.N., Schoenfeld A.M., and Riley E.P. Teratogenic effects of alcohol on brain and behavior. Alcohol Research & Health 25 (2001) 185-191
61. Meaney M.J., Mitchell J.B., Aitken D.H., Bhatnagar S., Bodnoff S.R., Iny L.J., and Sarrieau A. The effects of neonatal handling on the development of the adrenocortical response to stress: implications for neuropathology and cognitive deficits in later life. Psychoneuroendocrinology 16 (1991) 85-103
62. Meaney M.J., Diorio J., Francis D., Widdowson J., LaPlante P., Caldji C., Sharma S., and Seckl J.R. Early environmental regulation of forebrain glucocorticoid receptor gene expression: implications for adrenocortical responses to stress. Developmental Neuroscience 18 (1996) 49-72
63. Mitchell J.J., Paiva M., and Heaton M.B. The antioxidants vitamin E and beta-carotene protect against ethanol-induced neurotoxicity in embryonic rat hippocampal cultures. Alcohol 17 (1999) 163-168
64. Mohammed A.H., Henriksson B.G., Soderstrom S., Ebendal T., Olsson T., and Seckl J.R. Environmental influences on the central nervous system and their implications for the aging rat. Behavioural Brain Research 57 (1993) 183-191
65. Morse B.A., and Weiner L. Rehabilitation approaches for fetal alcohol syndrome. In: Spohr H.L., and Steinhausen H.C. (Eds). Alcohol, Pregnancy and the Developing Child (1996), Cambridge University Press, New York 249-268
66. Mothes H.K., Opitz B., Werner R., and Clausing P. Effects of prenatal ethanol exposure and early experience an home cage and open field activity in mice. Neurotoxicology and Teratology 18 (1996) 59-65
67. Napper R.M.A., and West J.R. Permanent neuronal cell loss in the cerebellum of rats exposed to continuous low blood alcohol levels during the brain growth spurt: a stereological investigation. Journal of Comparative Neurology 362 (1995) 283-292
68. Nordstrom Bailey B., Sood B.G., Sokol R.J., Ager J., Janisse J., Hannigan J.H., Covington C., and Delaney-Black V. Gender and alcohol moderate prenatal cocaine effects on teacher-report of child behavior. Neurotoxicology and Teratology 27 (2005) 181-189
69. Ogilvie K.M., and Rivier C. Prenatal alcohol exposure results in hyperactivity of the hypothalamic-pituitary-adrenal axis of the offspring: modulation by fostering at birth and postnatal handling. Alcoholism-Clinical and Experimental Research 21 (1997) 424-429
70. O'Leary S.K., McMechan A.P., Berman R.F., and Hannigan J.H. Persistence of environmental enrichment effects after prenatal alcohol exposure on morris water maze performance. Developmental Psychobiology 41 (2002) 318 #84 Abstract
71. Opitz B., Mothes H.K., and Clausing P. Effects of prenatal ethanol exposure and early experience on radial maze performance and conditioned taste aversion in mice. Neurotoxicology and Teratology 19 (1997) 185-190
72. Pilati M.L., Tritt S.H., Tio D.L., and Taylor A.N. The enhancement of morphine analgesia by fetal alcohol exposure (FAE) is attenuated by maternal treatment with naltrexone. Alcoholism-Clinical and Experimental Research 19 (1995) 103A
73. Pinaud R. Experience-dependent immediate early gene expression in the adult central nervous system: evidence from enriched-environment studies. International Journal of Neuroscience 114 (2004) 321-333
74. Roebuck T.M., Mattson S.N., and Riley E.P. Prenatal exposure to alcohol: effects on brain structure and neuropsychological functioning. In: Hannigan J.H., Spear N.E., and Goodlett C.R. (Eds). Alcohol and Alcoholism: Brain and Development (1999), L.A. Erlbaum Associates, Mahwah, NJ 11-16
75. Rosenzwieg M.R. Aspects of the search for neural mechanisms of memory. Annual Review of Psychology 47 (1996) 1-32
76. Sampson P.D., Streissguth A.P., Bookstein F.L., Little R.E., Clarren S.K., Dehaene P., Hanson J.W., and Graham Jr. J.M. Incidence of fetal alcohol syndrome and prevalence of alcohol-related neurodevelopmental disorder. Teratology 56 (1997) 317-326
77. Saunders D.E., Hannigan J.H., Zajac C.S., and Wappler N.L. Reversal of alcohol's effects on neurite extension and on neuronal GAP43/B50, N-myc, and c-myc protein levels by retinoic acid. Developmental Brain Research 86 (1995) 16-23
78. Sood B.G., Nordstrom Bailey B., Covington C., Sokol R.J., Ager J., Janisse J., Hannigan J.H., and Delaney-Black V. Gender and alcohol moderate caregiver reported child behavior after prenatal cocaine. Neurotoxicology and Teratology 27 (2005) 191-201
79. Spohr H.-L. Fetal alcohol syndrome in adolescence: long-term perspective of children diagnosed in infancy. In: Spohr H.-L., and Steinhausen H.-C. (Eds). Alcohol, Pregnancy and the Developing Child (1996), Cambridge University Press, Cambridge, MA 207-226
80. Stark K., Beblo S., Murthy M., Whitty J.E., Buda-Abela M., Janisse J., Rockett H., Martier S.S., Sokol R.J., Hannigan J.H., and Salem Jr. N. Alcohol consumption in pregnant, Black women is associated with decreased plasma and erythrocyte docosahexaenoic acid. Alcoholism Clinical and Experimental Research 29 (2005) 130-140
81. In: Stratton K., Howe C., and Battaglia F. (Eds). Fetal Alcohol Syndrome: Diagnosis, Epidemiology, Prevention, and Treatment (1996), National Academy Press, Washington, DC
82. Streissguth A.P. Fetal Alcohol Syndrome: A Guide for Families and Communities (1997), P.H. Brooker Publishing, Baltimore, MD 119-207ff
83. Streissguth A.P., Aase J.M., Clarren S.K., Randels S.P., LaDue R.A., and Smith D.F. Fetal alcohol syndrome in adolescents and adults. JAMA 26 (1991) 1961-1967
84. Streissguth A.P., Sampson P.D., Olson H.C., Bookstein F.L., Barr H.M., Scott M., Feldman J., and Mirsky A.F. Maternal drinking during pregnancy: attention and short-term memory in 14-year-old offspring-a longitudinal prospective study. Alcoholism Clinical andExperimental Research 18 (1994) 202-218
85. Streissguth, A.P., Barr, H.M., Kogan, J., Bookstein, F.L., 1996. Understanding the occurrance of secondary disabilities in clients with fetal alcohol syndrome (FAS) and fetal alcohol effects (FAE), CDC Final Report # CCR008515.
86. Svikis D.S., and Reid-Quinones K. Screening and prevention of alcohol and drug use disorders in women. Obstetric and Gynecology Clinics of North America 30 (2003) 447-468
87. Thomas J.D., Weinert S.P., Sharif S., and Riley E.P. MK-801 administration during ethanol withdrawal in neonatal rat pups attenuates ethanol-induced behavioral deficits. Alcoholism Clinical andExperimental Research 21 (1997) 1218-1225
88. Thomas J.D., LaFiette M.H., Quinn V.R., and Riley E.P. Neonatal choline supplementation ameliorates the effects of prenatal alcohol exposure on a discrimination learning task in rats. Neurotoxicology and Teratology 22 (2000) 703-711
89. Thomas J.D., Fleming S.L., and Riley E.P. MK-801 can exacerbate or attenuate behavioral alterations associated with neonatal alcohol exposure in the rat, depending on the timing of administration. Alcoholism Clinical and Experimental Research 25 (2001) 764-773
90. Thomas J.D., Garrison M., and O'Neill T.M. Perinatal choline supplementation attenuates behavioral alterations associated with neonatal alcohol exposure in rats. Neurotoxicology and Teratology 26 (2004) 35-45
91. Thomas J.D., O'Neill T.M., and Dominguez H.D. Perinatal choline supplementation does not mitigate motor coordination deficits associated with neonatal alcohol exposure in rats. Neurotoxicology and Teratology 26 (2004) 223-229
92. Torasdotter M., Metsis M., Henriksson B.G., Winblad B., and Mohammed A.H. Expression of neurotrophin-3 mRNA in the rat visual cortex and hippocampus is influenced by environmental conditions. Neuroscience Letters 218 (1996) 107-110
93. Uecker A., and Nadel L. Spatial locations gone awry: object and spatial memory deficits in children with fetal alcohol syndrome. Neuropsychologia 34 (1996) 209-223
94. Uecker A., and Nadel L. Spatial but not object memory impairments in children with fetal alcohol syndrome. American Journal of Mental Retardation 103 (1998) 12-18
95. van Praag H., Kempermann G., and Gage F.H. Neural consequences of environmental enrichment. Nature Reviews Neuroscience 1 (2000) 191-198
96. Wainwright P.E., Levesque S., Krempulec L., Bulman-Fleming B., and McCutcheon D. Effects of environmental enrichment on cortical depth and Morris-maze performance in B6D2F2 mice exposed prenatally to ethanol. Neurotoxicology and Teratology 15 (1993) 11-20
97. Weinberg J., and Gallo P.V. Prenatal ethanol exposure: pituitary-adrenal activity in pregnant dams and offspring. Neurobehavioral Toxicology and Teratology 4 (1982) 515-520
98. Weinberg J., Kim C.K., and Yu W. Early handling can attenuate adverse effects of fetal ethanol exposure. Alcohol 12 (1995) 317-327
99. West J.R., Dewey S.L., and Cassell M.D. Prenatal ethanol exposure alters the post-lesion reorganization (sprouting) of acetylcholinesterase staining in the dentate gyrus of adult rats. Developmental Brain Research 12 (1984) 83-95
100. West J.R., Hodges C.A., and Black A.C. Prenatal exposure to ethanol alters the organization of hippocampal mossy fibers in rats. Science 211 (1988) 957-959
101. Will B., Galani R., Kelche C., and Rosenzwieg M.R. Recovery from brain injury in animals: relative efficacy of environmental enrichment, physical exercise or formal training (1990-2002). Progress in Neurobiology 72 (2004) 167-182
102. Williams B.M., Luo Y., Ward C., Redd K., Gibson R., Kuczaj S.A., and McCoy J.G. Environmental enrichment: effects on spatial memory and hippocampal CREB immunoreactivity. Physiology & Behavior 73 (2001) 649-658
103. Young D., Lawlor P.A., Leone P., Dragunow M., and During M.J. Environmental enrichment inhibits spontaneous apoptosis, prevents seizures and is neuroprotective. Nature Medicine 5 (1999) 448-453
104. Zimmerberg B., and Weston H.E. Postnatal stress of early weaning exacerbates behavioral outcome in prenatal alcohol-exposed juvenile rats. Pharmacology and Biochemical Behaviour 73 (2002) 45-52