Environmental enrichment alters neurotrophin levels after fetal alcohol exposure in rats

Alcoholism: Clinical and Experimental Research

Volumn 32, Issue 10, 2008, Pages 1741-1751

  Parks, Elizabeth A ^a   McMechan, Andrew P ^b   Hannigan, John H ^b   Berman, Robert F ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

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

Author keywords

Brain derived neurotrophic factor; Environmental enrichment; Fetal alcohol syndrome; Nerve growth factor; Neurotrophin 3

Indexed keywords

ALCOHOL; BRAIN DERIVED NEUROTROPHIC FACTOR; NERVE GROWTH FACTOR; NEUROTROPHIN; NEUROTROPHIN 3;

ALCOHOL CONSUMPTION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CEREBELLUM VERMIS; CONTROLLED STUDY; ENVIRONMENTAL ENRICHMENT; FEMALE; FRONTAL CORTEX; GESTATION PERIOD; HIPPOCAMPUS; MALE; NONHUMAN; OCCIPITAL CORTEX; PRENATAL EXPOSURE; PRIORITY JOURNAL; RAT; SEX DIFFERENCE; WEANING;

ANIMALS; ANIMALS, NEWBORN; BRAIN; CENTRAL NERVOUS SYSTEM DEPRESSANTS; ENVIRONMENT; ETHANOL; FEMALE; FETAL ALCOHOL SYNDROME; LITTER SIZE; MATERNAL EXPOSURE; NERVE GROWTH FACTORS; NEUROTROPHIN 3; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; SEX RATIO; WEIGHT GAIN;

ANIMALIA; RATTUS;

EID: 52149105406     PISSN: 01456008     EISSN: 15300277     Source Type: Journal    
DOI: 10.1111/j.1530-0277.2008.00759.x     Document Type: Article

References (93)

1. Abel EL, Hannigan JH (1995) Maternal risk factors in fetal alcohol syndrome: provocative and permissive influences. Neurotoxicol Teratol 17 : 445 462.
2. Angelucci F, Aloe L, Vasquez PJ, Mathe AA (2000) Mapping the differences in the brain concentration of brain-derived neurotrophic factor (BDNF) and nerve growth factor (NGF) in an animal model of depression. Neuroreport 11 : 1369 1373.
3. Angelucci F, Fiore M, Cozzari C, Aloe L (1999) Prenatal ethanol effects on NGF level, NPY and ChAT immunoreactivity in mouse entorhinal cortex: a preliminary study. Neurotoxicol Teratol 21 : 415 425.
4. Bartesaghi R, Severi S (2004) Effects of early environment on field CA2 pyramidal neurons in the guinea-pig. Neuroscience 123 : 703 714.
5. Berman RF, Hannigan JH (2000) Effects of prenatal alcohol exposure on the hippocampus: spatial behavior, electrophysiology, and neuroanatomy. Hippocampus 10 : 94 110.
6. Berman RF, Hannigan JH, Sperry MA, Zajac CS (1996) Prenatal alcohol exposure and the effects of environmental enrichment on hippocampal dendritic spine density. Alcohol 13 : 209 216.
7. Bertrand J, Floyd RI, Weber MK, O'Connor M, Riley EP, Johnson KA, Cohen DE (2004) Fetal alcohol syndrome: Guidelines for referral and diagnosis. Centers for Disease Prevention and Diagnosis, Bethesda, MD.
8. Bimonte-Nelson HA, Granholm AC, Nelson ME, Moore AB (2008) Patterns of neurotrophin protein levels in male and female Fischer 344 rats from adulthood to senescence: how young is "young" and how old is "old"? Exp Aging Res 34 : 13 26.
9. Blanchard BA, Riley EP, Hannigan JH (1987) Deficits on a spatial navigation task following prenatal exposure to ethanol. Neurotoxicol Teratol 9 : 253 258.
10. Blum R, Konnerth A (2005) Neurotrophin-mediated rapid signaling in the central nervous system: mechanisms and functions. Physiology (Bethesda) 20 : 70 78.
11. Bonthius DJ, West JR (1990) Alcohol-induced neuronal loss in developing rats: increased brain damage with binge exposure. Alcohol Clin Exp Res 14 : 107 118.
12. Bonthius DJ, West JR (1991) Permanent neuronal deficits in rats exposed to alcohol during the brain growth spurt. Teratology 44 : 147 163.
13. Chao MV (2003) Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat Rev Neurosci 4 : 299 309.
14. Chen X, Li Y, Kline AE, Dixon CE, Zafonte RD, Wagner AK (2005) Gender and environmental effects on regional brain-derived neurotrophic factor expression after experimental traumatic brain injury. Neuroscience 135 : 11 17.
15. Clausing P, Ferguson SA, Holson RR, Allen RR, Paule MG (1995) Prenatal ethanol exposure in rats: long-lasting effects on learning. Neurotoxicol Teratol 17 : 545 552.
16. Climent E, Pascual M, Renau-Piqueras J, Guerri C (2002) Ethanol exposure enhances cell death in the developing cerebral cortex: role of brain-derived neurotrophic factor and its signaling pathways. J Neurosci Res 68 : 213 225.
17. Connor PD, Sampson PD, Streissguth AP, Bookstein FL, Barr HM (2006) Effects of prenatal alcohol exposure on fine motor coordination and balance: A study of two adult samples. Neuropsychologia 44 : 744 751.
18. Cortese BM, Moore GJ, Bailey BA, Jacobson SW, Delaney-Black V, Hannigan JH (2006) Magnetic resonance and spectroscopic imaging in prenatal alcohol-exposed children: preliminary findings in the caudate nucleus. Neurotoxicol Teratol 28 : 597 606.
19. Das KP, Chao SL, White LD, Haines WT, Harry GJ, Tilson HA, Barone S Jr (2001) Differential patterns of nerve growth factor, brain-derived neurotrophic factor and neurotrophin-3 mRNA and protein levels in developing regions of rat brain. Neuroscience 103 : 739 761.
20. Dicou E (2006) Multiple biological activities for two peptides derived from the nerve growth factor precursor. Biochem Biophys Res Commun 347 : 833 837.
21. Dreyfus CF (1998) Neurotransmitters and neurotrophins collaborate to influence brain development. Perspect Dev Neurobiol 5 : 389 399.
22. Driscoll CD, Streissguth AP, Riley EP (1990) Prenatal alcohol exposure: comparability of effects in humans and animal models. Neurotoxicol Teratol 12 : 231 237.
23. Fahnestock M, Yu G, Michalski B, Mathew S, Colquhoun A, Ross GM, Coughlin MD (2004) The nerve growth factor precursor proNGF exhibits neurotrophic activity but is less active than mature nerve growth factor. J Neurochem 89 : 581 592.
24. Falkenberg T, Mohammed AK, Henriksson B, Persson H, Winblad B, Lindefors N (1992) Increased expression of brain-derived neurotrophic factor mRNA in rat hippocampus is associated with improved spatial memory and enriched environment. Neurosci Lett 138 : 153 156.
25. Feng MJ, Yan SE, Yan QS (2005) Effects of prenatal alcohol exposure on brain-derived neurotrophic factor and its receptor tyrosine kinase B in offspring. Brain Res 1042 : 125 132.
26. Fiala BA, Joyce JN, Greenough WT (1978) Environmental complexity modulates growth of granule cell dendrites in developing but not adult hippocampus of rats. Exp Neurol 59 : 372 383.
27. Franklin TB, Perrot-Sinal TS (2006) Sex and ovarian steroids modulate brain-derived neurotrophic factor (BDNF) protein levels in rat hippocampus under stressful and non-stressful conditions. Psychoneuroendocrinology 31 : 38 48.
28. Goodlett CR, Peterson SD (1995) Sex differences in vulnerability to developmental spatial learning deficits induced by limited binge alcohol exposure in neonatal rats. Neurobiol Learn Mem 64 : 265 275.
29. Greenough WT, Chang FL (1988) Dendritic pattern formation involves both oriented regression and oriented growth in the barrels of mouse somatosensory cortex. Brain Res 471 : 148 152.
30. Hagerman RJ (1999) Fetal alcohol syndrome, in Neurodevelopmental Disorders: Diagnosis and Treatment, pp 3 59. Oxford University Press, New York.
31. Hannigan JH (1996) What research with animals is telling us about alcohol-related neurodevelopmental disorder. Pharmacol Biochem Behav 55 : 489 499.
32. Hannigan JH, Abel EL (1996) Animal models of fetal alcohol syndrome, in Alcohol, Pregnancy, and the Developing Child (Spohr HL, Steinhausen HC eds pp 63 75. Cambridge University Press, Cambridge.
33. Hannigan JH, Armant DR (2000) Alcohol in pregnancy and neonatal outcome. Semin Neonatol 5 : 243 254.
34. Hannigan JH, Berman RF, Zajac CS (1993) Environmental enrichment and the behavioral effects of prenatal exposure to alcohol in rats. Neurotoxicol Teratol 15 : 261 266.
35. Hannigan JH, O'Leary-Moore SK, Berman RF (2007) Postnatal environmental or experiential amelioration of neurobehavioral effects of perinatal alcohol exposure in rats. Neurosci Biobehav Rev 31 : 202 211.
36. Heaton MB, Mitchell JJ, Paiva M (1999) Ethanol-induced alterations in neurotrophin expression in developing cerebellum: relationship to periods of temporal susceptibility. Alcohol Clin Exp Res 23 : 1637 1642.
37. Heaton MB, Mitchell JJ, Paiva M (2000a) Overexpression of NGF ameliorates ethanol neurotoxicity in the developing cerebellum. J Neurobiol 45 : 95 104.
38. Heaton MB, Mitchell JJ, Paiva M, Walker DW (2000b) Ethanol-induced alterations in the expression of neurotrophic factors in the developing rat central nervous system. Brain Res Dev Brain Res 121 : 97 107.
39. Heaton MB, Moore DB, Paiva M, Madorsky I, Mayer J, Shaw G (2003a) The role of neurotrophic factors, apoptosis-related proteins, and endogenous antioxidants in the differential temporal vulnerability of neonatal cerebellum to ethanol. Alcohol Clin Exp Res 27 : 657 669.
40. Heaton MB, Paiva M, Madorsky I, Mayer J, Moore DB (2003b) Effects of ethanol on neurotrophic factors, apoptosis-related proteins, endogenous antioxidants, and reactive oxygen species in neonatal striatum: relationship to periods of vulnerability. Brain Res Dev Brain Res 140 : 237 252.
41. Heaton MB, Paiva M, Madorsky I, Shaw G (2003c) Ethanol effects on neonatal rat cortex: comparative analyses of neurotrophic factors, apoptosis-related proteins, and oxidative processes during vulnerable and resistant periods. Brain Res Dev Brain Res 145 : 249 262.
42. Hicks RR, Zhang L, Atkinson A, Stevenon M, Veneracion M, Seroogy KB (2002) Environmental enrichment attenuates cognitive deficits, but does not alter neurotrophin gene expression in the hippocampus following lateral fluid percussion brain injury. Neuroscience 112 : 631 637.
43. Holson RR, Pearce B (1992) Principles and pitfalls in the analysis of prenatal treatment effects in multiparous species. Neurotoxicol Teratol 14 : 221 228.
44. Ickes BR, Pham TM, Sanders LA, Albeck DS, Mohammed AH, Granholm AC (2000) Long-term environmental enrichment leads to regional increases in neurotrophin levels in rat brain. Exp Neurol 164 : 45 52.
45. Johnson TB, Goodlett CR (2002) Selective and enduring deficits in spatial learning after limited neonatal binge alcohol exposure in male rats. Alcohol Clin Exp Res 26 : 83 93.
46. Jones KL, Smith DW (1973) Recognition of the fetal alcohol syndrome in early infancy. Lancet 2 : 999 1001.
47. Juraska JM (1984) Sex differences in developmental plasticity in the visual cortex and hippocampal dentate gyrus. Prog Brain Res 61 : 205 214.
48. Juraska JM, Fitch JM, Washburne DL (1989) The dendritic morphology of pyramidal neurons in the rat hippocampal CA3 area. II. Effects of gender and the environment. Brain Res 479 : 115 119.
49. Kelly SJ, Day N, Streissguth AP (2000) Effects of prenatal alcohol exposure on social behavior in humans and other species. Neurotoxicol Teratol 22 : 143 149.
50. Keppel G (1991) Design and Analysis: A Researcher's Handbook. 3rd ed. Prentice Hall, Upper Saddle River, NJ.
51. Klintsova AY, Cowell RM, Swain RA, Napper RM, Goodlett CR, Greenough WT (1998) Therapeutic effects of complex motor training on motor performance deficits induced by neonatal binge-like alcohol exposure in rats. I. Behavioral results. Brain Res 800 : 48 61.
52. Klintsova AY, Dickson E, Yoshida R, Greenough WT (2004) Altered expression of BDNF and its high-affinity receptor TrkB in response to complex motor learning and moderate exercise. Brain Res 1028 : 92 104.
53. Lauterborn JC, Isackson PJ, Gall CM (1994) Cellular localization of NGF and NT-3 mRNAs in postnatal rat forebrain. Mol Cell Neurosci 5 : 46 62.
54. Light KE, Ge Y, Belcher SM (2001) Early postnatal ethanol exposure selectively decreases BDNF and truncated TrkB-T2 receptor mRNA expression in the rat cerebellum. Brain Res Mol Brain Res 93 : 46 55.
55. Lu B, Figurov A (1997) Role of neurotrophins in synapse development and plasticity. Rev Neurosci 8 : 1 12.
56. Maier SE, Chen WJ, Miller JA, West JR (1997) Fetal alcohol exposure and temporal vulnerability regional differences in alcohol-induced microencephaly as a function of the timing of binge-like alcohol exposure during rat brain development. Alcohol Clin Exp Res 21 : 1418 1428.
57. Maier SE, Cramer JA, West JR, Sohrabji F (1999a) Alcohol exposure during the first two trimesters equivalent alters granule cell number and neurotrophin expression in the developing rat olfactory bulb. J Neurobiol 41 : 414 423.
58. Maier SE, Miller JA, Blackwell JM, West JR (1999b) Fetal alcohol exposure and temporal vulnerability: regional differences in cell loss as a function of the timing of binge-like alcohol exposure during brain development. Alcohol Clin Exp Res 23 : 726 734.
59. Maier SE, West JR (2001) Regional differences in cell loss associated with binge-like alcohol exposure during the first two trimesters equivalent in the rat. Alcohol 23 : 49 57.
60. Mattson SN, Riley EP, Sowell ER, Jernigan TL, Sobel DF, Jones KL (1996) A decrease in the size of the basal ganglia in children with fetal alcohol syndrome. Alcohol Clin Exp Res 20 : 1088 1093.
61. McAllister AK, Katz LC, Lo DC (1999) Neurotrophins and synaptic plasticity. Annu Rev Neurosci 22 : 295 318.
62. McGoey TN, Reynolds JN, Brien JF (2003) Chronic prenatal ethanol exposure-induced decrease of guinea pig hippocampal CA1 pyramidal cell and cerebellar Purkinje cell density. Can J Physiol Pharmacol 81 : 476 484.
63. Minetti A, Arolfo MP, Virgolini MB, Brioni JD, Fulginiti S (1996) Spatial learning in rats exposed to acute ethanol intoxication on gestational day 8. Pharmacol Biochem Behav 53 : 361 367.
64. Mitchell JJ, Paiva M, Walker DW, Heaton MB (1999) BDNF and NGF afford in vitro neuroprotection against ethanol combined with acute ischemia and chronic hypoglycemia. Dev Neurosci 21 : 68 75.
65. Mohammed AH, Henriksson BG, Soderstrom S, Ebendal T, Olsson T, Seckl JR (1993) Environmental influences on the central nervous system and their implications for the aging rat. Behav Brain Res 57 : 183 191.
66. Moore DB, Madorsky I, Paiva M, Heaton MB (2004) Ethanol exposure alters neurotrophin receptor expression in the rat central nervous system: effects of prenatal exposure. J Neurobiol 60 : 1010 1113.
67. Nathaniel EJ, Nathaniel DR, Mohamed SA, Nahnybida L, Nathaniel L (1986b) Growth patterns of rat body, brain, and cerebellum in fetal alcohol syndrome. Exp Neurol 93 : 610 620.
68. Nathaniel EJ, Nathaniel DR, Mohamed S, Nathaniel L, Kowalzik C, Nahnybida L (1986a) Prenatal ethanol exposure and cerebellar development in rats. Exp Neurol 93 : 601 609.
69. O'Hare ED, Kan E, Yoshii J, Mattson SN, Riley EP, Thompson PM, Toga AW, Sowell ER (2005) Mapping cerebellar vermal morphology and cognitive correlates in prenatal alcohol exposure. Neuroreport 16 : 1285 1290.
70. Pham TM, Ickes B, Albeck D, Soderstrom S, Granholm AC, Mohammed AH (1999) Changes in brain nerve growth factor levels and nerve growth factor receptors in rats exposed to environmental enrichment for one year. Neuroscience 94 : 279 286.
71. Rasmussen C (2005) Executive functioning and working memory in fetal alcohol spectrum disorder. Alcohol Clin Exp Res 29 : 1359 1367.
72. Riley EP, McGee CL (2005) Fetal alcohol spectrum disorders: an overview with emphasis on changes in brain and behavior. Exp Biol Med (Maywood) 230 : 357 365.
73. Riley EP, McGee CL, Sowell ER (2004) Teratogenic effects of alcohol: a decade of brain imaging. Am J Med Genet C Semin Med Genet 127 : 35 41.
74. Sakata-Haga H, Sawada K, Hisano S, Fukui Y (2001) Abnormalities of cerebellar foliation in rats prenatally exposed to ethanol. Acta Neuropathol (Berl) 102 : 36 40.
75. Scharfman HE, Mercurio TC, Goodman JH, Wilson MA, MacLusky NJ (2003) Hippocampal excitability increases during the estrous cycle in the rat: a potential role for brain-derived neurotrophic factor. J Neurosci 23 : 11641 11652.
76. Segal RA (2003) Selectivity in neurotrophin signaling: theme and variations. Annu Rev Neurosci 26 : 299 330.
77. Silva-Gomez AB, Rojas D, Juarez I, Flores G (2003) Decreased dendritic spine density on prefrontal cortical and hippocampal pyramidal neurons in postweaning social isolation rats. Brain Res 983 : 128 136.
78. Snell LD, Bhave SV, Tabakoff B, Hoffman PL (2001) Chronic ethanol exposure delays the 'developmental switch' of the NMDA receptor 2A and 2B subunits in cultured cerebellar granule neurons. J Neurochem 78 : 396 405.
79. Sofroniew MV, Howe CL, Mobley WC (2001) Nerve growth factor signaling, neuroprotection, and neural repair. Annu Rev Neurosci 24 : 1217 1281.
80. Sowell ER, Jernigan TL, Mattson SN, Riley EP, Sobel DF, Jones KL (1996) Abnormal development of the cerebellar vermis in children prenatally exposed to alcohol: size reduction in lobules I-V. Alcohol Clin Exp Res 20 : 31 34.
81. Sowell ER, Mattson SN, Thompson PM, Jernigan TL, Riley EP, Toga AW (2001a) Mapping callosal morphology and cognitive correlates: effects of heavy prenatal alcohol exposure. Neurology 57 : 235 244.
82. Sowell ER, Thompson PM, Mattson SN, Tessner KD, Jernigan TL, Riley EP, Toga AW (2001b) Voxel-based morphometric analyses of the brain in children and adolescents prenatally exposed to alcohol. Neuroreport 12 : 515 523.
83. Sowell ER, Thompson PM, Mattson SN, Tessner KD, Jernigan TL, Riley EP, Toga AW (2002) Regional brain shape abnormalities persist into adolescence after heavy prenatal alcohol exposure. Cereb Cortex 12 : 856 865.
84. Streissguth AP, Aase JM, Clarren SK, Randels SP, LaDue RA, Smith DF (1991) Fetal alcohol syndrome in adolescents and adults. JAMA 265 : 1961 1967.
85. Streissguth AP, Bookstein FL, Barr HM, Sampson PD, O'Malley K, Young JK (2004) Risk factors for adverse life outcomes in fetal alcohol syndrome and fetal alcohol effects. J Dev Behav Pediatr 25 : 228 238.
86. Thomas JD, Goodlett CR, West JR (1998) Alcohol-induced Purkinje cell loss depends on developmental timing of alcohol exposure and correlates with motor performance. Brain Res Dev Brain Res 105 : 159 166.
87. Toga AW, Thompson PM, Sowell ER (2006) Mapping brain maturation. Trends Neurosci 29 : 148 159.
88. Turner CA, Lewis MH (2003) Environmental enrichment: effects on stereotyped behavior and neurotrophin levels. Physiol Behav 80 : 259 266.
89. Vaynman S, Ying Z, Gomez-Pinilla F (2004) Exercise induces BDNF and synapsin I to specific hippocampal subfields. J Neurosci Res 76 : 356 362.
90. Weinberg J (1985) Effects of ethanol and maternal nutritional status on fetal development. Alcohol Clin Exp Res 9 : 49 55.
91. West JR, Goodlett CR, Bonthius DJ, Pierce DR (1989) Manipulating peak blood alcohol concentrations in neonatal rats: review of an animal model for alcohol-related developmental effects. Neurotoxicology 10 : 347 365.
92. Zhu SW, Yee BK, Nyffeler M, Winblad B, Feldon J, Mohammed AH (2006) Influence of differential housing on emotional behaviour and neurotrophin levels in mice. Behav Brain Res 169 : 10 20.
93. Zilles K, Wree A (1985) Cortex: areal and laminar structure, in The Rat Nervous System, Vol. 1 (Paxinos G ed pp 375 415. Academic Press, North Ryde, NSW.