Examination of age-dependent effects of fetal ethanol exposure on behavior, hippocampal cell counts, and doublecortin immunoreactivity in rats

Developmental Neurobiology

Volumn 74, Issue 5, 2014, Pages 498-513

  Elibol Can, Birsen ^a   Dursun, Ilknur ^b   Telkes, Ilknur ^a   Kilic, Ertugrul ^c   Canan, Sinan ^d   Jakubowska Dogru, Ewa ^a  

^a MIDDLE EAST TECHNICAL UNIVERSITY   (Turkey)

^b USKUDAR UNIVERSITY   (Turkey)

^c ISTANBUL MEDIPOL UNIVERSITY   (Turkey)

^d YILDIRIM BEYAZIT UNIVERSITY   (Turkey)

Author keywords

Doublecortin immunoreactivity; Fetal alcohol; Postnatal hippocampal development; Rat; Unbiased stereology

Indexed keywords

ALCOHOL; DOUBLECORTIN; CENTRAL DEPRESSANT AGENT; DOUBLECORTIN PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; NEUROPEPTIDE;

ADULT; AGE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; BEHAVIOR; BRAIN SIZE; CELL COUNT; CONTROLLED STUDY; CORRELATION ANALYSIS; DENTATE GYRUS; ENVIRONMENTAL EXPOSURE; FEMALE; GRANULAR CELL; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; LOCOMOTION; MALE; NERVOUS SYSTEM DEVELOPMENT; NEUROANATOMY; NEWBORN; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; RAT; SECOND TRIMESTER PREGNANCY; SPATIAL LEARNING; STEREOLOGY; TASK PERFORMANCE; WISTAR RAT; YOUNG ADULT; ANIMAL; ANIMAL BEHAVIOR; DRUG EFFECTS; EXPLORATORY BEHAVIOR; FETAL ALCOHOL SYNDROME; GROWTH, DEVELOPMENT AND AGING; MAZE TEST; METABOLISM; NERVE CELL; ORGAN SIZE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PREGNANCY; PRENATAL EXPOSURE; TOXICITY;

ANIMALS; BEHAVIOR, ANIMAL; CELL COUNT; CENTRAL NERVOUS SYSTEM DEPRESSANTS; ETHANOL; EXPLORATORY BEHAVIOR; FEMALE; FETAL ALCOHOL SPECTRUM DISORDERS; HIPPOCAMPUS; MALE; MAZE LEARNING; MICROTUBULE-ASSOCIATED PROTEINS; NEUROGENESIS; NEURONS; NEUROPEPTIDES; ORGAN SIZE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PYRAMIDAL CELLS; RATS, WISTAR;

EID: 84898031459     PISSN: 19328451     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.22143     Document Type: Article

References (92)

1. Abel EL. 1982. In utero alcohol exposure and developmental delay of response inhibition. Alcohol Clin Exp Res 6:369-376.
2. Abel EL, Hannigan JH. 1995. Maternal risk factors in fetal alcohol syndrome: Provocative and permissive influences. Neurotoxicol Teratol 17:445-462.
3. Aberg E, Hofstetter CP, Olson L, Brené S. 2005. Moderate ethanol consumption increases hippocampal cell proliferation and neurogenesis in the adult mouse. Int J Neuropsychopharmacol 8:557-567.
4. Austin MP, Leader LR, Reilly N. 2005. Prenatal stress, the hypothalamic-pituitary-adrenal axis, and fetal and infant neurobehaviour. Early Hum Dev. 81:917-926.
5. Bandeira F, Lent R, Herculano-Houzel S. 2009. Changing numbers of neuronal and non-neuronal cells underlie postnatal brain growth in the rat. Proc Natl Acad Sci USA 106:14108-14113.
6. Bayer SA, Yackel JW, Puri PS. 1982. Neurons in the rat dentate gyrus granular layer substantially increase during juvenile and adult life. Science 216:890-892.
7. Bayer SA, Altman J, Russo RJ, Zhang X. 1993. Timetables of neurogenesisin the human brain based on experimentally determined patterns in the rat. Neurotoxicol 14:83-144.
8. Blackstad TW. 1956. Commissural connections of the hippocampal region in the rat, with special reference to their mode of termination. J Comp Neurol 105:417-538.
9. Boldrini M, Hen R, Underwood MD, Rosoklija GB, Dwork AJ, Mann JJ, Arango V. 2012. Hippocampal angiogenesis and progenitor cell proliferation are increased with antidepressant use in major depression. Biol Psychiatry 72:562-571.
10. Bond NW. 1981. Prenatal alcohol exposure in rodents: A review of its effects on offspring activity and learning ability. Aust J Psych 33:331-344.
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. Bonthius DJ, McKim R, Koele L, Harb H, Karacay B, Mahoney J, Pantazis NJ. 2004. Use of frozen sections to determine neuronal number in the murine hippocampus and neocortex using the optical disector and optical fractionator. Brain Res Brain Res Protoc 14:45-57.
14. Brown JP, Couillard-Després S, Cooper-Kuhn CM, Winkler J, Aigner L, Kuhn HG. 2003. Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467:1-10.
15. Carneiro LM, Diógenes JP, Vasconcelos SM, Aragão GF, Noronha EC, Gomes PB, Viana GS. 2005. Behavioral and neurochemical effects on rat offspring after prenatal exposure to ethanol. Neurotoxicol Teratol 27:585-592.
16. Chang GQ, Karatayev O, Liang SC, Barson JR, Leibowitz SF. 2012. Prenatal ethanol exposure stimulates neurogenesis in hypothalamic and limbic peptide systems: Possible mechanism for offspring ethanol overconsumption. Neuroscience 222:417-428.
17. Darnaudéry M, Maccari S. 2008. Epigenetic programming of the stress response in male and female rats by prenatal restraint stress. Brain Res Rev 57:571-585.
18. Denenberg VH. 1969. Open-field behavior in the rat: What does it mean? Ann N Y Acad Sci 159:852-859.
19. Dobbing J, Sands J. 1979. Comparative aspects of the brain growth spurt. Early Hum Dev 3:79-83.
20. Driscoll CD, Streissguth AP, Riley EP. 1990. Prenatal alcohol exposure: Comparability of effects in humans and animal models. Neurotoxicol Teratol 12:231-237.
21. Dursun I, Jakubowska-Doǧru E, Uzbay T. 2006. Effects of prenatal exposure to alcohol on activity, anxiety, motor coordination, and memory in young adult Wistar rats. Pharmacol Biochem Behav 85:345-355.
22. Dursun I, Jakubowska-Doǧru E, van der List D, Liets LC, Coombs JL, Berman RF. 2011. Effects of early postnatal exposure to ethanol on retinal ganglion cell morphology and numbers of neurons in the dorsolateral geniculate in mice. Alcohol Clin Exp Res 35:2063-2074.
23. Dursun I, Jakubowska-Doǧru E, Elibol-Can B, van der List D, Chapman B, Qi L, Berman RF. 2013. Effects of early postnatal alcohol exposure on the developing retinogeniculate projections in C57BL/6 mice. Alcohol 47:173-179.
24. Fitting S, Booze RM, Hasselrot U, Mactutus CF. 2010. Dose-dependent long-term effects of Tat in the rat hippocampal formation: A design-based stereological study. Hippocampus 20:469-480.
25. Gabriel KI, Yu CL, Osborn JA, Weinberg J. 2006. Prenatal ethanol exposure alters sensitivity to the effects of corticotropin-releasing factor (CRF) on behavior in the elevated plus-maze. Psychoneuroendocrinology 31:1046-1056.
26. Gil-Mohapel J, Boehme F, Kainer L, Christie BR. 2010. Hippocampal cell loss and neurogenesis after fetal alcohol exposure: Insights from different rodent models. Brain Res Rev 64:283-303.
27. Gianoulakis C. 1990. Rats exposed prenatally to alcohol exhibit impairment in spatial navigation test. Behav Brain Res 36:217-228.
28. Girard TA, Xing HC, Ward GR, Wainwright PE. 2000. Early postnatal ethanol exposure has long-term effects on the performance of male rats in a delayed matching-to-place task in the Morris water maze. Alcohol Clin Exp Res 24:300-306.
29. Gokcimen A, Ragbetli MC, Bas O, Tunc AT, Aslan H, Yazici AC, Kaplan S. 2007. Effect of prenatal exposure to an anti-inflammatory drug on neuron number in cornu ammonis and dentate gyrus of the rat hippocampus: A stereological study. Brain Res 1127:185-192.
30. Gonzàles-Burgos M, Alejandre-Gómez ME, Olvera-Cortés MI, Pérez-Vega S, Evans S, Feria-Velasco A. 2006. Prenatal-through-postnatal exposure to moderate levels of ethanol leads to damage on the hippocampal CA1 field of juvenile rats: A stereology and golgi study. Neurosci Res 56:400-408.
31. Goodlett CR, Marcussen BL, West JR. 1990. A single day of alcohol exposure during the brain growth spurt induces brain weight restriction and cerebellar Purkinje cell loss. Alcohol 7:107-114.
32. Goodlett CR, Pearlman AD, Lundahl KR. 1997. Binge-like alcohol exposure of neonatal rats via intragastric intubation induces both Purkinje cell loss and cortical astrogliosis. Alcohol Clin Exp Res 21:1010-1017.
33. Gundersen HJ, Jensen EB. 1987. The efficiency of systematic sampling in stereology and its prediction. J Microsc 147:229-263.
34. Gundersen HJG, Jensen EBV, Kieu K, Nielsen J. 1999. The efficiency of systematic sampling in stereology-reconsidered. J Microsc 193:199-211.
35. Hall CS, Ballachey EL. 1932. A study of the rat's behavior in a field: A contribution to method in comparative psychology. Univ Calif Publ Psychol 6:1-12.
36. Inta D, Alfonso J, von Engelhardt J, Kreuzberg MM, Meyer AH, van Hooft JA, Monyer H. 2008. Neurogenesis and widespread forebrain migration of distinct GABAergic neurons from the postnatal subventricular zone. Proc Natl Acad Sci USA 105:20994-20999.
37. Jones KL, Smith DW, Ulleland CN, Streissguth AP. 1973. Pattern of malformation in offspring of chronic alcoholic mothers. Lancet 1:1267-1271.
38. Kaplan MS, Bell DH. 1983. Neuronal proliferation in the 9-month-old rodent-radioautographic study of granule cells in the hippocampus. Exp Brain Res 52:1-5.
39. Kapoor A, Dunn E, Kostaki A, Andrews MH, Matthews SG. 2006, Fetal programming of hypothalamo-pituitary-adrenal function: Prenatal stress and glucocorticoids. J Physiol 1;572:31-44.
40. Kayir H, Uzbay IT. 2006. Nicotine antagonizes caffeine- but not pentylenetetrazole-induced anxiogenic effect in mice. Psychopharmacology 184: 464-469.
41. Kelly SJ, Pierce DR, West JR. 1987. Microencephaly and hyperactivity in adult rats can be induced by neonatal exposure to high blood alcohol concentrations. Exp Neurol 96:580-593.
42. Kesaniemi YA, Sippel HW. 1975. Placental and foetal metabolism of acetaldehyde in rat: I. Contents of ethanol and acetaldehyde in placenta and foetus of the pregnant rat during ethanol oxidation. Acta Pharm Toxicol 37:43-48.
43. Kilic E, Elali A, Kilic L, Guo Z, Ugur M, Uslu U, Bassetti CL, et al. 2010. Role of Nogo-A in neuronal survival in the reperfused ischemic brain. J Cereb Blood Flow Metab 30:969-984.
44. Koehl M, Lemaire V, Le Moal M, Abrous DN. 2009. Age-dependent effect of prenatal stress on hippocampal cell proliferation in female rats. Eur J Neurosci 29:635-640.
45. Lemaire V, Koehl M, Le Moal M, Abrous DN. 2000. Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci USA 97:11032-11037.
46. Lister RG. 1987. The use of a plus-maze to measure anxiety inthe mouse. Psychopharmacology 92:180-185.
47. Livy DJ, Miller EK, Maier SE, West JR. 2003. Fetal alcohol exposure and temporal vulnerability: Effects of binge-like alcohol exposure on the developing rat hippocampus. Neurotoxicol Teratol 25:447-458.
48. Lucassen PJ, Bosch OJ, Jousma E, Krömer SA, Andrew R, Seckl JR, Neumann ID. 2009. Prenatal stress reduces postnatal neurogenesis in rats selectively bred for high, but not low, anxiety: Possible key role of placental 11beta-hydroxysteroid dehydrogenase type 2. Eur J Neurosci 29:97-103.
49. Lyck L, Krøigård T, Finsen B. 2007. Unbiased cell quantification reveals a continued increase in the number of neocortical neurons during early post-natal development in mice. Eur J Neurosci 26:1749-1764.
50. 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.
51. Marino MD, Cronise K, Lugo JN, Kelly SJ. 2002. Ultrasonic vocalizations and maternal- infant interactions in a rat model of fetal alcohol syndrome. Dev Psychobiol 41:341-351.
52. Meyer LS, Riley EP. 1986. Behavioral teratology of alcohol. In: Riley EP, Vorhees CV, editors. Handbook of Behavioral Teratology. New York: Plenum, pp 101-140.
53. Mihalick SM, Crandall JE, Langlois JC, Krienke JD, Dube WM. 2001. Prenatal ethanol exposure generalized learning impairment and medial prefrontal cortical deficits in rats. Neurotoxicol Teratol 23:453-462.
54. Miki T, Harris SJ, Wilce PA, Takeuchi Y, Bedi KS. 2003. Effects of alcohol exposure during early life on neuron numbers in the rat hippocampus. I. Hilus neurons and granule cells. Hippocampus 13:388-398.
55. Miller MW. 1995. Generation of neurons in the rat dentate gyrus and hippocampus: Effects of prenatal and postnatal treatment with ethanol. Alcohol Clin Exp Res 19:1500-1509.
56. Mirescu C, Gould E. 2006. Stress and adult neurogenesis. Hippocampus 16:233-238.
57. Morris R. 1984. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 11:47-60.
58. Morterá P, Herculano-Houzel S. 2012. Age-related neuronal loss in the rat brain starts at the end of adolescence. Front Neuroanat 6:45.
59. Nagahara AH, Handa RJ. 1997. Fetal alcohol exposure produces delay-dependent memory deficits in juvenile and adult rats. Alcohol Clin Exp Res 21:710-715.
60. Ogilvie KM, Rivier C. 1997. Prenatal alcohol exposure results in hyperactivity of the hypothalamic-pituitary-adrenal axis of the offspring: Modulation by fostering at birth and postnatal handling. Alcohol Clin Exp Res 21:424-429.
61. Olney JW, Wozniak DF, Jevtovic-Todorovic V, Farber NB, Bittigau P, Ikonomidou C. 2002. Glutamate and GABA receptor dysfunction in the fetal alcohol syndrome. Neurotox Res 4:315-325.
62. Osborn JA, Kim CK, Steiger J, Weinberg J. 1998. Prenatal ethanol exposure differentially alters behavior in males and females on the elevated plus maze. Alcohol Clin Exp Res 22:685-696.
63. Paxinos G, Watson C. 2007. The rat brain in stereotaxic coordinates. USA: Academic Press, Figures 45-90.
64. Paxinos G, Halliday G, Watson C, Yuri K, HongQin W. 2007. Atlas of the developing mouse brain. USA: Academic Press, Figures 63-78.
65. Pellow S, Chopin P, File SE, Briley M. 1985. Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods 14:149-167.
66. Prut L, Belzung C. 2003. The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: A review. Eur J Pharmacol 463:3-33.
67. Randall S, Hannigan JH. 1999. In utero alcohol and postnatal methylphenidate: Locomotion and dopamine receptors. Neurotoxicol Teratol 21:587-593.
68. Redila VA, Olson AK, Swann SE, Mohades G, Webber AJ, Weinberg J, Christie BR. 2006. Hippocampal cell proliferation is reduced following prenatal ethanol exposure but can be rescued with voluntary exercise. Hippocampus 16:305-311.
69. Rietze R, Poulin P, Weiss S. 2000. Mitotically active cells that generate neurons and astrocytes are present in multiple regions of the adult mouse hippocampus. J Comp Neurol 424:397-408.
70. Sag C, Yokusoglu M, Cincik M, Ozkan M, Kayir H, Uzun M, Baykal B, et al. 2006. The prevention of myocardial ultrastructural changes by perindopril, atenonol, and amlodipine in chronic alcohol administered rats. Pharmacol Res 53:142-148.
71. Schmitz C, Rhodes ME, Bludau M, Kaplan S, Ong P, Ueffing I, Vehoff J, et al. 2002. Depression: Reduced number of granule cells in the hippocampus of female, but not male, rats due to prenatal restraint stress. Mol Psychiatry 7:810-813.
72. Singh AK, Gupta S, Jiang Y, Younus M, Ramzan M. 2009. In vitro neurogenesis from neural progenitor cells isolated from the hippocampus region of the brain of adult rats exposed to ethanol during early development through their alcohol-drinking mothers. Alcohol 44:185-198.
73. Sliwowska JH, Barker JM, Barha CK, Lan N, Weinberg J, Galea LA. 2010. Stress-induced suppression of hippocampal neurogenesis in adult male rats is altered by prenatal ethanol exposure. Stress 13:301-313.
74. Smith AM, Pappalardo D, Chen WJ. 2008. Estimation of neuronal numbers in rat hippocampus following neonatal amphetamine exposure: A stereology study. Neurotoxicol Teratol 30:495-502.
75. Smith AM, Wellmann KA, Lundblad TM, Carter ML, Barron S, Dwoskin LP. 2012. Lobeline attenuates neonatal ethanol-mediated changes in hyperactivity and dopamine transporter function in the prefrontal cortex in rats. Neuroscience 206:245-254.
76. Thomas JD, Warren KR, Hewitt BG, 2010. Fetal alcohol spectrum disorders: From research to policy. Alcohol Res Health 33:118-126.
77. Tran DT, Kelly SJ. 2003. Critical periods for ethanol-induced cell loss in the hippocampal formation. Neurotoxicol Teratol 25:519-528.
78. Tran TD, Cronise K, Marino MD, Jenkins WJ, Kelly SJ. 2000. Critical periods for the effects of alcohol exposure on brain weight, body weight, activity and investigation. Behav Brain Res 116:99-110.
79. Ulug S, Riley EP. 1983. The effect of methylphenidate on overactivity in rats prenatally exposed to alcohol. Neurobehav Toxicol Teratol 5:35-39.
80. Uzbay IT, Celik T, Aydin A, Kayir H, Tokgöz S, Bilgi C. 2004. Effects of chronic ethanol administration and ethanol withdrawal on cyclic guanosine 3′, 5′-monophosphate (cGMP) levels in the rat brain. Drug Alcohol Depend 74: 55-59.
81. Vázquez-Roque RA, Ramos B, Tecuatl C, Juárez I, Adame A, de la Cruz F, Zamudio S, et al. 2012. Chronic administration of the neurotrophic agent cerebrolysin ameliorates the behavioral and morphological changes induced by neonatal ventral hippocampus lesion in a rat model of schizophrenia. J Neurosci Res 90:288-306.
82. Veena J, Rao BS, Srikumar BN. 2011. Regulation of adult neurogenesis in the hippocampus by stress, acetylcholine and dopamine. J Nat Sci Biol Med 2:26-37.
83. Vorhees CV, Fernandez K. 1986. Effects of short-term prenatal alcohol exposure on maze, activity, and olfactory orientation performance in rats. Neurobehav Toxicol Teratol 8:23-28.
84. Warren KR, Hewitt BG, Thomas JD, 2011. Fetal alcohol spectrum disorders: Research challenges and opportunities. Alcohol Res Health 34:4-14.
85. Weinberg J, Taylor AN, Gianoulakis C. 1996. Fetal ethanol exposure: Hypothalamic-pituitary-adrenal and beta-endorphin responses to repeated stress. Alcohol Clin Exp Res 20:122-131.
86. West MJ, Slomankia L, Gundersen HJ. 1991. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482-497.
87. Westergren S, Rydenhag B, Bassen M, Archer T, Conradi NG. 1996. Effects of prenatal alcohol exposure on activity and learning in Sprague-Dawley rats. Pharmacol Biochem Behav 55:515-520.
88. Wigal T, Amsel A. 1990. Behavioral and neuroanatomical effects of prenatal, postnatal, or combined exposure to ethanol in weanling rats. Behav Neurosci 104:116-126.
89. Wozniak DF, Hartman RE, Boyle MP, Vogt SK, Brooks AR, Tenkova T, Young C, et al. 2004. Apoptotic neurodegeneration induced by ethanol in neonatal mice is associated with profound learning/memory deficits in juveniles followed by progressive functional recovery in adults. Neurobiol Dis 17:403-414.
90. Yamamura T, Barker JM, Balthazart J, Ball GF. 2011. Androgens and estrogens synergistically regulate the expression of doublecortin and enhance neuronal recruitment in the song system of adult female canaries. J Neurosci 31:9649-9657.
91. Zimmerberg B; Sukel HL; Stekler JD. 1991. Spatial learning of adult rats with fetal alcohol exposure: Deficits are sex-dependent. Behav Brain Res 42:49-56.
92. Zimmerberg B, Drucker PC, Weider JM. 1995. Differential behavioral effects of the neuroactive steroid allopregnanolone on neonatal rats prenatally exposed to alcohol. Pharmacol Biochem Behav 51:463-468.