Prenatal ethanol exposure has sex-specific effects on hippocampal long-term potentiation
Article first published online: 4 OCT 2013
Copyright © 2013 Wiley Periodicals, Inc.
Volume 24, Issue 1, pages 54–64, January 2014
How to Cite
Sickmann, H.M., Patten, A.R., Morch, K., Sawchuk, S., Zhang, C., Parton, R., Szlavik, L. and Christie, B.R. (2014), Prenatal ethanol exposure has sex-specific effects on hippocampal long-term potentiation. Hippocampus, 24: 54–64. doi: 10.1002/hipo.22203
- Issue published online: 10 DEC 2013
- Article first published online: 4 OCT 2013
- Accepted manuscript online: 31 AUG 2013 05:44AM EST
- Manuscript Accepted: 22 AUG 2013
- CIHR. Grant Number: 36331
- NSERC. Grant Number: 34872
- Michael Smith Foundation. Grant Number: 33839
- The Alfred Benzon Foundation
- 1994. Differential changes in cell morphology, macromolecular composition and membrane protein profiles of neurons and astrocytes in chronic ethanol treated rats. Mol Cell Biochem 130:29–40. , , .
- 2005. Reversal of ethanol toxicity in embryonic neurons with growth factors and estrogen. Brain Res Bull 67:459–465. , , , .
- 2005. NMDA receptor subunit composition controls synaptic plasticity by regulating binding to CaMKII. Neuron 48:289–301. , .
- 1987. Deficits on a spatial navigation task following prenatal exposure to ethanol. Neurotoxicol Teratol 9:253–258. , , .
- 2013 Moderate prenatal alcohol exposure reduces plasticity and alters NMDA receptor subunit somposition in the dentate gyrus. J Neurosci 33:1062–1067. , , , , , .
- 2011. The role of oxidative stress in fetal alcohol spectrum disorders. Brain Res Rev 67:209–225. , , .
- 2012. Anxiety- and depression-like behaviors are accompanied by an increase in oxidative stress in a rat model of fetal alcohol spectrum disorders: Protective effects of voluntary physical exercise. Neuropharmacology 62:1607–1618. , , , , , .
- 1989. A novel NMDA antagonist, MK-801, impairs performance in a hippocampal-dependent spatial learning task. Pharmacol Biochem Behav 34:13–16. .
- 2005. Voluntary exercise rescues deficits in spatial memory and long-term potentiation in prenatal ethanol-exposed male rats. Eur J Neurosci 21:1719–1726. , , , , , , .
- 1997. Estrogen facilitates induction of long term potentiation in the hippocampus of awake rats. Brain Res 778:430–438. , .
- 2005. Ovariectomy-induced disruption of long-term synaptic depression in the hippocampal CA1 region in vivo is attenuated with chronic estrogen replacement. Neurobiol Learn Mem 83:13–21. , .
- 2008. NMDA receptor antagonists reveal age-dependent differences in the properties of visual cortical plasticity. J Neurophysiol 100:1936–1948. , , , , , , .
- 2004. Effects of voluntary exercise on synaptic plasticity and gene expression in the dentate gyrus of adult male Sprague-Dawley rats in vivo. Neuroscience 124:71–79. , , , , , .
- 2005. Alcohol is a potent stimulant of immature neuronal networks: Implications for fetal alcohol spectrum disorder. J Neurochem 94:1500–1511. , , .
- 2010. Hippocampal cell loss and neurogenesis after fetal alcohol exposure: Insights from different rodent models. Brain Res Rev 64:283–303. , , , .
- 2011. Altered adult hippocampal neuronal maturation in a rat model of fetal alcohol syndrome. Brain Res 1384:29–41. , , , , , , , .
- 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. , .
- 2008. Estrogen synthesis in the brain—Role in synaptic plasticity and memory. Mol Cell Endocrinol 290:31–43. , , , , , , , , .
- 2003. Prenatal ethanol exposure modifies [3H]MK-801 binding to NMDA receptors: Spermidine and ifenprodil. Alcohol Clin Exp Res 27:1993–2001. , , .
- 2004. Chronic prenatal ethanol exposure alters hippocampal GABA(A) receptors and impairs spatial learning in the guinea pig. Behav Brain Res 150:117–125. , , , .
- 1980. Endocrine effects of meternal alcoholization: Plasma and brain testosterone, dihydrotestosterone, estradiol, and corticosterone. Alcohol Clin Exp Res 4:57–61. , , .
- 1988. NMDA application potentiates synaptic transmission in the hippocampus. Nature 334:250–252. , , .
- 1988. Impaired spatial navigation in adult female but not adult male rats exposed to alcohol during the brain growth spurt. Behav Brain Res 27:247–257. , , , .
- 2004. Hippocampal synapses depend on hippocampal estrogen synthesis. J Neurosci 24:5913–5921. , , , , , , , , , , .
- 1991. Maternal alcohol exposure before and during pregnancy: Effect on development of neurons and glial cells in culture. Alcohol Alcohol 26:169–176. , , .
- 2004. Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science 304:1021–1024. , , , , , , , .
- 2006. Ethanol exposure during development reduces resident aggression and testosterone in rats. Physiol Behav 87:330–337. , , , , .
- 1994. Sex differences in hippocampal long-term potentiation (LTP) and Pavlovian fear conditioning in rats: Positive correlation between LTP and contextual learning. Brain Res 661:25–34. , , .
- 2010. Sex-specific proteome differences in the anterior cingulate cortex of schizophrenia. J Psychiatr Res 44:989–991. , , , , , , .
- 2009. Proteomics approach in the study of the pathophysiology of alcohol-related brain damage. Alcohol Alcohol 44:171–176. .
- 2009. Prevalence and epidemiologic characteristics of FASD from various research methods with an emphasis on recent in-school studies. Dev Disabil Res Rev 15:176–192. , , , , , , .
- 1996. Spatial learning in rats exposed to acute ethanol intoxication on gestational day 8. Pharmacol Biochem Behav 53:361–367. , , , , .
- 2004. Sexual differentiation of the vertebrate nervous system. Nat Neurosci 7:1034–1039. , , .
- 2002. Effect of prenatal and postnatal ethanol exposure on the developmental profile of mRNAs encoding NMDA receptor subunits in rat hippocampus. J Neurochem 80:850–860. , .
- 2004. NMDA receptor subunit expression after combined prenatal and postnatal exposure to ethanol. Alcohol Clin Exp Res 28:105–112. , , , .
- 1979. Fine structural localization of glutamine synthetase in astrocytes of rat brain. Brain Res 161:303–310. , .
- 2012. Modulation of synaptic plasticity in the hippocampus by hippocampus-derived estrogen and androgen. J Steroid Biochem Mol Biol 131:37–51. , , , , , , , , , .
- 2013. Omega-3 supplementation can restore glutathione levels and prevent oxidative damage caused by prenatal ethanol exposure. J Nutr Biochem 24:760–769. , , .
- 1995. Spatial learning ability of rats following acute exposure to alcohol during early postnatal life. Physiol Behav 58:1013–1020. , , .
- 2001. Developmental sex differences in glutamic acid decarboxylase (GAD(65)) and the housekeeping gene, GAPDH. Brain Res 922:201–208. , , .
- 2003. Para/autocrine regulation of estrogen receptors in hippocampal neurons. Hippocampus 13:226–234. , , , .
- 1989. The effects of prenatal alcohol exposure on radial arm maze performance in adult rats. Physiol Behav 46:45–48. , , .
- 2002. Impaired acquisition in the water maze and hippocampal long-term potentiation after chronic prenatal ethanol exposure in the guinea-pig. Eur J Neurosci 16:1593–1598. , , , , .
- 2008. Choline supplementation attenuates learning deficits associated with neonatal alcohol exposure in the rat: Effects of varying the timing of choline administration. Brain Res 1237:91–100. , , .
- 2010. Hippocampal N-methyl-d-aspartate receptor subunit expression profiles in a mouse model of prenatal alcohol exposure. Alcohol Clin Exp Res 34:342–353. , , , .
- 2000. Sex differences in GABA turnover and glutamic acid decarboxylase (GAD(65) and GAD(67)) mRNA in the rat hypothalamus. Brain Res 878:11–19. , , , , .
- 2009. Estradiol and the relationship between dendritic spines, NR2B containing NMDA receptors, and the magnitude of long-term potentiation at hippocampal CA3-CA1 synapses. Psychoneuroendocrinology 34 (Suppl 1):S130–S142. , , .
- 2003. Fetal alcohol spectrum disorder. JAMA 290:2996–2999. , , .
- 2008. Estrous cycle regulates activation of hippocampal Akt, LIM kinase, and neurotrophin receptors in C57BL/6 mice. Neuroscience 155:1106–1119. , , , .
- 1997. Prenatal exposure to moderate levels of ethanol can have long-lasting effects on hippocampal synaptic plasticity in adult offspring. Hippocampus 7:232–238. , , .
- 1988. Prenatal exposure to ethanol decreases physiological plasticity in the hippocampus of the adult rat. Alcohol 5:121–124. , , , .
- 1980. Gonadal steroids: Effects on excitability of hippocampal pyramidal cells. Science 209:1017–1018. , , , .
- 2012. Prenatal ethanol exposure enhances NMDAR-dependent long-term potentiation in the adolescent female dentate gyrus. Hippocampus 22:69–81. , .
- 1998. Spatial but not object memory impairments in children with fetal alcohol syndrome. Am J Ment Retard 103:12–18. , .
- 2012. Aromatase inhibition abolishes LTP generation in female but not in male mice. J Neurosci 32:8116–8126. , , , , , , , , , , , , .
- 2011. Knockout of GAD65 has major impact on synaptic GABA synthesized from astrocyte-derived glutamine. J Cereb Blood Flow Metab 31:494–503. , , , , , , , .
- 2001. Steroidogenic factor-1 expression in marmoset and rat hippocampus: Co-localization with StAR and aromatase. J Neurochem 76:1879–1886. , , .
- 1985. Effects of ethanol and maternal nutritional status on fetal development. Alcohol Clin Exp Res 9:49–55. .
- 2007. The control of sexual differentiation of the reproductive system and brain. Reproduction 133:331–359. , .
- 1991. Spatial learning of adult rats with fetal alcohol exposure: Deficits are sex-dependent. Behav Brain Res 42:49–56. , , .