Dietary choline during periadolescence attenuates cognitive damage caused by neonatal maternal separation in male rats

References

• Meck WH, Williams CL. Metabolic imprinting of choline by its availability during gestation: implications for memory and attentional processing across the lifespan. Neurosci Biobehav Rev 2003;27(4):385–99. doi: 10.1016/S0149-7634(03)00069-1
   PubMed Web of Science ®Google Scholar
• Guan J, MacGibbon A, Zhang R, Elliffe DM, Moon S, Liu DX. Supplementation of complex milk lipid concentrate (CMLc) improved the memory of aged rats. Nutr Neurosci 2015;18(1):22–9. doi: 10.1179/1476830513Y.0000000096
   PubMed Web of Science ®Google Scholar
• Corriveau J, Glenn M. Postnatal choline levels mediate cognitive deficits in a rat model of schizophrenia. Pharmacol Biochem Behav 2012;103:60–8. doi: 10.1016/j.pbb.2012.08.002
   PubMed Web of Science ®Google Scholar
• Langley EA, Krykbaeva M, Blusztajn JK, Mellott TJ. High maternal choline consumption during pregnancy and nursing alleviates deficits in social interaction and improves anxiety-like behaviors in the BTBR T+ Itpr3tf/J mouse model of autism. Behav Brain Res 2015;278:210–20. doi: 10.1016/j.bbr.2014.09.043
   PubMed Web of Science ®Google Scholar
• Schulz KM, Pearson JN, Gasparrini ME, Brooks KF, Drake-Frazier C, Zajkowski ME, et al. Dietary choline supplementation to dams during pregnancy and lactation mitigates the effects of in utero stress exposure on adult anxiety-related behaviors. Behav Brain Res 2014;268:104–10. doi: 10.1016/j.bbr.2014.03.031
   PubMed Web of Science ®Google Scholar
• Wu WL, Adams CE, Stevens KE, Chow KH, Freedman R, Patterson PH. The interaction between maternal immune activation and alpha 7 nicotinic acetylcholine receptor in regulating behaviors in the offspring. Brain Behav Immun 2015;46:192–202. doi: 10.1016/j.bbi.2015.02.005
   PubMed Web of Science ®Google Scholar
• Wurtman RJ. Non-nutritional uses of nutrients. Eur J Pharmacol 2011;668:S10–5. doi: 10.1016/j.ejphar.2011.07.005
   PubMed Web of Science ®Google Scholar
• Hirsch MJ, Growdon JH, Wurtman RJ. Relations between dietary choline or lecithin intake, serum choline levels, and various metabolic indices. Metabolism 1978;27(8):953–60. doi: 10.1016/0026-0495(78)90139-7
   PubMed Web of Science ®Google Scholar
• Zeisel SH, Epstein MF, Wurtman RJ. Elevated choline concentration in neonatal plasma. Life Sci 1980;26(21):1827–31. doi: 10.1016/0024-3205(80)90585-8
   PubMed Web of Science ®Google Scholar
• Cohen EL, Wurtman RJ. Brain acetylcholine: control by dietary choline. Science 1976;191(4227):561–2. doi: 10.1126/science.1251187
   PubMed Web of Science ®Google Scholar
• Hirsch MJ, Wurtman RJ. Increase in striatal choline acetyltransferase activity after choline administration. Brain Res 1979;165:358–61. doi: 10.1016/0006-8993(79)90570-5
   PubMed Web of Science ®Google Scholar
• Wecker L, Cawley G, Rothermel S. Acute choline supplementation in vivo enhances acetylcholine synthesis in vitro when neurotransmitter release is increased by potassium. J Neurochem 1989;52(2):568–75. doi: 10.1111/j.1471-4159.1989.tb09157.x
   PubMed Web of Science ®Google Scholar
• Wecker L. The synthesis and release of acetylcholine by depolarized hippocampal slices is increased by increased choline available in vitro prior to stimulation. J Neurochem 1991;57(4):111927. doi: 10.1111/j.1471-4159.1991.tb08269.x
   Web of Science ®Google Scholar
• Rada PV, Mark GP, Hoebel BG. Effects of supplemental choline on extracellular acetylcholine in the nucleus accumbens during normal behavior and pharmacological acetylcholine depletion. Synapse 1994;16:211–8. doi: 10.1002/syn.890160306
   PubMed Web of Science ®Google Scholar
• Buyukuysal RL, Ulus IH, Aydin S, Kiran BK. 3, 4-Diaminopyridine and choline increase in vivo acetylcholine release in rat striatum. Eur J Pharmacol 1995;281(2):179–85. doi: 10.1016/0014-2999(95)00241-C
   PubMed Web of Science ®Google Scholar
• Garner SC, Mar MH, Zeisel SH. Choline distribution and metabolism in pregnant rats and fetuses are influenced by the choline content of the maternal diet. J Nutr 1995;125(11):2851–8.
   PubMed Web of Science ®Google Scholar
• Köppen A, Klein J, Erb C, Löffelholz K. Acetylcholine release and choline availability in rat hippocampus: effects of exogenous choline and nicotinamide. J Pharmacol Exp Ther 1997;282(3):1139–45.
   PubMed Web of Science ®Google Scholar
• Lupien SJ, McEwen BS, Gunnar MR, Heim C. Effects of stress throughout the lifespan on the brain, behavior and cognition. Nat Rev Neurosci 2009;10(6):434–45. doi: 10.1038/nrn2639
   PubMed Web of Science ®Google Scholar
• Brown RE. An introduction to neuroendocrinology. Cambridge: Cambridge University Press; 1994. p. 19–27.
   Google Scholar
• De Kloet ER, Vreugdenhil E, Oitzl MS, Joels M. Brain corticosteroid receptor balance in health and disease 1. Endocr Rev 1998;19(3):269–301.
   PubMed Web of Science ®Google Scholar
• De Kloet ER. Stress in the brain. Eur J Pharmacol 2000;405(1):187–98. doi: 10.1016/S0014-2999(00)00552-5
   PubMed Web of Science ®Google Scholar
• McEwen BS, De Kloet ER, Rostene W. Adrenal steroid receptors and actions in the nervous system. Physiol Rev 1986;66(4):1121–88.
   PubMed Web of Science ®Google Scholar
• Meaney MJ, Diorio J, Francis D, Widdowson J, LaPlante P, Caldji C, et al. Early environmental regulation of forebrain glucocorticoid receptor gene expression: implications for adrenocortical responses to stress. Dev Neurosci 1996;18(1–2):61–72. doi: 10.1159/000111396
   Web of Science ®Google Scholar
• Aisa B, Tordera R, Lasheras B, Del Rio J, Ramírez MJ. Cognitive impairment associated to HPA axis hyperactivity after maternal separation in rats. Psychoneuroendocrinology 2007;32:256–66. doi: 10.1016/j.psyneuen.2006.12.013
   PubMed Web of Science ®Google Scholar
• Gunnar MR, Cheatham CL. Brain and behavior interface: stress and the developing brain. Infant Ment Health J 2003;24(3):195–211. doi: 10.1002/imhj.10052
   Web of Science ®Google Scholar
• Kuhn CM, Pauk J, Schanberg SM. Endocrine responses to mother-infant separation in developing rats. Dev Psychobiol 1990;23(5):395–410. doi: 10.1002/dev.420230503
   PubMed Web of Science ®Google Scholar
• Eichenbaum H. The hippocampus and declarative memory: cognitive mechanisms and neural codes. Behav Brain Res 2001;127(1):199–207. doi: 10.1016/S0166-4328(01)00365-5
   PubMed Web of Science ®Google Scholar
• Hollup SA, Kjelstrup KG, Hoff J, Moser MB, Moser EI. Impaired recognition of the goal location during spatial navigation in rats with hippocampal lesions. J Neurosci 2001;21(12):4505–13.
   PubMed Web of Science ®Google Scholar
• Jarrard LE. On the role of the hippocampus in learning and memory in the rat. Behav Neural Biol 1993;60(1):9–26. doi: 10.1016/0163-1047(93)90664-4
   PubMedGoogle Scholar
• Papp G, Witter MP, Treves A. The CA3 network as a memory store for spatial representations. Learn Mem 2007;14(11):732–44. doi: 10.1101/lm.687407
   PubMed Web of Science ®Google Scholar
• McEwen BS. Stress and hippocampal plasticity. Annu Rev Neurosci 1999;22(1):105–22. doi: 10.1146/annurev.neuro.22.1.105
   PubMed Web of Science ®Google Scholar
• Sapolsky RM, Krey LC, McEwen BS. Prolonged glucocorticoid exposure reduces hippocampal neuron number: implications for aging. J Neurosci 1985;5(5):1222–7.
   PubMed Web of Science ®Google Scholar
• Sousa VC, Vital J, Costenla AR, Batalha VL, Sebastião AM, Ribeiro JA, et al. Maternal separation impairs long term-potentiation in CA1-CA3 synapses and hippocampal-dependent memory in old rats. Neurobiol Aging 2014;35(7):1680–5. doi: 10.1016/j.neurobiolaging.2014.01.024
   PubMed Web of Science ®Google Scholar
• Fadda F, Cocco S, Stancampiano R. Hippocampal acetylcholine release correlates with spatial learning performance in freely moving rats. Neuroreport 2000;11(10):2265–9. doi: 10.1097/00001756-200007140-00040
   PubMed Web of Science ®Google Scholar
• Moreno HC, de Brugada I, Carias D, Gallo M. Long-lasting effects of prenatal dietary choline availability on object recognition memory ability in adult rats. Nutr Neurosci 2013;16(6):269–74. doi: 10.1179/1476830513Y.0000000055
   PubMed Web of Science ®Google Scholar
• Markham JA, Taylor AR, Taylor SB, Bell DB, Koenig JI. Characterization of the cognitive impairments induced by prenatal exposure to stress in the rat. Front Behav Neurosci 2010;4–173. doi: 10.3389/fnbeh.2010.00173
   PubMed Web of Science ®Google Scholar
• Benetti F, Mello PB, Bonini JS, Monteiro S, Cammarota M, Izquierdo I. Early postnatal maternal deprivation in rats induces memory deficits in adult life that can be reversed by donepezil and galantamine. Int J Dev Neurosci 2009;27:59–64. doi: 10.1016/j.ijdevneu.2008.09.200
   PubMed Web of Science ®Google Scholar
• Hulshof HJ, Novati A, Sgoifo A, Luiten PG, Den Boer JA, Meerlo P. Maternal separation decreases adult hippocampal cell proliferation and impairs cognitive performance but has little effect on stress sensitivity and anxiety in adult Wistar rats. Behav Brain Res 2011;216(2):552–60. doi: 10.1016/j.bbr.2010.08.038
   PubMed Web of Science ®Google Scholar
• Gähwiler BH. Development of the hippocampus in vitro: cell types, synapses and receptors. Neuroscience 1984;11(4):751–60. doi: 10.1016/0306-4522(84)90192-1
   PubMed Web of Science ®Google Scholar
• Sapolsky RM, Krey LC, McEwen BS. The neuroendocrinology of stress and aging: the glucocorticoid cascade hypothesis*. Endocr Rev 1986;7(3):284–301. doi: 10.1210/edrv-7-3-284
   PubMed Web of Science ®Google Scholar
• Ivy AS, Rex CS, Chen Y, Dube C, Maras PM, Grigoriadis DE., et al. Hippocampal dysfunction and cognitive impairments provoked by chronic early-life stress involve excessive activation of CRH receptors. J Neurosci 2010;30:13005–15. doi: 10.1523/JNEUROSCI.1784-10.2010
   PubMed Web of Science ®Google Scholar
• Cintra A, Bhatnagar M, Chadi G, Tinner B, Lindberg J, Gustafsson JA, et al. Glial and neuronal glucocorticoid receptor immunoreactive cell populations in developing, adult, and aging brain. Annu NY Acad Sci 1994;746:42–61. doi: 10.1111/j.1749-6632.1994.tb39210.x
   PubMed Web of Science ®Google Scholar
• Han JS, Bizon JL, Chun HJ, Maus CE, Gallagher M. Decreased glucocorticoid receptor mRNA and dysfunction of HPA axis in rats after removal of the cholinergic innervation to hippocampus. Eur J Neurosci 2002;16(7):1399–404. doi: 10.1046/j.1460-9568.2002.02191.x
   PubMed Web of Science ®Google Scholar
• Helm KA, Han JS, Gallagher M. Effects of cholinergic lesions produced by infusions of 192 IgG-saporin on glucocorticoid receptor mRNA expression in hippocampus and medial prefrontal cortex of the rat. Neuroscience 2002;115(3):765–74. doi: 10.1016/S0306-4522(02)00487-6
   PubMed Web of Science ®Google Scholar
• Helm KA, Ziegler DR, Gallagher M. Habituation to stress and dexamethasone suppression in rats with selective basal forebrain cholinergic lesions. Hippocampus 2004;14(5):628–35. doi: 10.1002/hipo.10203
   PubMed Web of Science ®Google Scholar
• Emgard M, Paradisi M, Pirondi S, Fernández M, Giardino L, Calzà L. Prenatal glucocorticoid exposure affects learning and vulnerability of cholinergic neurons. Neurobiol Aging 2007;28:112–21. doi: 10.1016/j.neurobiolaging.2005.11.015
   PubMed Web of Science ®Google Scholar
• Aisa B, Gil-Bea FJ, Marcos B, Tordera R, Lasheras B, Del Río J, et al. Neonatal stress affects vulnerability of cholinergic neurons and cognition in the rat: involvement of the HPA axis. Psychoneuroendocrinology 2009;34(10):1495–505. doi: 10.1016/j.psyneuen.2009.05.003
   PubMed Web of Science ®Google Scholar
• McClelland S, Korosi A, Cope J, Ivy A, Baram TZ. Emerging roles of epigenetic mechanisms in the enduring effects of early-life stress and experience on learning and memory. Neurobiol Learn Mem 2011;96(1):79–88. doi: 10.1016/j.nlm.2011.02.008
   PubMed Web of Science ®Google Scholar
• Sable P, Randhir K, Kale A, Chavan-Gautam P, Joshi S. Maternal micronutrients and brain global methylation patterns in the offspring. Nutr Neurosci 2015;18(1):30–36. doi: 10.1179/1476830513Y.0000000097
   PubMed Web of Science ®Google Scholar
• Zhang N. Epigenetic modulation of DNA methylation by nutrition and its mechanisms in animals. Anim Nutr 2015.
   Google Scholar
• Lillycrop KA, Phillips ES, Jackson AA, Hanson MA, Burdge GC. Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J Nutr 2005;135(6):1382–6.
   PubMed Web of Science ®Google Scholar
• Farias N, Ho N, Butler S, Delaney L, Morrison J, Shahrzad S, et al. The effects of folic acid on global DNA methylation and colonosphere formation in colon cancer cell lines. J Nutr Biochem 2015;26:818–26. doi: 10.1016/j.jnutbio.2015.02.002
   PubMed Web of Science ®Google Scholar
• Chen J, Evans AN, Liu Y, Honda M, Saavedra JM, Aguilera G. Maternal deprivation in rats is associated with corticotrophin-releasing hormone (CRH) Promoter hypomethylation and enhances CRH transcriptional responses to stress in adulthood. J Neuroendocrinol 2012;24(7):1055–64. doi: 10.1111/j.1365-2826.2012.02306.x
   PubMed Web of Science ®Google Scholar
• Holmes GL, Yang Y, Liu Z, Cermak JM, Sarkisian MR, Stafstrom CE, et al. Seizure-induced memory impairment is reduced by choline supplementation before or after status epilepticus. Epileptic Res 2002;48:3–13. doi: 10.1016/S0920-1211(01)00321-7
   PubMed Web of Science ®Google Scholar
• Nag N, Mellott TJ, Berger-Sweeney JE. Effects of postnatal dietary choline supplementation on motor regional brain volume and growth factor expression in a mouse model of Rett syndrome. Brain Res 2008;1237:101–9. doi: 10.1016/j.brainres.2008.08.042
   PubMed Web of Science ®Google Scholar
• Glenn MJ, Gibson EM, Kirby ED, Mellott TJ, Blusztajn JK, Williams CL. Prenatal choline availability modulates hippocampal neurogenesis and neurogenic responses to enriching experiences in adult female rats. Eur J Neurosci 2007;25:2473–82. doi: 10.1111/j.1460-9568.2007.05505.x
   PubMed Web of Science ®Google Scholar
• Choy KH, de Visser Y, Nichols NR, van den Buuse M. Combined neonatal stress and young-adult glucocorticoid stimulation in rats reduce BDNF expression in hippocampus: effects on learning and memory. Hippocampus 2008;18:655–67. doi: 10.1002/hipo.20425
   PubMed Web of Science ®Google Scholar
• Lajud N, Roque A, Cajero M, Gutierrez-Ospina G, Torner L. Periodic maternal separation decreases hippocampal neurogenesis without affecting basal corticosterone during the stress hyporesponsive period, but alters HPA axis and coping behavior in adulthood. Psychoneuroendocrinology 2012;37:410–20. doi: 10.1016/j.psyneuen.2011.07.011
   PubMed Web of Science ®Google Scholar
• Alkondon M, Pereira EFR, Cortes WS, Maelicke A, Albuquerque EX. Choline is a selective agonist of α7 nicotinic acetylcholine receptors in the rat brain neurons. Eur J Neurosci 1997;9:2734–42. doi: 10.1111/j.1460-9568.1997.tb01702.x
   PubMed Web of Science ®Google Scholar
• Weaver IC, Champagne FA, Brown SE, Dymov S, Sharma S, Meaney MJ, et al. Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: altering epigenetic marking later in life. J Neurosci 2005;25(47):11045–54. doi: 10.1523/JNEUROSCI.3652-05.2005
   PubMed Web of Science ®Google Scholar
• Anderson OS, Sant KE, Dolinoy DC. Nutrition and epigenetics: an interplay of dietary methyl donors, one-carbon metabolism and DNA methylation. J Nutr Biochem 2012;23(8):853–9. doi: 10.1016/j.jnutbio.2012.03.003
   PubMed Web of Science ®Google Scholar
• Detich N, Hamm S, Just G, Knox JD, Szyf M. The methyl donor S-adenosylmethionine inhibits active demethylation of DNA a candidate novel mechanism for the pharmacological effects of S-adenosylmethionine. J Biol Chem 2003;278(23):20812–20. doi: 10.1074/jbc.M211813200
   PubMed Web of Science ®Google Scholar
• Jiang X, Yan J, West AA, Perry CA, Malysheva OV, Devapatla S, et al. Maternal choline intake alters the epigenetic state of fetal cortisol-regulating genes in humans. FASEB J 2012;26(8):3563–74. doi: 10.1096/fj.12-207894
   PubMed Web of Science ®Google Scholar
• Cai L, Gibbs RB, Johnson DA. Recognition of novel objects and their location in rats with selective cholinergic lesion of the medial septum. Neurosci Lett 2012;506(2):261–5. doi: 10.1016/j.neulet.2011.11.019
   PubMed Web of Science ®Google Scholar
• Melichercik AM, Elliott KS, Bianchi C, Ernst SM, Winters BD. Nicotinic receptor activation in perirhinal cortex and hippocampus enhances object memory in rats. Neuropharmacology 2012;62(5):2096–105. doi: 10.1016/j.neuropharm.2012.01.008
   PubMed Web of Science ®Google Scholar
• NICHD Early Child Care Research Network. Early child care and children's development prior to school entry: results from the NICHD Study of Early Child Care. Am Edu Res J 2002;39:133–64. doi: 10.3102/00028312039001133
   Web of Science ®Google Scholar
• Gunnar MR, Donzella B. Social regulation of the cortisol levels in early human development. Psychoneuroendocrinology 2002;27(1):199–220. doi: 10.1016/S0306-4530(01)00045-2
   PubMed Web of Science ®Google Scholar
• Dettling AC, Parker SW, Lane S, Sebanc A, Gunnar MR. Quality of care and temperament determine whether cortisol levels rise over the day for children in full-day childcare. Psychoneuroendocrinology 2000;25:819–36. doi: 10.1016/S0306-4530(00)00028-7
   PubMed Web of Science ®Google Scholar
• Legendre A. Environmental features influencing toddlers’ bioemotional reactions in day care centers. Environ Behav 2003;35(4):523–49. doi: 10.1177/0013916503035004005
   Web of Science ®Google Scholar
• Groeneveld MG, Vermeer HJ, van IJzendoorn MH, Linting M. Children's wellbeing and cortisol levels in home-based and center-based childcare. Early Childhood Res Quart 2010;25(4):502–14. doi: 10.1016/j.ecresq.2009.12.004
   Web of Science ®Google Scholar