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Perinatal and Postnatal Determinants of Brain Development: Recent Studies and Methodological Advances

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Book cover Prenatal and Postnatal Determinants of Development

Part of the book series: Neuromethods ((NM,volume 109))

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Abstract

Perinatal diet is an important factor in programming brain development and susceptibility to obesity. There are currently several elegant and simple prenatal and postnatal animal models in use to mimic the effects of early life overfeeding and to study its impact on brain and metabolic development. In this chapter we will discuss the background to some of these models, with a specific focus on manipulating rodent litter sizes to alter the early life nutritional environment.

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References

  1. Flegal KM, Carroll MD, Ogden CL, Johnson CL (2002) Prevalence and trends in obesity among US adults, 1999-2000. JAMA 288(14):1723–1727

    Article  PubMed  Google Scholar 

  2. Colagiuri S, Lee CM, Colagiuri R, Magliano D, Shaw JE, Zimmet PZ et al (2010) The cost of overweight and obesity in Australia. Med J Aust 192(5):260–264

    PubMed  Google Scholar 

  3. Ong ZY, Muhlhausler BS (2011) Maternal “junk-food” feeding of rat dams alters food choices and development of the mesolimbic reward pathway in the offspring. FASEB J 25(7):2167–2179

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  4. Casas M, Chatzi L, Carsin AE, Amiano P, Guxens M, Kogevinas M et al (2013) Maternal pre-pregnancy overweight and obesity, and child neuropsychological development: two Southern European birth cohort studies. Int J Epidemiol 42(2):506–517

    Article  PubMed  Google Scholar 

  5. Kasturi SS, Tannir J, Brannigan RE (2008) The metabolic syndrome and male infertility. J Androl 29(3):251–259

    Article  CAS  PubMed  Google Scholar 

  6. Figueroa-Colon R, Arani RB, Goran MI, Weinsier RL (2000) Paternal body fat is a longitudinal predictor of changes in body fat in premenarcheal girls. Am J Clin Nutr 71(3):829–834

    CAS  PubMed  Google Scholar 

  7. Ng SF, Lin RC, Laybutt DR, Barres R, Owens JA, Morris MJ (2010) Chronic high-fat diet in fathers programs beta-cell dysfunction in female rat offspring. Nature 467(7318):963–966

    Article  CAS  PubMed  Google Scholar 

  8. Aerts L, Holemans K, Van Assche FA (1990) Maternal diabetes during pregnancy: consequences for the offspring. Diabetes Metab Rev 6(3):147–167

    Article  CAS  PubMed  Google Scholar 

  9. Silverman BL, Metzger BE, Cho NH, Loeb CA (1995) Impaired glucose tolerance in adolescent offspring of diabetic mothers. Relationship to fetal hyperinsulinism. Diabetes Care 18(5):611–617

    Article  CAS  PubMed  Google Scholar 

  10. Plagemann A, Harder T, Kohlhoff R, Rohde W, Dorner G (1997) Glucose tolerance and insulin secretion in children of mothers with pregestational IDDM or gestational diabetes. Diabetologia 40(9):1094–1100

    Article  CAS  PubMed  Google Scholar 

  11. Weiss PA, Scholz HS, Haas J, Tamussino KF, Seissler J, Borkenstein MH (2000) Long-term follow-up of infants of mothers with type 1 diabetes: evidence for hereditary and nonhereditary transmission of diabetes and precursors. Diabetes Care 23(7):905–911

    Google Scholar 

  12. Albuquerque KT, Sardinha FL, Telles MM, Watanabe RL, Nascimento CM, Tavares do Carmo MG et al (2006) Intake of trans fatty acid-rich hydrogenated fat during pregnancy and lactation inhibits the hypophagic effect of central insulin in the adult offspring. Nutrition 22(7–8):820–829

    Article  CAS  PubMed  Google Scholar 

  13. Srinivasan M, Katewa SD, Palaniyappan A, Pandya JD, Patel MS (2006) Maternal high-fat diet consumption results in fetal malprogramming predisposing to the onset of metabolic syndrome-like phenotype in adulthood. Am J Physiol Endocrinol Metab 291(4):E792–E799

    Article  CAS  PubMed  Google Scholar 

  14. Ashino NG, Saito KN, Souza FD, Nakutz FS, Roman EA, Velloso LA et al (2012) Maternal high-fat feeding through pregnancy and lactation predisposes mouse offspring to molecular insulin resistance and fatty liver. J Nutr Biochem 23(4):341–348

    Article  CAS  PubMed  Google Scholar 

  15. Whitaker RC, Wright JA, Pepe MS, Seidel KD, Dietz WH (1997) Predicting obesity in young adulthood from childhood and parental obesity. N Engl J Med 337(13):869–873

    Article  CAS  PubMed  Google Scholar 

  16. Biro FM, Wien M (2010) Childhood obesity and adult morbidities. Am J Clin Nutr 91(5):1499S–1505S

    Article  PubMed Central  PubMed  Google Scholar 

  17. Lucas A (1998) Programming by early nutrition: an experimental approach. J Nutr 128(Suppl 2):406S

    Google Scholar 

  18. Gluckman PD, Hanson MA (2004) Living with the past: evolution, development, and patterns of disease. Science 305(5691):1733–1736

    Article  CAS  PubMed  Google Scholar 

  19. Singhal A, Kennedy K, Lanigan J, Fewtrell M, Cole TJ, Stephenson T et al (2010) Nutrition in infancy and long-term risk of obesity: evidence from 2 randomized controlled trials. Am J Clin Nutr 92(5):1133–1144

    Article  CAS  PubMed  Google Scholar 

  20. Stettler N, Stallings VA, Troxel AB, Zhao J, Schinnar R, Nelson SE et al (2005) Weight gain in the first week of life and overweight in adulthood: a cohort study of European American subjects fed infant formula. Circulation 111(15):1897–1903

    Article  PubMed  Google Scholar 

  21. Park Y, Albright KJ, Storkson JM, Liu W, Pariza MW (2007) Conjugated linoleic acid (CLA) prevents body fat accumulation and weight gain in an animal model. J Food Sci 72(8):S612–S617

    Article  CAS  PubMed  Google Scholar 

  22. Racine NM, Watras AC, Carrel AL, Allen DB, McVean JJ, Clark RR et al (2010) Effect of conjugated linoleic acid on body fat accretion in overweight or obese children. Am J Clin Nutr 91(5):1157–1164

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  23. Rist L, Mueller A, Barthel C, Snijders B, Jansen M, Simoes-Wust AP et al (2007) Influence of organic diet on the amount of conjugated linoleic acids in breast milk of lactating women in the Netherlands. Br J Nutr 97(4):735–743

    Article  CAS  PubMed  Google Scholar 

  24. Lassek WD, Gaulin SJ (2013) Maternal milk DHA content predicts cognitive performance in a sample of 28 nations. Matern Child Nutr

    Google Scholar 

  25. Koletzko B, von Kries R, Monasterolo RC, Subias JE, Scaglioni S, Giovannini M et al (2009) Infant feeding and later obesity risk. Adv Exp Med Biol 646:15–29

    Article  PubMed  Google Scholar 

  26. Willatts P, Forsyth S, Agostoni C, Casaer P, Riva E, Boehm G (2013) Effects of long-chain PUFA supplementation in infant formula on cognitive function in later childhood. Am J Clin Nutr 98(2):536S–542S

    Article  CAS  PubMed  Google Scholar 

  27. Seach KA, Dharmage SC, Lowe AJ, Dixon JB (2010) Delayed introduction of solid feeding reduces child overweight and obesity at 10 years. Int J Obes 34(10):1475–1479

    Article  CAS  Google Scholar 

  28. Durmus B, van Rossem L, Duijts L, Arends LR, Raat H, Moll HA et al (2011) Breast-feeding and growth in children until the age of 3 years: the Generation R Study. Br J Nutr 105(11):1704–1711

    Article  CAS  PubMed  Google Scholar 

  29. Fiorotto ML, Burrin DG, Perez M, Reeds PJ (1991) Intake and use of milk nutrients by rat pups suckled in small, medium, or large litters. Am J Physiol 260(6 Pt 2):R1104–R1113

    CAS  PubMed  Google Scholar 

  30. West JR (1993) Use of pup in a cup model to study brain development. J Nutr 123(Suppl 2):382–385

    CAS  PubMed  Google Scholar 

  31. Vuguin PM (2007) Animal models for small for gestational age and fetal programming of adult disease. Horm Res 68(3):113–123

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  32. Lukaszewski MA, Eberle D, Vieau D, Breton C (2013) Nutritional manipulations in the perinatal period program adipose tissue in offspring. Am J Physiol Endocrinol Metab 305(10):E1195–E1207

    Article  CAS  PubMed  Google Scholar 

  33. Williams L, Seki Y, Vuguin PM, Charron MJ (2014) Animal models of in utero exposure to a high fat diet: a review. Biochim Biophys Acta 1842(3):507–519

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  34. Bouret SG, Simerly RB (2007) Development of leptin-sensitive circuits. J Neuroendocrinol 19(8):575–582

    Article  CAS  PubMed  Google Scholar 

  35. Perez-Cano FJ, Franch A, Castellote C, Castell M (2012) The suckling rat as a model for immunonutrition studies in early life. Clin Dev Immunol 2012:537310

    PubMed Central  PubMed  Google Scholar 

  36. Plagemann A, Heidrich I, Gotz F, Rohde W, Dorner G (1992) Obesity and enhanced diabetes and cardiovascular risk in adult rats due to early postnatal overfeeding. Exp Clin Endocrinol 99(3):154–158

    Article  CAS  PubMed  Google Scholar 

  37. Panchal SK, Brown L (2011) Rodent models for metabolic syndrome research. J Biomed Biotechnol 2011:351982

    Article  PubMed Central  PubMed  Google Scholar 

  38. Speakman J, Hambly C, Mitchell S, Krol E (2008) The contribution of animal models to the study of obesity. Lab Anim 42(4):413–432

    Article  CAS  PubMed  Google Scholar 

  39. Buckley AJ, Keseru B, Briody J, Thompson M, Ozanne SE, Thompson CH (2005) Altered body composition and metabolism in the male offspring of high fat-fed rats. Metabolism 54(4):500–507

    Article  CAS  PubMed  Google Scholar 

  40. Samuelsson AM, Matthews PA, Argenton M, Christie MR, McConnell JM, Jansen EH et al (2008) Diet-induced obesity in female mice leads to offspring hyperphagia, adiposity, hypertension, and insulin resistance: a novel murine model of developmental programming. Hypertension 51(2):383–392

    Article  CAS  PubMed  Google Scholar 

  41. Chen H, Simar D, Morris MJ (2009) Hypothalamic neuroendocrine circuitry is programmed by maternal obesity: interaction with postnatal nutritional environment. PLoS One 4(7):e6259

    Article  PubMed Central  PubMed  Google Scholar 

  42. Desai M, Jellyman JK, Han G, Beall M, Lane RH, Ross MG (2014) Rat maternal obesity and high fat diet program offspring metabolic syndrome. Am J Obstet Gynecol 211(3):237.e1–237.e13

    Article  Google Scholar 

  43. Hall WG (1975) Weaning and growth of artificially reared rats. Science 190(4221):1313–1315

    Article  CAS  PubMed  Google Scholar 

  44. Beierle EA, Chen MK, Hartwich JE, Iyengar M, Dai W, Li N et al (2004) Artificial rearing of mouse pups: development of a mouse pup in a cup model. Pediatr Res 56(2):250–255

    Article  PubMed  Google Scholar 

  45. Diaz J, Moore E, Petracca F, Schacher J, Stamper C (1982) Artificial rearing of rat pups with a protein-enriched formula. J Nutr 112(5):841–847

    CAS  PubMed  Google Scholar 

  46. Spencer SJ, Tilbrook A (2009) Neonatal overfeeding alters adult anxiety and stress responsiveness. Psychoneuroendocrinology 34(8):1133–1143

    Article  PubMed Central  PubMed  Google Scholar 

  47. Clarke MA, Stefanidis A, Spencer SJ (2012) Postnatal overfeeding leads to obesity and exacerbated febrile responses to lipopolysaccharide throughout life. J Neuroendocrinol 24(3):511–524

    Article  CAS  PubMed  Google Scholar 

  48. Stefanidis A, Spencer SJ (2012) Effects of neonatal overfeeding on juvenile and adult feeding and energy expenditure in the rat. PLoS One 7(12), e52130

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  49. Smith JT, Spencer SJ (2012) Preweaning over- and underfeeding alters onset of puberty in the rat without affecting kisspeptin. Biol Reprod 86(5):145, 141–148

    Google Scholar 

  50. Bulfin LJ, Clarke MA, Buller KM, Spencer SJ (2011) Anxiety and hypothalamic-pituitary-adrenal axis responses to psychological stress are attenuated in male rats made lean by large litter rearing. Psychoneuroendocrinology 36(7):1080–1091

    Article  CAS  PubMed  Google Scholar 

  51. Clarke M, Cai G, Saleh S, Buller KM, Spencer SJ (2013) Being suckled in a large litter mitigates the effects of early-life stress on hypothalamic-pituitary-adrenal axis function in the male rat. J Neuroendocrinol 25(9):792–802

    Article  CAS  PubMed  Google Scholar 

  52. Farrell WJ, Alberts JR (2007) Rat behavioral thermoregulation integrates with nonshivering thermogenesis during postnatal development. Behav Neurosci 121(6):1333–1341

    Article  PubMed  Google Scholar 

  53. Suckow MA, Weisbroth SH, Franklin CL (2005) The laboratory rat. Academic, New York, NY

    Google Scholar 

  54. Lane-Petter W (1968) Cannibalism in rats and mice. Proc R Soc Med 61(12):1295–1296

    PubMed Central  CAS  PubMed  Google Scholar 

  55. DeSantis DT, Schmaltz LW (1984) The mother-litter relationship in developmental rat studies: cannibalism vs caring. Dev Psychobiol 17(3):255–262

    Article  CAS  PubMed  Google Scholar 

  56. http://www.arc.wa.gov.au

  57. Cierpial MA, Murphy CA, McCarty R (1990) Maternal behavior of spontaneously hypertensive and Wistar-Kyoto normotensive rats: effects of reciprocal cross-fostering of litters. Behav Neural Biol 54(1):90–96

    Article  CAS  PubMed  Google Scholar 

  58. Sharpe RM, Morris A, Wyatt AC (1973) The effect of the sex of litter-mates on the subsequent behaviour and breeding performance of cross-fostered rats. Lab Anim 7(1):51–59

    Article  CAS  PubMed  Google Scholar 

  59. Moore CL, Morelli GA (1979) Mother rats interact differently with male and female offspring. J Comp Physiol Psychol 93(4):677–684

    Article  CAS  PubMed  Google Scholar 

  60. Lazic SE (2010) The problem of pseudoreplication in neuroscientific studies: is it affecting your analysis? BMC Neurosci 11:5

    Article  PubMed Central  PubMed  Google Scholar 

  61. Liu D, Diorio J, Tannenbaum B, Caldji C, Francis D, Freedman A et al (1997) Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 277(5332):1659–1662

    Article  CAS  PubMed  Google Scholar 

  62. Caldji C, Tannenbaum B, Sharma S, Francis D, Plotsky PM, Meaney MJ (1998) Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proc Natl Acad Sci U S A 95(9):5335–5340

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  63. Francis DD, Meaney MJ (1999) Maternal care and the development of stress responses. Curr Opin Neurobiol 9(1):128–134

    Article  CAS  PubMed  Google Scholar 

  64. Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR et al (2004) Epigenetic programming by maternal behavior. Nat Neurosci 7(8):847–854

    Article  CAS  PubMed  Google Scholar 

  65. Hellstrom IC, Dhir SK, Diorio JC, Meaney MJ (2012) Maternal licking regulates hippocampal glucocorticoid receptor transcription through a thyroid hormone-serotonin-NGFI-A signalling cascade. Philos Trans R Soc Lond B Biol Sci 367(1601):2495–2510

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  66. Champagne F, Meaney MJ (2001) Like mother, like daughter: evidence for non-genomic transmission of parental behavior and stress responsivity. Prog Brain Res 133:287–302

    Article  CAS  PubMed  Google Scholar 

  67. Boullu-Ciocca S, Dutour A, Guillaume V, Achard V, Oliver C, Grino M (2005) Postnatal diet-induced obesity in rats upregulates systemic and adipose tissue glucocorticoid metabolism during development and in adulthood: its relationship with the metabolic syndrome. Diabetes 54(1):197–203

    Article  CAS  PubMed  Google Scholar 

  68. Schmidt I, Fritz A, Scholch C, Schneider D, Simon E, Plagemann A (2001) The effect of leptin treatment on the development of obesity in overfed suckling Wistar rats. Int J Obes Relat Metab Disord 25(8):1168–1174

    Article  CAS  PubMed  Google Scholar 

  69. Bouret SG, Draper SJ, Simerly RB (2004) Formation of projection pathways from the arcuate nucleus of the hypothalamus to hypothalamic regions implicated in the neural control of feeding behavior in mice. J Neurosci 24(11):2797–2805

    Article  CAS  PubMed  Google Scholar 

  70. Bouret SG, Draper SJ, Simerly RB (2004) Trophic action of leptin on hypothalamic neurons that regulate feeding. Science 304(5667):108–110

    Article  CAS  PubMed  Google Scholar 

  71. Bouret SG, Simerly RB (2006) Developmental programming of hypothalamic feeding circuits. Clin Genet 70(4):295–301

    Article  CAS  PubMed  Google Scholar 

  72. Oscai LB, McGarr JA (1978) Evidence that the amount of food consumed in early life fixes appetite in the rat. Am J Physiol 235(3):R141–R144

    CAS  PubMed  Google Scholar 

  73. Lopez M, Tovar S, Vazquez MJ, Nogueiras R, Seoane LM, Garcia M et al (2007) Perinatal overfeeding in rats∁ results in increased levels of plasma leptin but unchanged cerebrospinal leptin in adulthood. Int J Obes 31(2):371–377

    Article  CAS  Google Scholar 

  74. Rodrigues AL, De Souza EP, Da Silva SV, Rodrigues DS, Nascimento AB, Barja-Fidalgo C et al (2007) Low expression of insulin signaling molecules impairs glucose uptake in adipocytes after early overnutrition. J Endocrinol 195(3):485–494

    Article  CAS  PubMed  Google Scholar 

  75. Rodrigues AL, de Moura EG, Passos MC, Dutra SC, Lisboa PC (2009) Postnatal early overnutrition changes the leptin signalling pathway in the hypothalamic-pituitary-thyroid axis of young and adult rats. J Physiol 587(Pt 11):2647–2661

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  76. Xiao XQ, Williams SM, Grayson BE, Glavas MM, Cowley MA, Smith MS et al (2007) Excess weight gain during the early postnatal period is associated with permanent reprogramming of brown adipose tissue adaptive thermogenesis. Endocrinology 148(9):4150–4159

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by a Discovery Project Grant from the Australian Research Council (ARC) to SJS (DP130100508). SJS is an ARC Future Fellow (FT110100084) and an RMIT University VC Senior Research Fellow.

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Correspondence to Sarah J. Spencer .

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Spencer, S.J., Jenkins, T.A. (2016). Perinatal and Postnatal Determinants of Brain Development: Recent Studies and Methodological Advances. In: Walker, D. (eds) Prenatal and Postnatal Determinants of Development. Neuromethods, vol 109. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-3014-2_9

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  • DOI: https://doi.org/10.1007/978-1-4939-3014-2_9

  • Publisher Name: Humana Press, New York, NY

  • Print ISBN: 978-1-4939-3013-5

  • Online ISBN: 978-1-4939-3014-2

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