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Reproductive Sciences

, Volume 19, Issue 5, pp 493–504 | Cite as

Sex-Dependent Cognitive Performance in Baboon Offspring Following Maternal Caloric Restriction in Pregnancy and Lactation

  • Jesse S. RodriguezEmail author
  • Thad Q. Bartlett
  • Kathryn E. Keenan
  • Peter W. Nathanielsz
  • Mark J. Nijland
Original Articles

Abstract

In humans a suboptimal diet during development has negative outcomes in offspring. We investigated the behavioral outcomes in baboons born to mothers undergoing moderate maternal nutrient restriction (MNR). Maternal nutrient restriction mothers (n = 7) were fed 70% of food eaten by controls (CTR, n = 12) fed ad libitum throughout gestation and lactation. At 3.3 ± 0.2 (mean ± standard error of the mean [SEM]) years of age offspring (controls: female [FC, n = 8], male [MC, n = 4]; nutrient restricted: female [FR, n = 3] and male [MR, n = 4]) were administered progressive ratio, simple discrimination, intra-/extra-dimension set shift and delayed matching to sample tasks to assess motivation, learning, attention, and working memory, respectively. A treatment effect was observed in MNR offspring who demonstrated less motivation and impaired working memory. Nutrient-restricted female offspring showed improved learning, while MR offspring showed impaired learning and attentional set shifting and increased impulsivity. In summary, 30% restriction in maternal caloric intake has long lasting neurobehavioral outcomes in adolescent male baboon offspring.

Keywords

developmental programming motivation learning memory attention 

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References

  1. 1.
    Baker PN, Wheeler SJ, Sanders TA, et al. A prospective study of micronutrient status in adolescent pregnancy. Am J Clin Nutr. 2009;89(4):1114–1124.PubMedCrossRefPubMedCentralGoogle Scholar
  2. 2.
    Beard JR, Lincoln D, Donoghue D, et al. Socioeconomic and maternal determinants of small-for-gestational age births: patterns of increasing disparity. Acta Obstet Gynecol Scand. 2009;88(5):575–583.PubMedCrossRefPubMedCentralGoogle Scholar
  3. 3.
    Taylor PD, Poston L. Developmental programming of obesity in mammals. Exp Physiol. 2007;92(2):287–298.PubMedCrossRefPubMedCentralGoogle Scholar
  4. 4.
    Nijland MJ, Ford SP, Nathanielsz PW. Prenatal origins of adult disease. Curr Opin Obstet Gynecol. 2008;20(2):132–138.PubMedCrossRefPubMedCentralGoogle Scholar
  5. 5.
    Nuyt AM, Alexander BT. Developmental programming and hypertension. Curr Opin Nephrol Hypertens. 2009;18(2):144–152.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Solomons NW. Developmental origins of health and disease: concepts, caveats, and consequences for public health nutrition. Nutr Rev. 2009;67(suppl 1):S12–S16.PubMedCrossRefPubMedCentralGoogle Scholar
  7. 7.
    Symonds ME, Sebert SP, Hyatt MA, Budge H. Nutritional programming of the metabolic syndrome. Nat Rev Endocrinol. 2009;5(11):604–610.PubMedCrossRefPubMedCentralGoogle Scholar
  8. 8.
    Bouret SG. Development of hypothalamic neural networks controlling appetite. Forum Nutr. 2010;63:84–93.PubMedCrossRefPubMedCentralGoogle Scholar
  9. 9.
    Warner MJ, Ozanne SE. Mechanisms involved in the developmental programming of adulthood disease. Biochem J. 2010;427(3):333–347.PubMedCrossRefPubMedCentralGoogle Scholar
  10. 10.
    Armitage JA, Khan IY, Taylor PD, Nathanielsz PW, Poston L. Developmental programming of the metabolic syndrome by maternal nutritional imbalance: how strong is the evidence from experimental models in mammals? J Physiol. 2004;561(Pt 2):355–377.PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Harding JE. The nutritional basis of the fetal origins of adult disease. Int J Epidemiol. 2001;30(1):15–23.PubMedCrossRefPubMedCentralGoogle Scholar
  12. 12.
    Duggan MB. Nutritional update: relevance to maternal and child health in East Africa. Afr Health Sci. 2003;3(3):136–143.PubMedPubMedCentralGoogle Scholar
  13. 13.
    Guilloteau P, Zabielski R, Hammon HM, Metges CC. Adverse effects of nutritional programming during prenatal and early postnatal life, some aspects of regulation and potential prevention and treatments. J Physiol Pharmacol. 2009;60(suppl 3):17–35.PubMedPubMedCentralGoogle Scholar
  14. 14.
    Stein AD, Pierik FH, Verrips GH, Susser ES, Lumey LH. Maternal exposure to the Dutch famine before conception and during pregnancy: quality of life and depressive symptoms in adult offspring. Epidemiology. 2009;20(6):909–915.PubMedCrossRefPubMedCentralGoogle Scholar
  15. 15.
    Morgane PJ, Austin-LaFrance R, Bronzino J, et al. Prenatal malnutrition and development of the brain. Neurosci Biobehav Rev. 1993;17(1):91–128.PubMedCrossRefPubMedCentralGoogle Scholar
  16. 16.
    Morgane PJ, Mokler DJ, Galler JR. Effects of prenatal protein malnutrition on the hippocampal formation. Neurosci Biobehav Rev. 2002;26(4):471–483.PubMedCrossRefPubMedCentralGoogle Scholar
  17. 17.
    Bedi KS. Nutritional effects on neuron numbers. Nutr Neurosci. 2003;6(3):141–152.PubMedCrossRefPubMedCentralGoogle Scholar
  18. 18.
    Lister JP, Blatt GJ, DeBassio WA, et al. Effect of prenatal protein malnutrition on numbers of neurons in the principal cell layers of the adult rat hippocampal formation. Hippocampus. 2005;15(3):393–403.PubMedCrossRefPubMedCentralGoogle Scholar
  19. 19.
    Lister JP, Tonkiss J, Blatt GJ, et al. Asymmetry of neuron numbers in the hippocampal formation of prenatally malnourished and normally nourished rats: a stereological investigation. Hippocampus. 2006;16(11):946–958.PubMedCrossRefPubMedCentralGoogle Scholar
  20. 20.
    Benton D. The influence of children’s diet on their cognition and behavior. Eur J Nutr. 2008;47(suppl 3):25–37.PubMedCrossRefPubMedCentralGoogle Scholar
  21. 21.
    Lucas A. Long-term programming effects of early nutrition—implications for the preterm infant. J Perinatol. 2005;25(suppl 2):S2–S6.PubMedCrossRefPubMedCentralGoogle Scholar
  22. 22.
    Galler JR, Ramsey FC, Morley DS, Archer E, Salt P. The long-term effects of early kwashiorkor compared with marasmus. IV. Performance on the national high school entrance examination. Pediatr Res. 1990;28(3):235–239.PubMedCrossRefPubMedCentralGoogle Scholar
  23. 23.
    Galler JR, Waber D, Harrison R, Ramsey F. Behavioral effects of childhood malnutrition. Am J Psychiatry. 2005;162(9):1760–1761.PubMedCrossRefPubMedCentralGoogle Scholar
  24. 24.
    Antonow-Schlorke I, Schwab M, Cox LA, et al. From the cover: Vulnerability of the fetal primate brain to moderate reduction in maternal global nutrient availability. Proc Natl Acad Sci U S A. 2011;108(7):3011–3016.PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Tonkiss J, Shukitt-Hale B, Formica RN, Rocco FJ, Galler JR. Prenatal protein malnutrition alters response to reward in adult rats. Physiol Behav. 1990;48(5):675–680.PubMedCrossRefPubMedCentralGoogle Scholar
  26. 26.
    Tonkiss J, Galler JR, Formica RN, Shukitt-Hale B, Timm RR. Fetal protein malnutrition impairs acquisition of a DRL task in adult rats. Physiol Behav. 1990;48(1):73–77.PubMedCrossRefPubMedCentralGoogle Scholar
  27. 27.
    Ranade SC, Rose A, Rao M, Gallego J, Gressens P, Mani S. Different types of nutritional deficiencies affect different domains of spatial memory function checked in a radial arm maze. Neuroscience. 2008;152(4):859–866.PubMedCrossRefPubMedCentralGoogle Scholar
  28. 28.
    Tonkiss J, Galler JR. Prenatal protein malnutrition and working memory performance in adult rats. Behav Brain Res. 1990;40(2):95–107.PubMedCrossRefPubMedCentralGoogle Scholar
  29. 29.
    Tonkiss J, Shultz PL, Shumsky JS, Galler JR. Development of spatial navigation following prenatal cocaine and malnutrition in rats: lack of additive effects. Neurotoxicol Teratol. 1997;19(5):363–372.PubMedCrossRefPubMedCentralGoogle Scholar
  30. 30.
    Reyes-Castro LA, Rodriguez JS, Rodriguez-Gonzalez GL, et al. Pre- and/or postnatal protein restriction in rats impairs learning and motivation in male offspring. Int J Dev Neurosci. 2011;29(2):177–182.PubMedCrossRefPubMedCentralGoogle Scholar
  31. 31.
    Reyes-Castro LA, Rodriguez JS, Rodriguez-Gonzalez GL, et al. Pre and/or postnatal protein restriction developmentally programs affect and risk assessment behaviors in adult male rats. Behav Brain Res. doi:10.1016/j.bbr.2011.06.008.PubMedCrossRefPubMedCentralGoogle Scholar
  32. 32.
    Coupe B, Dutriez-Casteloot I, Breton C, et al. Perinatal undernutrition modifies cell proliferation and brain-derived neurotrophic factor levels during critical time-windows for hypothalamic and hippocampal development in the male rat. J Neuroendocrinal. 2009;21(1):40–48.CrossRefGoogle Scholar
  33. 33.
    Morgane PJ, Galler JR, Mokler DJ. A review of systems and networks of the limbic forebrain/limbic midbrain. Prog Neurobiol. 2005;75(2):143–160.PubMedCrossRefPubMedCentralGoogle Scholar
  34. 34.
    Kursmark M, Weitzman M. Recent findings concerning childhood food insecurity. Curr Opin Clin Nutr Metab Care. 2009; 12(3):310–316.PubMedCrossRefPubMedCentralGoogle Scholar
  35. 35.
    Schlabritz-Loutsevitch NE, Li C, Cox L, Nathanielsz PW. Baboon placental system N amino acid (AA) transporter protein is down regulated by moderate global maternal nutrient restriction (MNR). Reprod Sci. 2008;15(2):178A.Google Scholar
  36. 36.
    Schlabritz-Loutsevitch NE, Howell K, Rice K, et al. Development of a system for individual feeding of baboons maintained in an outdoor group social environment. Ja Med Primatol. 2004;33(3):117–126.CrossRefGoogle Scholar
  37. 37.
    Li C, Levitz M, Hubbard GB, et al. The IGF axis in baboon pregnancy: placental and systemic responses to feeding 70% global ad libitum diet. Placenta. 2007;28(11–12):1200–1210.PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Koenen SV, Mecenas CA, Smith GS, Jenkins S, Nathanielsz PW. Effects of maternal betamethasone administration on fetal and maternal blood pressure and heart rate in the baboon at 0. 7 of gestation. Am J Obstet Gynecol. 2002;186(4):812–817.PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Schlabritz-Loutsevitch NE, Lopez-Alvarenga JC, Comuzzie AG, et al. The prolonged effect of repeated maternal glucocorticoid exposure on the maternal and fetal leptin/insulin-like growth factor axis in Papio species. Reprod Sci. 2009;16(3):308–319.PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Choi J, Li C, McDonald TJ, Comuzzie AG, Mattern V, Nathanielsz PW. Emergence of insulin resistance in juvenile baboon offspring of mothers exposed to moderate maternal nutrient reduction. Am J Physiol Regul Integr Comp Physiol. 2011;301(3):R757–R762.PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Glassman DM, Coelho AM Jr, Carey KD, Bramblett CA. Weight growth in savannah baboons: a longitudinal study from birth to adulthood. Growth. 1984;48(4):425–433.PubMedPubMedCentralGoogle Scholar
  42. 42.
    Zurcher NR, Rodriguez JS, Jenkins SL, et al. Performance of juvenile baboons on neuropsychological tests assessing associative learning, motivation and attention. J Neurosci Methods. 2010;188(2):219–225.PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Rodriguez JS, Zurcher NR, Bartlett TQ, Nathanielsz PW, Nijland MJ. CANTAB delayed matching to sample task performance in juvenile baboons. J Neurosci Methods. 2011;196(2):258–263.PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Rodriguez JS, Morris SM, Hotchkiss CE, et al. The effects of chronic methylphenidate administration on operant test battery performance in juvenile rhesus monkeys. Neurotoxicol Teratol. 2010;32(2):142–151.PubMedCrossRefPubMedCentralGoogle Scholar
  45. 45.
    Miles JL, Landon J, Davison M, et al. Prenatally undernourished rats show increased preference for wheel running v. lever pressing for food in a choice task. Br J Nutr. 2009;101(6):902–908.PubMedCrossRefPubMedCentralGoogle Scholar
  46. 46.
    Dominguez-Salazar E, Camacho FJ, Paredes RG. Perinatal inhibition of aromatization enhances the reward value of sex. Behav Neurosci. 2008;122(4):855–860.PubMedCrossRefPubMedCentralGoogle Scholar
  47. 47.
    Nijland MJ, Mitsuya K, Li C, et al. Epigenetic modification of fetal baboon hepatic phosphoenolpyruvate carboxykinase following exposure to moderately reduced nutrient availability. J Physiol. 2010;588(Pt 8):1349–1359.PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Landon J, Davison M, Krageloh CU, et al. Global undernutrition during gestation influences learning during adult life. Learn Behav. 2007;35(2):79–86.PubMedCrossRefPubMedCentralGoogle Scholar
  49. 49.
    Erhard HW, Boissy A, Rae MT, Rhind SM. Effects of prenatal undernutrition on emotional reactivity and cognitive flexibility in adult sheep. Behav Brain Res. 2004;151(1–2):25–35.PubMedCrossRefPubMedCentralGoogle Scholar
  50. 50.
    Zhang Y, Li N, Yang Z. Perinatal food restriction impaired spatial learning and memory behavior and decreased the density of nitric oxide synthase neurons in the hippocampus of adult male rat offspring. Toxicol Lett. 2010;193(2):167–172.PubMedCrossRefPubMedCentralGoogle Scholar
  51. 51.
    Vuguin PM. Animal models for small for gestational age and fetal programming of adult disease. Horm Res. 2007;68(3):113–123.PubMedPubMedCentralGoogle Scholar
  52. 52.
    Zambrano E, Rodriguez-Gonzalez GL, Guzman C, et al. A maternal low protein diet during pregnancy and lactation in the rat impairs male reproductive development. J Physiol. 2005;563(Pt 1):275–284.PubMedCrossRefPubMedCentralGoogle Scholar
  53. 53.
    Hotchkiss AK, Lambright CS, Ostby JS, Parks-Saldutti L, Van-denbergh JG, Gray LE Jr. Prenatal testosterone exposure permanently masculinizes anogenital distance, nipple development, and reproductive tract morphology in female Sprague-Dawley rats. Toxicol Sci. 2007;96(2):335–345.PubMedCrossRefPubMedCentralGoogle Scholar
  54. 54.
    Puts DA, McDaniel MA, Jordan CL, Breedlove SM. Spatial ability and prenatal androgens: meta-analyses of congenital adrenal hyperplasia and digit ratio (2D:4D) studies. Arch Sex Behav. 2008;37(1):100–111.PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Meyer-Bahlburg HF. Brain development and cognitive, psychosocial, and psychiatric functioning in classical 21-hydroxylase deficiency. Endocr Dev. 2011;20:88–95.PubMedCrossRefPubMedCentralGoogle Scholar
  56. 56.
    Antonow-Schlorke I, Kuhn B, Muller T, et al. Antenatal betamethasone treatment reduces synaptophysin immunoreactivity in presynaptic terminals in the fetal sheep brain. Neurosci Lett. 2001;297(3):147–150.PubMedCrossRefPubMedCentralGoogle Scholar
  57. 57.
    Antonow-Schlorke I, Schwab M, Li C, Nathanielsz PW. Glucocorticoid exposure at the dose used clinically alters cytoskeletal proteins and presynaptic terminals in the fetal baboon brain. J Physiol. 2003;547(Pt 1):117–123.PubMedCrossRefPubMedCentralGoogle Scholar
  58. 58.
    Szuran TF, Pliska V, Pokorny J, Welzl H. Prenatal stress in rats: effects on plasma corticosterone, hippocampal glucocorticoid receptors, and maze performance. Physiol Behav. 2000;71(3–4):353–362.PubMedCrossRefPubMedCentralGoogle Scholar
  59. 59.
    Weinstock M. The long-term behavioural consequences of prenatal stress. Neurosci Biobehav Rev. 2008;32(6):1073–1086.PubMedCrossRefPubMedCentralGoogle Scholar
  60. 60.
    French NP, Hagan R, Evans SF, Mullan A, Newnham JP. Repeated antenatal corticosteroids: effects on cerebral palsy and childhood behavior. Am J Obstet Gynecol. 2004;190(3):588–595.PubMedCrossRefPubMedCentralGoogle Scholar
  61. 61.
    Johnson JW, Mitzner W, Beck JC, et al. Long-term effects of betamethasone on fetal development. Am J Obstet Gynecol. 1981;141(8):1053–1064.PubMedCrossRefPubMedCentralGoogle Scholar
  62. 62.
    Karemaker R, Heijnen CJ, Veen S, et al. Differences in behavioral outcome and motor development at school age after neonatal treatment for chronic lung disease with dexamethasone versus hydrocortisone. Pediatr Res. 2006;60(6):745–750.PubMedCrossRefPubMedCentralGoogle Scholar
  63. 63.
    Karemaker R, Kavelaars A, ter WM, et al. Neonatal dexamethasone treatment for chronic lung disease of prematurity alters the hypothalamus-pituitary-adrenal axis and immune system activity at school age. Pediatrics. 2008;121(4):e870–e878.PubMedCrossRefPubMedCentralGoogle Scholar
  64. 64.
    Matthews SG. Antenatal glucocorticoids and the developing brain: mechanisms of action. Semin Neonatol. 2001;6(4):309–317.PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Seckl JR. Glucocorticoids, developmental ‘programming’ and the risk of affective dysfunction. Prog Brain Res. 2008;167:17–34.PubMedCrossRefPubMedCentralGoogle Scholar
  66. 66.
    Uno H, Lohmiller L, Thieme C, et al. Brain damage induced by prenatal exposure to dexamethasone in fetal rhesus macaques. I. Hippocampus. Brain Res Dev Brain Res. 1990;53(2):157–167.PubMedCrossRefPubMedCentralGoogle Scholar
  67. 67.
    Uno H, Eisele S, Sakai A, et al. Neurotoxicity of glucocorticoids in the primate brain. Horm Behav. 1994;28(4):336–348.PubMedCrossRefPubMedCentralGoogle Scholar
  68. 68.
    Rodriguez JS, Zurcher NR, Keenan KE, Bartlett TQ, Nathanielsz PW, Nijland MJ. Prenatal betamethasone exposure has sex specific effects in reversal learning and attention in juvenile baboons. Am J Obstet Gynecol. 2011;204(6):e1–e10. doi:10.1016/j.ajog. 2011.01.063.CrossRefGoogle Scholar
  69. 69.
    Allvin K, Ankarberg-Lindgren C, Fors H, Dahlgren J. Elevated serum levels of estradiol, dihydrotestosterone, and inhibin B in adult males born small for gestational age. J Clin Endocrinol Metab. 2008;93(4):1464–1469.PubMedCrossRefPubMedCentralGoogle Scholar
  70. 70.
    Ong AD, Bergeman CS, Boker SM. Resilience comes of age: defining features in later adulthood. J Pera. 2009;77(6):1777–1804.Google Scholar
  71. 71.
    Torres N, Bautista CJ, Tovar AR, et al. Protein restriction during pregnancy affects maternal liver lipid metabolism and fetal brain lipid composition in the rat. Am J Physiol Endocrinol Metab. 2010;298(2):E270–7.PubMedCrossRefPubMedCentralGoogle Scholar
  72. 72.
    Galler JR, Ramsey F. A follow-up study of the influence of early malnutrition on development: behavior at home and at school. J Am Acad Child Adolesc Psychiatry. 1989;28(2):254–261.PubMedCrossRefPubMedCentralGoogle Scholar
  73. 73.
    Galler JR, Ramsey FC, Forde V, Salt P, Archer E. Long-term effects of early kwashiorkor compared with marasmus. II. Intellectual performance. J Pediatr Gastroenterol Nutr. 1987;6(6):847–854.PubMedCrossRefPubMedCentralGoogle Scholar
  74. 74.
    Galler JR, Ramsey F, Solimano G. The influence of early malnutrition on subsequent behavioral development III. Learning disabilities as a sequel to malnutrition. Pediatr Res. 1984;18(4):309–313.PubMedCrossRefPubMedCentralGoogle Scholar
  75. 75.
    Galler JR, Ramsey F, Solimano G, Lowell WE, Mason E. The influence of early malnutrition on subsequent behavioral development. I. Degree of impairment in intellectual performance. J Am Acad Child Psychiatry. 1983;22(1):8–15.PubMedCrossRefPubMedCentralGoogle Scholar
  76. 76.
    Rice D, Barone S Jr. Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Perspect. 2000;108(suppl 3):511–533.PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Jazin E, Cahill L. Sex differences in molecular neuroscience: from fruit flies to humans. Nat Rev Neurosci. 2010;11(1):9–17.PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Society for Reproductive Investigation 2012

Authors and Affiliations

  • Jesse S. Rodriguez
    • 1
    Email author
  • Thad Q. Bartlett
    • 2
  • Kathryn E. Keenan
    • 3
  • Peter W. Nathanielsz
    • 1
  • Mark J. Nijland
    • 1
  1. 1.Center for Pregnancy and Newborn Research, Department of Obstetrics and GynecologyUniversity of Texas Health Science CenterSan AntonioUSA
  2. 2.Department of AnthropologyUniversity of TexasSan AntonioUSA
  3. 3.Department of PsychiatryUniversity of ChicagoChicagoUSA

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