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23 - Prenatal Influences on Cognitive Aging

from Part IV - Cognitive, Social, and Biological Factors across the Lifespan

Published online by Cambridge University Press:  28 May 2020

Ayanna K. Thomas
Affiliation:
Tufts University, Massachusetts
Angela Gutchess
Affiliation:
Brandeis University, Massachusetts
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Summary

In studying determinants of cognitive aging and neurodegenerative diseases such as dementia, focus in research has mostly been on genetic background and lifestyle factors in adulthood. Over the past two decades, though, it has become increasingly clear that the foundations for brain functioning in later life are laid down in utero and adverse conditions during the prenatal period may increase the risk for the development of premature cognitive decline and neurodegenerative diseases. In this chapter, preclinical as well as clinical research that has provided evidence for prenatal influences on cognitive aging will be discussed. Especially in humans, the number of studies examining the effects of prenatal factors on cognitive aging and dementia is still limited. Evidence from studies such as the Dutch famine birth cohort study, though, suggests that factors such as undernutrition in pregnancy influence brain development and accelerate aging of the brain with negative repercussions for cognitive function and risk for dementia in later life. The evidence for a role of prenatal factors in cognitive aging is discussed in the light of the reserve capacity model, and potential underlying mechanisms are briefly reviewed. Finally, experimental studies in rodents suggest that the negative effects of adverse circumstances in early life are reversible. This is highly important and merits further investigation, especially since the number of prenatal factors that may influence cognitive aging is potentially large and may include factors such as maternal obesity and depression, and prenatal exposure to challenges of the immune system and air pollution. Improving these adverse prenatal circumstances may improve cognitive function in later life and decrease the risk for neurodegenerative diseases such as dementia.

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The Cambridge Handbook of Cognitive Aging
A Life Course Perspective
, pp. 423 - 439
Publisher: Cambridge University Press
Print publication year: 2020

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References

Adane, A. A., Mishra, G. D., & Tooth, L. R. (2016). Maternal pre-pregnancy obesity and childhood physical and cognitive development of children: A systematic review. International Journal of Obesity, 40(11), 16081618. doi: 10.1038/ijo.2016.140Google Scholar
Almond, D. M. B., & van Ewijk, R. (2015). In utero Ramadan exposure and children’s academic performance. Economic Journal, 125, 15011533. doi: 10.1111/ecoj.12168CrossRefGoogle Scholar
Antonow-Schlorke, I., Schwab, M., Cox, L. A., et al. (2011). Vulnerability of the fetal primate brain to moderate reduction in maternal global nutrient availability. Proceedings of the National Academy of Sciences USA, 108(7), 30113016. doi: 10.1073/pnas.1009838108CrossRefGoogle ScholarPubMed
Ars, C. L., Nijs, I. M., Marroun, H. E., et al. (2016). Prenatal folate, homocysteine and vitamin B12 levels and child brain volumes, cognitive development and psychological functioning: The Generation R Study. British Journal of Nutrition, 19. doi: 10.1017/s0007114515002081CrossRefGoogle Scholar
Behan, A. T., van den Hove, D. L., Mueller, L., et al. (2011). Evidence of female-specific glial deficits in the hippocampus in a mouse model of prenatal stress. European Neuropsychopharmacology, 21(1), 7179. doi: 10.1016/j.euroneuro.2010.07.004CrossRefGoogle Scholar
Bhat, N. R. (2010). Linking cardiometabolic disorders to sporadic Alzheimer’s disease: A perspective on potential mechanisms and mediators. Journal of Neurochemistry, 115(3), 551562. doi: 10.1111/j.1471-4159.2010.06978.xCrossRefGoogle ScholarPubMed
Borenstein, A. R., Copenhaver, C. I., & Mortimer, J. A. (2006). Early-life risk factors for Alzheimer disease. Alzheimer Disease and Associated Disorders, 20(1), 6372. doi: 10.1097/01.wad.0000201854.62116.d7Google Scholar
Brown, A. S., Vinogradov, S., Kremen, W. S., et al. (2009). Prenatal exposure to maternal infection and executive dysfunction in adult schizophrenia. American Journal of Psychiatry, 166(6), 683690. doi: 10.1176/appi.ajp.2008.08010089Google Scholar
Budni, J., Bellettini-Santos, T., Mina, F., Garcez, M. L., & Zugno, A. I. (2015). The involvement of BDNF, NGF and GDNF in aging and Alzheimer’s disease. Aging and Disease, 6(5), 331341. doi: 10.14336/ad.2015.0825Google ScholarPubMed
Buitelaar, J. K., Huizink, A. C., Mulder, E. J., de Medina, P. G., & Visser, G. H. (2003). Prenatal stress and cognitive development and temperament in infants. Neurobiology of Aging, 24(Suppl. 1), 5360; discussion 67–58. doi: 10.1016/S0197-4580(03)00050-2CrossRefGoogle ScholarPubMed
Buss, C., Entringer, S., & Wadhwa, P. D. (2012). Fetal programming of brain development: Intrauterine stress and susceptibility to psychopathology. Science Signaling, 5(245), pt7. doi: 10.1126/scisignal.2003406Google Scholar
Cao-Lei, L., de Rooij, S. R., King, S., et al. (2017). Prenatal stress and epigenetics. Neuroscience and Biobehavioral Reviews, 35(1), 1722. doi: 10.1016/j.neubiorev.2017.05.016Google Scholar
Cohen, S., & Greenberg, M. E. (2008). Communication between the synapse and the nucleus in neuronal development, plasticity, and disease. Annual Review of Cell and Developmental Biology, 24, 183209. doi: 10.1146/annurev.cellbio.24.110707.175235CrossRefGoogle ScholarPubMed
de Groot, R. H., Stein, A. D., Jolles, J., et al. (2011). Prenatal famine exposure and cognition at age 59 years. International Journal of Epidemiology, 40(2), 327337. doi: 10.1093/ije/dyq261CrossRefGoogle ScholarPubMed
de Rooij, S. R. (2018). A matter of survival: The detrimental consequences of adverse early life conditions. American Journal of Epidemiology, 187(10), 20932094. doi: 10.1093/aje/kwy088CrossRefGoogle ScholarPubMed
de Rooij, S. R., Caan, M. W., Swaab, D. F., et al. (2016). Prenatal famine exposure has sex-specific effects on brain size. Brain, 139(8), 21362142. doi: 10.1093/brain/aww132Google Scholar
de Rooij, S. R., Wouters, H., Yonker, J. E., Painter, R. C., & Roseboom, T. J. (2010). Prenatal undernutrition and cognitive function in late adulthood. Proceedings of the National Academy of Sciences USA, 107(39), 1688116886. doi: 10.1073/pnas.1009459107Google Scholar
Eckstrand, K. L., Ding, Z., Dodge, N. C., et al. (2012). Persistent dose-dependent changes in brain structure in young adults with low-to-moderate alcohol exposure in utero. Alcoholism: Clinical and Experimental Research, 36(11), 18921902. doi: 10.1111/j.1530-0277.2012.01819.xCrossRefGoogle ScholarPubMed
Entringer, S., Buss, C., Swanson, J. M., et al. (2012). Fetal programming of body composition, obesity, and metabolic function: The role of intrauterine stress and stress biology. Journal of Nutrition and Metabolism, 2012, 632548. doi: 10.1155/2012/632548Google Scholar
Ernst, M., & Korelitz, K. E. (2009). Cerebral maturation in adolescence: Behavioral vulnerability. Encephale, 35 (Suppl. 6), 182189. doi: 10.1016/s0013-7006(09)73469-4CrossRefGoogle ScholarPubMed
Franke, K., Clarke, G. D., Dahnke, R., et al. (2017). Premature brain aging in baboons resulting from moderate fetal undernutrition. Frontiers in Aging Neuroscience, 9, 92. doi: 10.3389/fnagi.2017.00092Google Scholar
Franke, K., Gaser, C., & Alzheimer’s Disease Neuroimaging Initiative (2012). Longitudinal changes in individual BrainAGE in healthy aging, mild cognitive impairment, and Alzheimer’s disease. GeroPsych: The Journal of Gerontopsychology and Geriatric Psychiatry, 25(4), 235245. doi: 10.1024/1662-9647/a000074Google Scholar
Franke, K., Gaser, C., Roseboom, S. R., Schwab, M., & de Rooij, T. J. (2017). Premature brain aging in humans exposed to maternal nutrient restriction during early gestation. NeuroImage, 173, 460471. doi: 10.1016/j.neuroimage.2017.10.047Google Scholar
Gale, C. R., Walton, S., & Martyn, C. N. (2003). Foetal and postnatal head growth and risk of cognitive decline in old age. Brain, 126(10), 22732278. doi: 10.1093/brain/awg225Google Scholar
Georgieff, M. K. (2007). Nutrition and the developing brain: Nutrient priorities and measurement. American Journal of Clinical Nutrition, 85(2), 614S620S. doi: 10.1093/ajcn/85.2.614SGoogle Scholar
Gil-Mohapel, J., Titterness, A. K., Patten, A. R., et al. (2014). Prenatal ethanol exposure differentially affects hippocampal neurogenesis in the adolescent and aged brain. Neuroscience, 273, 174188. doi: 10.1016/j.neuroscience.2014.05.012CrossRefGoogle ScholarPubMed
Glenn, M. J., Kirby, E. D., Gibson, E. M., et al. (2008). Age-related declines in exploratory behavior and markers of hippocampal plasticity are attenuated by prenatal choline supplementation in rats. Brain Research, 1237, 110123. doi: 10.1016/j.brainres.2008.08.049Google Scholar
Gluckman, P., & Hanson, M. (2004). Echoes of the past: Evolution, development, health and disease. Discovery Medicine, 4(24), 401407.Google Scholar
Guxens, M., Lubczynska, M. J., Muetzel, R. L., et al. (2018). Air pollution exposure during fetal life, brain morphology, and cognitive function in school-age children. Biological Psychiatry, 84(4), 295303. doi: 10.1016/j.biopsych.2018.01.016CrossRefGoogle ScholarPubMed
Haukvik, U. K., Rimol, L. M., Roddey, J. C., et al. (2014). Normal birth weight variation is related to cortical morphology across the psychosis spectrum. Schizophrenia Bulletin, 40(2), 410419. doi: 10.1093/schbul/sbt005Google Scholar
He, P., Liu, L., Salas, J. M. I., et al. (2018). Prenatal malnutrition and adult cognitive impairment: A natural experiment from the 1959–1961 Chinese famine. British Journal of Nutrition, 120(2), 198203. doi: 10.1017/s0007114518000958Google Scholar
Institute of Medicine & National Academy of Sciences (1992). Discovering the Brain. Washington: The National Academies Press.Google Scholar
Ishiwata, H., Shiga, T., & Okado, N. (2005). Selective serotonin reuptake inhibitor treatment of early postnatal mice reverses their prenatal stress-induced brain dysfunction. Neuroscience, 133(4), 893901. doi: 10.1016/j.neuroscience.2005.03.048Google Scholar
Kang, Y., Zhang, Y., Feng, Z., et al. (2017). Nutritional deficiency in early life facilitates aging-associated cognitive decline. Current Alzheimer Research, 14(8), 841849. doi: 10.2174/1567205014666170425112331Google Scholar
Katzman, R., Terry, R., DeTeresa, R., et al. (1988). Clinical, pathological, and neurochemical changes in dementia: A subgroup with preserved mental status and numerous neocortical plaques. Annals of Neurology, 23(2), 138144. doi: 10.1002/ana.410230206CrossRefGoogle ScholarPubMed
Kesse-Guyot, E., Julia, C., Andreeva, V., et al. (2015). Evidence of a cumulative effect of cardiometabolic disorders at midlife and subsequent cognitive function. Age and Ageing, 44(4), 648654. doi: 10.1093/ageing/afv053CrossRefGoogle ScholarPubMed
Koehl, M., Lemaire, V., Vallee, M., et al. (2001). Long term neurodevelopmental and behavioral effects of perinatal life events in rats. Neurotoxicity Research, 3(1), 6583. doi: 10.1007/BF03033231Google Scholar
Langley-Evans, S. C., & McMullen, S. (2010). Developmental origins of adult disease. Medical Principles and Practice, 19(2), 8798. doi: 10.1159/000273066Google Scholar
Lardenoije, R., Iatrou, A., Kenis, G., et al. (2015). The epigenetics of aging and neurodegeneration. Progress in Neurobiology, 131, 2164. doi: 10.1016/j.pneurobio.2015.05.002Google Scholar
Lemaire, V., Koehl, M., Le Moal, M., & Abrous, D. N. (2000). Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proceedings of the National Academy of Sciences USA, 97(20), 1103211037. doi: 10.1073/pnas.97.20.11032CrossRefGoogle ScholarPubMed
Li, J., Na, L., Ma, H., et al. (2015). Multigenerational effects of parental prenatal exposure to famine on adult offspring cognitive function. Scientific Reports, 5, 13792. doi: 10.1038/srep13792CrossRefGoogle ScholarPubMed
Liu, J., Lester, B. M., Neyzi, N., et al. (2013). Regional brain morphometry and impulsivity in adolescents following prenatal exposure to cocaine and tobacco. JAMA Pediatrics, 167(4), 348354. doi: 10.1001/jamapediatrics.2013.550CrossRefGoogle ScholarPubMed
Loomans, E. M., van der Stelt, O., van Eijsden, M., et al. (2012). High levels of antenatal maternal anxiety are associated with altered cognitive control in five-year-old children. Developmental Psychobiology, 54(4), 441450. doi: 10.1002/dev.20606Google Scholar
Lordi, B., Protais, P., Mellier, D., & Caston, J. (1997). Acute stress in pregnant rats: Effects on growth rate, learning, and memory capabilities of the offspring. Physiology and Behavior, 62(5), 10871092. doi: 10.1016/s0031-9384(97)00261-8Google Scholar
Markham, A., Bains, R., Franklin, P., & Spedding, M. (2014). Changes in mitochondrial function are pivotal in neurodegenerative and psychiatric disorders: How important is BDNF? British Journal of Pharmacology, 171(8), 22062229. doi: 10.1111/bph.12531CrossRefGoogle ScholarPubMed
Martinussen, M., Flanders, D. W., Fischl, B., et al. (2009). Segmental brain volumes and cognitive and perceptual correlates in 15-year-old adolescents with low birth weight. Journal of Pediatrics, 155(6), 848853. doi: 10.1016/j.jpeds.2009.06.015CrossRefGoogle ScholarPubMed
Martyn, C. N., Gale, C. R., Sayer, A. A., & Fall, C. (1996). Growth in utero and cognitive function in adult life: Follow up study of people born between 1920 and 1943. BMJ, 312(7043), 13931396. doi: 10.1136/bmj.312.7043.1393aGoogle Scholar
McGaughy, J. A., Amaral, A. C., Rushmore, R. J., et al. (2014). Prenatal malnutrition leads to deficits in attentional set shifting and decreases metabolic activity in prefrontal subregions that control executive function. Developmental Neuroscience, 36(6), 532541. doi: 10.1159/000366057Google Scholar
Meng, X., & D’Arcy, C. (2012). Education and dementia in the context of the cognitive reserve hypothesis: A systematic review with meta-analyses and qualitative analyses. PLoS One, 7(6), e38268. doi: 10.1371/journal.pone.0038268Google Scholar
Merlot, E., Couret, D., & Otten, W. (2008). Prenatal stress, fetal imprinting and immunity. Brain, Behavior and Immunity, 22(1), 4251. doi: 10.1016/j.bbi.2007.05.007CrossRefGoogle ScholarPubMed
Morava, E., & Kozicz, T. (2013). Mitochondria and the economy of stress (mal)adaptation. Neuroscience and Biobehavioral Reviews, 37(4), 668680. doi: 10.1016/j.neubiorev.2013.02.005CrossRefGoogle ScholarPubMed
Muller, M., Sigurdsson, S., Kjartansson, O., et al. (2014). Birth size and brain function 75 years later. Pediatrics, 134(4), 761770. doi: 10.1542/peds.2014-1108Google Scholar
Naninck, E. F., Oosterink, J. E., Yam, K. Y., et al. (2017). Early micronutrient supplementation protects against early stress-induced cognitive impairments. FASEB Journal, 31(2), 505518. doi: 10.1096/fj.201600834RGoogle Scholar
Odberg, M. D., Aukland, S. M., Rosendahl, K., & Elgen, I. B. (2010). Cerebral MRI and cognition in nonhandicapped, low birth weight adults. Pediatric Neurology, 43(4), 258262. doi: 10.1016/j.pediatrneurol.2010.05.014Google Scholar
Orozco-Solis, R., Matos, R. J., Guzman-Quevedo, O., et al. (2010). Nutritional programming in the rat is linked to long-lasting changes in nutrient sensing and energy homeostasis in the hypothalamus. PLoS One, 5(10), e13537. doi: 10.1371/journal.pone.0013537Google Scholar
Ozanne, S. (2014). Nutrigenomic programming of cardiovascular and metabolic diseases. Free Radical Biology and Medicine, 75 (Suppl. 1), 11. doi: 10.1016/j.freeradbiomed.2014.10.857Google Scholar
Phillips, C. (2017). Lifestyle modulators of neuroplasticity: How physical activity, mental engagement, and diet promote cognitive health during aging. Neural Plasticity, 2017, 3589271. doi: 10.1155/2017/3589271Google Scholar
Raikkonen, K., Kajantie, E., Pesonen, A. K., et al. (2013). Early life origins cognitive decline: Findings in elderly men in the Helsinki Birth Cohort Study. PLoS One, 8(1), e54707. doi: 10.1371/journal.pone.0054707Google Scholar
Reynolds, M. D., Johnston, J. M., Dodge, H. H., DeKosky, S. T., & Ganguli, M. (1999). Small head size is related to low Mini-Mental State Examination scores in a community sample of nondemented older adults. Neurology, 53(1), 228229. doi: 10.1212/wnl.53.1.228Google Scholar
Rodriguez, J. S., Bartlett, T. Q., Keenan, K. E., Nathanielsz, P. W., & Nijland, M. J. (2012). Sex-dependent cognitive performance in baboon offspring following maternal caloric restriction in pregnancy and lactation. Reproductive Sciences, 19(5), 493504. doi: 10.1177/1933719111424439Google Scholar
Roseboom, T. J., Painter, R. C., van Abeelen, A. F., Veenendaal, M. V., & de Rooij, S. R. (2011). Hungry in the womb: What are the consequences? Lessons from the Dutch famine. Maturitas, 70(2), 141145. doi: 10.1016/j.maturitas.2011.06.017Google Scholar
Satz, P. (1993). Brain reserve capacity on symptom onset after brain injury: A formulation and review of evidence for threshold theory. Neuropsychology, 7, 273295. doi: 10.1037/0894-4105.7.3.273Google Scholar
Shenkin, S. D., Rivers, C. S., Deary, I. J., Starr, J. M., & Wardlaw, J. M. (2009). Maximum (prior) brain size, not atrophy, correlates with cognition in community-dwelling older people: A cross-sectional neuroimaging study. BMC Geriatrics, 9, 12. doi: 10.1186/1471-2318-9-12Google Scholar
Shenkin, S. D., Starr, J. M., & Deary, I. J. (2004). Birth weight and cognitive ability in childhood: A systematic review. Psychological Bulletin, 130(6), 9891013. doi: 10.1037/0033-2909.130.6.989Google Scholar
Sierksma, A. S., Prickaerts, J., Chouliaras, L., et al. (2013). Behavioral and neurobiological effects of prenatal stress exposure in male and female APPswe/PS1dE9 mice. Neurobiology of Aging, 34(1), 319337. doi: 10.1016/j.neurobiolaging.2012.05.012CrossRefGoogle ScholarPubMed
Stern, Y. (2009). Cognitive reserve. Neuropsychologia, 47(10), 20152028. doi: 10.1016/j.neuropsychologia.2009.03.004Google Scholar
Stern, Y. (2012). Cognitive reserve in ageing and Alzheimer’s disease. Lancet Neurology, 11(11), 10061012. doi: 10.1016/s1474-4422(12)70191-6Google Scholar
Swaab, D. F., & Bao, A. M. (2011). (Re-)activation of neurons in aging and dementia: Lessons from the hypothalamus. Experimental Gerontology, 46(2–3), 178184. doi: 10.1016/j.exger.2010.08.028Google Scholar
Vallee, M., MacCari, S., Dellu, F., et al. (1999). Long-term effects of prenatal stress and postnatal handling on age-related glucocorticoid secretion and cognitive performance: A longitudinal study in the rat. European Journal of Neuroscience, 11(8), 29062916. doi: 10.1046/j.1460-9568.1999.00705.xCrossRefGoogle ScholarPubMed
van Abeelen, A. F., Veenendaal, M. V., Painter, R. C., et al. (2012). Survival effects of prenatal famine exposure. American Journal of Clinical Nutrition, 95(1), 179183. doi: 10.3945/ajcn.111.022038Google Scholar
Van den Bergh, B. R., Mennes, M., Oosterlaan, J., et al. (2005). High antenatal maternal anxiety is related to impulsivity during performance on cognitive tasks in 14- and 15-year-olds. Neuroscience and Biobehavioral Reviews, 29(2), 259269. doi: 10.1016/j.neubiorev.2004.10.010Google Scholar
Van den Bergh, B. R. H., van den Heuvel, M. I., Lahti, M., et al. (2017). Prenatal developmental origins of behavior and mental health: The influence of maternal stress in pregnancy. Neuroscience and Biobehavioral Reviews. doi: 10.1016/j.neubiorev.2017.07.003Google Scholar
Walhovd, K. B., Krogsrud, S. K., Amlien, I. K., et al. (2016). Neurodevelopmental origins of lifespan changes in brain and cognition. Proceedings of the National Academy of Sciences USA, 113(33), 93579362. doi: 10.1073/pnas.1524259113Google Scholar
Wang, C., An, Y., Yu, H., et al. (2016). Association between exposure to the Chinese famine in different stages of early life and decline in cognitive functioning in adulthood. Frontiers in Behavioral Neuroscience, 10, 146. doi: 10.3389/fnbeh.2016.00146Google Scholar
Weinstock, M. (2011). Sex-dependent changes induced by prenatal stress in cortical and hippocampal morphology and behaviour in rats: An update. Stress, 14(6), 604613. doi: 10.3109/10253890.2011.588294Google Scholar
World Health Organization (2019). Dementia. www.who.int/news-room/fact-sheets/detail/dementiaGoogle Scholar
Xu, H., Zhang, Z., Li, L., & Liu, J. (2018). Early life exposure to China’s 1959–61 famine and midlife cognition. International Journal of Epidemiology, 47(1), 109120. doi: 10.1093/ije/dyx222Google Scholar
Zheng, A., Li, H., Cao, K., et al. (2015). Maternal hydroxytyrosol administration improves neurogenesis and cognitive function in prenatally stressed offspring. Journal of Nutritional Biochemistry, 26(2), 190199. doi: 10.1016/j.jnutbio.2014.10.006Google Scholar

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