Effects of Prenatal Stress on Structural Brain Development and Aging in Humans

Healthy brain aging is a major determinant of quality of life, allowing integration into society at all ages. Human epidemiological and animal studies indicate that in addition to lifestyle and genetic factors, environmental influences in prenatal life have a major impact on brain aging and age-associated brain disorders. The aim of this review is to summarize the existing literature on the consequences of maternal anxiety, stress, and malnutrition for structural brain aging and predisposition for age-associated brain diseases, focusing on studies with human samples. In conclusion, the results underscore the importance of a healthy mother-child relationship, starting in pregnancy, and the need for early interventions if this relationship is compromised.

[1]  M Piras,et al.  Fetal programming of the human brain: is there a link with insurgence of neurodegenerative disorders in adulthood? , 2014, Current medicinal chemistry.

[2]  P. Gluckman,et al.  Prenatal Maternal Depression Associates with Microstructure of Right Amygdala in Neonates at Birth , 2013, Biological Psychiatry.

[3]  J. Seckl,et al.  Mechanisms of Disease: glucocorticoids, their placental metabolism and fetal 'programming' of adult pathophysiology , 2007, Nature Clinical Practice Endocrinology &Metabolism.

[4]  M. Susser,et al.  Famine and Human Development: The Dutch Hunger Winter of 1944-1945 , 1975 .

[5]  Massimo Buscema,et al.  Two different Alzheimer diseases in men and women: clues from advanced neural networks and artificial intelligence. , 2005, Gender medicine.

[6]  O. Pryds,et al.  PRENATAL STRESSORS OF HUMAN LIFE AFFECT FETAL BRAIN DEVELOPMENT , 1994, Developmental medicine and child neurology.

[7]  Anqi Qiu,et al.  Antenatal maternal anxiety predicts variations in neural structures implicated in anxiety disorders in newborns. , 2015, Journal of the American Academy of Child and Adolescent Psychiatry.

[8]  P. Gluckman,et al.  Prenatal maternal depression alters amygdala functional connectivity in 6-month-old infants , 2015, Translational Psychiatry.

[9]  T. Bale,et al.  Epigenetic and transgenerational reprogramming of brain development , 2015, Nature Reviews Neuroscience.

[10]  Anqi Qiu,et al.  COMT haplotypes modulate associations of antenatal maternal anxiety and neonatal cortical morphology. , 2015, The American journal of psychiatry.

[11]  K. Lillycrop,et al.  The Effect of Nutrition during Early Life on the Epigenetic Regulation of Transcription and Implications for Human Diseases , 2012, Lifestyle Genomics.

[12]  A. Brunet,et al.  Disaster-related prenatal maternal stress influences birth outcomes: project Ice Storm. , 2011, Early human development.

[13]  Oliver J. Rando,et al.  I’m Eating for Two: Parental Dietary Effects on Offspring Metabolism , 2015, Cell.

[14]  A. Charil,et al.  Prenatal stress and brain development , 2010, Brain Research Reviews.

[15]  Anqi Qiu,et al.  Birth weight and gestation influence striatal morphology and motor response in normal six-year-old boys , 2012, NeuroImage.

[16]  A. Hofman,et al.  Prenatal folate, homocysteine and vitamin B12 levels and child brain volumes, cognitive development and psychological functioning: the Generation R Study , 2016, British Journal of Nutrition.

[17]  C. Aiken,et al.  Sex differences in developmental programming models. , 2013, Reproduction.

[18]  M Ernst,et al.  Cerebral maturation in adolescence: behavioral vulnerability. , 2009, L'Encephale.

[19]  L. Partridge,et al.  Promoting Health and Longevity through Diet: From Model Organisms to Humans , 2015, Cell.

[20]  M. Georgieff,et al.  Preterm nutrition and the brain. , 2014, World review of nutrition and dietetics.

[21]  P. Rodríguez,et al.  BDNF val66met polymorphism influences motor system function in the human brain. , 2010, Cerebral cortex.

[22]  R. Morley Nutrition and cognitive development. , 1998, Nutrition.

[23]  Bruce Fischl,et al.  Segmental brain volumes and cognitive and perceptual correlates in 15-year-old adolescents with low birth weight. , 2009, The Journal of pediatrics.

[24]  M. Catani,et al.  Prenatal stress and limbic-prefrontal white matter microstructure in children aged 6–9 years: a preliminary diffusion tensor imaging study , 2014, The world journal of biological psychiatry : the official journal of the World Federation of Societies of Biological Psychiatry.

[25]  Deanna Greenstein,et al.  Prenatal growth in humans and postnatal brain maturation into late adolescence , 2012, Proceedings of the National Academy of Sciences.

[26]  P. Gluckman,et al.  Maternal anxiety and infants' hippocampal development: timing matters , 2013, Translational Psychiatry.

[27]  Monique Ernst,et al.  Cerebral maturation in adolescence: behavioral vulnerability. , 2009, L'Encephale.

[28]  H. Baker-Henningham,et al.  Review of the evidence linking protein and energy to mental development. , 2005, Public health nutrition.

[29]  Mandyam V. Srinivasan,et al.  Scent-triggered navigation in honeybees , 2004 .

[30]  Julie Meeks Gardner,et al.  Child development: risk factors for adverse outcomes in developing countries , 2007, The Lancet.

[31]  R. S. Kahn,et al.  Prenatal exposure to famine and brain morphology in schizophrenia , 2000, Schizophrenia Research.

[32]  Francesco Amato,et al.  Importance of Multimodal MRI in Characterizing Brain Tissue and Its Potential Application for Individual Age Prediction , 2016, IEEE Journal of Biomedical and Health Informatics.

[33]  D J Barker,et al.  In utero programming of chronic disease. , 1998, Clinical science.

[34]  P. Wainwright,et al.  Nutrition and the development of cognitive functions: interpretation of behavioral studies in animals and human infants. , 2006, The American journal of clinical nutrition.

[35]  R. Westerhausen,et al.  Selectively Reduced Posterior Corpus Callosum Size in a Population-Based Sample of Young Adults Born with Low Birth Weight , 2011, American Journal of Neuroradiology.

[36]  C. Lebel,et al.  Prepartum and Postpartum Maternal Depressive Symptoms Are Related to Children’s Brain Structure in Preschool , 2016, Biological Psychiatry.

[37]  R. Harris,et al.  Early origins of adult disease: approaches for investigating the programmable epigenome in humans, nonhuman primates, and rodents. , 2012, ILAR journal.

[38]  J. Olsen,et al.  Stressful life events in pregnancy and head circumference at birth. , 2003, Developmental medicine and child neurology.

[39]  V. Gudnason,et al.  Birth Size and Brain Function 75 Years Later , 2014, Pediatrics.

[40]  Heidi Furre Østgård,et al.  Brain morphometry and cognition in young adults born small for gestational age at term. , 2014, The Journal of pediatrics.

[41]  Kate Keenan,et al.  Poor nutrition during pregnancy and lactation negatively affects neurodevelopment of the offspring: evidence from a translational primate model. , 2013, The American journal of clinical nutrition.

[42]  K. Rosendahl,et al.  Cerebral MRI and cognition in nonhandicapped, low birth weight adults. , 2010, Pediatric neurology.

[43]  S E Ozanne,et al.  Pathways linking the early environment to long-term health and lifespan. , 2011, Progress in biophysics and molecular biology.

[44]  G. Juhász,et al.  Systems biology of Alzheimer's disease: How diverse molecular changes result in memory impairment in AD , 2011, Neurochemistry International.

[45]  D. Klein,et al.  The Role of Brain-Derived Neurotrophic Factor Genotype, Parental Depression, and Relationship Discord in Predicting Early-Emerging Negative Emotionality , 2010, Psychological science.

[46]  P. Lucassen,et al.  The interplay of early-life stress, nutrition, and immune activation programs adult hippocampal structure and function , 2015, Front. Mol. Neurosci..

[47]  P. Gluckman,et al.  Brain-derived neurotrophic factor (BDNF) Val66Met polymorphism influences the association of the methylome with maternal anxiety and neonatal brain volumes , 2015, Development and Psychopathology.

[48]  D. Kurrasch,et al.  Neurodevelopmental consequences of maternal distress: what do we really know? , 2013, Clinical genetics.

[49]  Mark W. Woolrich,et al.  Benefits of multi-modal fusion analysis on a large-scale dataset: Life-span patterns of inter-subject variability in cortical morphometry and white matter microstructure , 2012, NeuroImage.

[50]  Keith M Godfrey,et al.  Cohort profile: Growing Up in Singapore Towards healthy Outcomes (GUSTO) birth cohort study. , 2014, International journal of epidemiology.

[51]  K. Godfrey,et al.  Prenatal Origins of Temperament: Fetal Growth, Brain Structure, and Inhibitory Control in Adolescence , 2014, PloS one.

[52]  Frederik Barkhof,et al.  Global and Regional Differences in Brain Anatomy of Young Children Born Small for Gestational Age , 2011, PloS one.

[53]  C. Buss,et al.  High pregnancy anxiety during mid-gestation is associated with decreased gray matter density in 6–9-year-old children , 2010, Psychoneuroendocrinology.

[54]  D. Ivanovic,et al.  Long-term effects of severe undernutrition during the first year of life on brain development and learning in Chilean high-school graduates. , 2000, Nutrition.

[55]  R. Yando,et al.  Pregnancy anxiety and comorbid depression and anger: Effects on the fetus and neonate , 2003, Depression and anxiety.

[56]  Heidi Furre Østgård,et al.  Fetal Growth, Cognitive Function, and Brain Volumes in Childhood and Adolescence , 2015, Obstetrics and gynecology.

[57]  V. Pinn,et al.  Sex and gender factors in medical studies: implications for health and clinical practice. , 2003, JAMA.

[58]  A. Gabory,et al.  Placental contribution to nutritional programming of health and diseases: epigenetics and sexual dimorphism , 2015, Journal of Experimental Biology.

[59]  Matthan W A Caan,et al.  Prenatal famine exposure has sex-specific effects on brain size. , 2016, Brain : a journal of neurology.

[60]  C. Propper,et al.  Observed parenting behaviors interact with a polymorphism of the brain-derived neurotrophic factor gene to predict the emergence of oppositional defiant and callous–unemotional behaviors at age 3 years , 2013, Development and Psychopathology.

[61]  Patrick M M Bossuyt,et al.  Survival effects of prenatal famine exposure. , 2012, The American journal of clinical nutrition.

[62]  I. Gotlib,et al.  BDNF genotype moderates the relation between physical activity and depressive symptoms. , 2010, Health psychology : official journal of the Division of Health Psychology, American Psychological Association.

[63]  J. Bronzino,et al.  Prenatal malnutrition and development of the brain , 1993, Neuroscience & Biobehavioral Reviews.

[64]  A. Clark,et al.  The brain-derived neurotrophic factor Val66Met polymorphism moderates early deprivation effects on attention problems , 2012, Development and Psychopathology.

[65]  S. Ozanne,et al.  The impact of early nutrition on the ageing trajectory , 2014, Proceedings of the Nutrition Society.

[66]  Further evidence of relation between prenatal famine and major affective disorder. , 2000, The American journal of psychiatry.

[67]  Chunshui Yu,et al.  Dosage Effects of BDNF Val66Met Polymorphism on Cortical Surface Area and Functional Connectivity , 2014, The Journal of Neuroscience.

[68]  A. Gibbons,et al.  Solving the Brain's Energy Crisis , 1998, Science.

[69]  D. Benton,et al.  The influence of children’s diet on their cognition and behavior , 2008, European journal of nutrition.

[70]  I. Loy-English,et al.  Gender differences in dementia risk factors. , 2007, Gender medicine.

[71]  R. Hunter,et al.  Neuroepigenetics of stress , 2014, Neuroscience.

[72]  C. Buss,et al.  Fetal Exposure to Maternal Depressive Symptoms Is Associated With Cortical Thickness in Late Childhood , 2015, Biological Psychiatry.

[73]  T. Paus Mapping brain maturation and cognitive development during adolescence , 2005, Trends in Cognitive Sciences.

[74]  V. Glover,et al.  Antenatal maternal stress and long-term effects on child neurodevelopment: how and why? , 2007, Journal of child psychology and psychiatry, and allied disciplines.

[75]  J. Neu Vulnerability of the fetal primate brain to moderate reduction in maternal global nutrient availability , 2011 .

[76]  J. Olsen,et al.  Maternal Psychosocial Adversity During Pregnancy Is Associated With Length of Gestation and Offspring Size at Birth: Evidence From a Population-Based Cohort Study , 2010, Psychosomatic medicine.

[77]  E. Gratacós,et al.  Brainstem and cerebellar differences and their association with neurobehavior in term small-for-gestational-age fetuses assessed by fetal MRI. , 2014, American journal of obstetrics and gynecology.

[78]  T. Roseboom,et al.  The Dutch famine and its long-term consequences for adult health. , 2006, Early human development.

[79]  Jesse S. Rodriguez,et al.  Sex-Dependent Cognitive Performance in Baboon Offspring Following Maternal Caloric Restriction in Pregnancy and Lactation , 2012, Reproductive Sciences.

[80]  Shao-Wu Zhang,et al.  Lifespan: Catch-up growth and obesity in male mice , 2004, Nature.

[81]  B. Shahbaba,et al.  Maternal cortisol over the course of pregnancy and subsequent child amygdala and hippocampus volumes and affective problems , 2012, Proceedings of the National Academy of Sciences.

[82]  S. Cramer,et al.  BDNF val66met polymorphism is associated with modified experience-dependent plasticity in human motor cortex , 2006, Nature Neuroscience.

[83]  K. Olness Effects on Brain Development Leading to Cognitive Impairment: A Worldwide Epidemic , 2003, Journal of developmental and behavioral pediatrics : JDBP.

[84]  A. Dale,et al.  Cerebral cortex thickness in 15-year-old adolescents with low birth weight measured by an automated MRI-based method. , 2005, Brain : a journal of neurology.

[85]  Hans Wouters,et al.  Prenatal undernutrition and cognitive function in late adulthood , 2010, Proceedings of the National Academy of Sciences.