Temporally and sex-specific effects of maternal perinatal stress on offspring cortical gyrification and mood in young adulthood
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
European Union: Marie Curie Intra-European Fellowship for Career Development FP7-IEF-2013) Ministry of Education, Youth and Sports of the Czech Republic: CEITEC 2020, LQ1601, LM201812, LM2015062, LM2018129. CAMH Foundation: Koerner New Scientist Award, Discovery Fund Postdoctoral Fellowship.
PubMed
33010202
PubMed Central
PMC7643354
DOI
10.1002/hbm.25163
Knihovny.cz E-zdroje
- Klíčová slova
- dysregulated mood, gyrification, magnetic resonance imaging, perinatal stress, prenatal birth cohort, sex, young adulthood,
- MeSH
- afektivní symptomy * diagnostické zobrazování etiologie patologie patofyziologie MeSH
- dospělí MeSH
- emoční regulace fyziologie MeSH
- kojenec MeSH
- lidé MeSH
- longitudinální studie MeSH
- magnetická rezonanční tomografie MeSH
- mladý dospělý MeSH
- mozková kůra * diagnostické zobrazování patologie patofyziologie MeSH
- novorozenec MeSH
- poporodní období MeSH
- psychický stres komplikace MeSH
- těhotenství MeSH
- zpožděný efekt prenatální expozice * diagnostické zobrazování etiologie patologie patofyziologie MeSH
- Check Tag
- dospělí MeSH
- kojenec MeSH
- lidé MeSH
- mladý dospělý MeSH
- mužské pohlaví MeSH
- novorozenec MeSH
- těhotenství MeSH
- ženské pohlaví MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Maternal stress during pregnancy and shortly thereafter is associated with altered offspring brain development that may increase risk of mood and anxiety disorders. Cortical gyrification is established during the prenatal period and the first 2 years of life and is altered in psychiatric disorders. Here, we sought to characterize the effects of perinatal stress exposure on offspring gyrification patterns and mood dysregulation in young adulthood. Participants included 85 young adults (56.5% women; 23-24 years) from the European Longitudinal Study of Pregnancy and Childhood (ELSPAC) with perinatal stress data across four distinct timepoints and structural MRI data from young adulthood. Perinatal stress exposure was measured as maternal stress during first and second half of pregnancy, first 6 months, and 6-18 months after birth. Cortical gyrification and mood dysregulation were quantified using local gyrification index (LGI), computed with Freesurfer, and the Profile of Mood States questionnaire, respectively. Perinatal stress predicted cortical gyrification in young adulthood, and its timing influenced location, direction, and sex-specificity of effects. In particular, whereas early prenatal stress was associated with sex-dependent medium-to-large effects in large temporal, parietal, and occipital regions (f2 = 0.19-0.38, p < .001), later perinatal stress was associated with sex-independent small-to-medium effects in smaller, more anterior regions (f2 = 0.10-0.19, p < .003). Moreover, in females, early prenatal stress predicted higher LGI in a large temporal region, which was further associated with mood disturbance in adulthood (r = 0.399, p = .006). These findings point out the long-term implications of perinatal stress exposure for cortical morphology and mood dysregulation.
Department of Psychiatry University of Toronto Toronto Ontario Canada
RECETOX Faculty of Science Masaryk University Brno Czech Republic
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Acosta, H. , Tuulari, J. J. , Scheinin, N. M. , Hashempour, N. , Rajasilta, O. , Lavonius, T. I. , … Karlsson, H. (2019). Maternal pregnancy‐related anxiety is associated with sexually dimorphic alterations in amygdala volume in 4‐year‐old children. Frontiers in Behavioral Neuroscience, 13, 175 10.3389/fnbeh.2019.00175 PubMed DOI PMC
Andersen, S. L. , & Teicher, M. H. (2004). Delayed effects of early stress on hippocampal development. Neuropsychopharmacology, 29(11), 1988–1993. 10.1038/sj.npp.1300528 PubMed DOI
Andersen, S. L. , & Teicher, M. H. (2008). Stress, sensitive periods and maturational events in adolescent depression. Trends in Neurosciences, 31(4), 183–191. 10.1016/j.tins.2008.01.004 PubMed DOI
Armstrong, E. , Schleicher, A. , Omran, H. , Curtis, M. , & Zilles, K. (1995). The ontogeny of human gyrification. Cerebral Cortex, 5(1), 56–63. 10.1093/cercor/5.1.56 PubMed DOI
Barrett, E. S. , Redmon, J. B. , Wang, C. , Sparks, A. , & Swan, S. H. (2014). Exposure to prenatal life events stress is associated with masculinized play behavior in girls. Neurotoxicology, 41, 20–27. 10.1016/j.neuro.2013.12.011 PubMed DOI PMC
Behan, A. T. , van den Hove, D. L. , Mueller, L. , Jetten, M. J. , Steinbusch, H. W. , Cotter, D. R. , & Prickaerts, J. (2011). Evidence of female‐specific glial deficits in the hippocampus in a mouse model of prenatal stress. European Neuropsychopharmacology, 21(1), 71–79. 10.1016/j.euroneuro.2010.07.004 PubMed DOI
Bock, J. , Gruss, M. , Becker, S. , & Braun, K. (2005). Experience‐induced changes of dendritic spine densities in the prefrontal and sensory cortex: Correlation with developmental time windows. Cerebral Cortex, 15(6), 802–808. 10.1093/cercor/bhh181 PubMed DOI
Bock, J. , Wainstock, T. , Braun, K. , & Segal, M. (2015). Stress in utero: Prenatal programming of brain plasticity and cognition. Biological Psychiatry, 78(5), 315–326. 10.1016/j.biopsych.2015.02.036 PubMed DOI
Bowman, R. E. , MacLusky, N. J. , Sarmiento, Y. , Frankfurt, M. , Gordon, M. , & Luine, V. N. (2004). Sexually dimorphic effects of prenatal stress on cognition, hormonal responses, and central neurotransmitters. Endocrinology, 145(8), 3778–3787. 10.1210/en.2003-1759 PubMed DOI
Brown, A. S. , van Os, J. , Driessens, C. , Hoek, H. W. , & Susser, E. S. (2000). Further evidence of relation between prenatal famine and major affective disorder. The American Journal of Psychiatry, 157(2), 190–195. 10.1176/appi.ajp.157.2.190 PubMed DOI
Buss, C. , Davis, E. P. , Class, Q. A. , Gierczak, M. , Pattillo, C. , Glynn, L. M. , & Sandman, C. A. (2009). Maturation of the human fetal startle response: Evidence for sex‐specific maturation of the human fetus. Early Human Development, 85(10), 633–638. 10.1016/j.earlhumdev.2009.08.001 PubMed DOI PMC
Buss, C. , Davis, E. P. , Muftuler, L. T. , Head, K. , & Sandman, C. A. (2010). High pregnancy anxiety during mid‐gestation is associated with decreased gray matter density in 6‐9‐year‐old children. Psychoneuroendocrinology, 35(1), 141–153. 10.1016/j.psyneuen.2009.07.010 PubMed DOI PMC
Buss, C. , Entringer, S. , Swanson, J. M. , & Wadhwa, P. D. (2012). The role of stress in brain development: The gestational Environment's long‐term effects on the brain. Cerebrum, 2012, 4. PubMed PMC
Cao, B. , Mwangi, B. , Passos, I. C. , Wu, M. J. , Keser, Z. , Zunta‐Soares, G. B. , … Soares, J. C. (2017). Lifespan gyrification trajectories of human brain in healthy individuals and patients with major psychiatric disorders. Scientific Reports, 7(1), 511 10.1038/s41598-017-00582-1 PubMed DOI PMC
Chi, J. G. , Dooling, E. C. , & Gilles, F. H. (1977). Gyral development of the human brain. Annals of Neurology, 1(1), 86–93. 10.1002/ana.410010109 PubMed DOI
Clifton, V. L. (2010). Review: Sex and the human placenta: Mediating differential strategies of fetal growth and survival. Placenta, 31(31 Suppl), S33–S39. 10.1016/j.placenta.2009.11.010 PubMed DOI
Dale, A. M. , Fischl, B. , & Sereno, M. I. (1999). Cortical surface‐based analysis. I. Segmentation and surface reconstruction. NeuroImage, 9(2), 179–194. 10.1006/nimg.1998.0395 PubMed DOI
Depping, M. S. , Thomann, P. A. , Wolf, N. D. , Vasic, N. , Sosic‐Vasic, Z. , Schmitgen, M. M. , … Wolf, R. C. (2018). Common and distinct patterns of abnormal cortical gyrification in major depression and borderline personality disorder. European Neuropsychopharmacology, 28(10), 1115–1125. 10.1016/j.euroneuro.2018.07.100 PubMed DOI
DiPietro, J. A. , & Voegtline, K. M. (2017). The gestational foundation of sex differences in development and vulnerability. Neuroscience, 342, 4–20. 10.1016/j.neuroscience.2015.07.068 PubMed DOI PMC
Fish, A. M. , Cachia, A. , Fischer, C. , Mankiw, C. , Reardon, P. K. , Clasen, L. S. , … Raznahan, A. (2017). Influences of brain size, sex, and sex chromosome complement on the architecture of human cortical folding. Cerebral Cortex, 27(12), 5557–5567. 10.1093/cercor/bhw323 PubMed DOI PMC
Ganella, E. P. , Burnett, A. , Cheong, J. , Thompson, D. , Roberts, G. , Wood, S. , … Bartholomeusz, C. (2015). Abnormalities in orbitofrontal cortex gyrification and mental health outcomes in adolescents born extremely preterm and/or at an extremely low birth weight. Human Brain Mapping, 36(3), 1138–1150. 10.1002/hbm.22692 PubMed DOI PMC
Garthus‐Niegel, S. , Ayers, S. , Martini, J. , von Soest, T. , & Eberhard‐Gran, M. (2017). The impact of postpartum post‐traumatic stress disorder symptoms on child development: A population‐based, 2‐year follow‐up study. Psychological Medicine, 47(1), 161–170. 10.1017/s003329171600235x PubMed DOI
Gilman, S. E. , Cherkerzian, S. , Buka, S. L. , Hahn, J. , Hornig, M. , & Goldstein, J. M. (2016). Prenatal immune programming of the sex‐dependent risk for major depression. Translational Psychiatry, 6(5), e822 10.1038/tp.2016.91 PubMed DOI PMC
Gilmore, J. H. , Schmitt, J. E. , Knickmeyer, R. C. , Smith, J. K. , Lin, W. , Styner, M. , … Neale, M. C. (2010). Genetic and environmental contributions to neonatal brain structure: A twin study. Human Brain Mapping, 31(8), 1174–1182. 10.1002/hbm.20926 PubMed DOI PMC
Goldstein, J. M. , Hale, T. , Foster, S. L. , Tobet, S. A. , & Handa, R. J. (2019). Sex differences in major depression and comorbidity of cardiometabolic disorders: Impact of prenatal stress and immune exposures. Neuropsychopharmacology, 44(1), 59–70. 10.1038/s41386-018-0146-1 PubMed DOI PMC
Graham, A. M. , Rasmussen, J. M. , Entringer, S. , Ben Ward, E. , Rudolph, M. D. , Gilmore, J. H. , … Buss, C. (2019). Maternal cortisol concentrations during pregnancy and sex‐specific associations with neonatal amygdala connectivity and emerging internalizing behaviors. Biological Psychiatry, 85(2), 172–181. 10.1016/j.biopsych.2018.06.023 PubMed DOI PMC
Han, K. M. , Won, E. , Kang, J. , Kim, A. , Yoon, H. K. , Chang, H. S. , … Ham, B. J. (2017). Local gyrification index in patients with major depressive disorder and its association with tryptophan hydroxylase‐2 (TPH2) polymorphism. Human Brain Mapping, 38(3), 1299–1310. 10.1002/hbm.23455 PubMed DOI PMC
Haukvik, U. K. , Schaer, M. , Nesvag, R. , McNeil, T. , Hartberg, C. B. , Jonsson, E. G. , … Agartz, I. (2012). Cortical folding in Broca's area relates to obstetric complications in schizophrenia patients and healthy controls. Psychological Medicine, 42(6), 1329–1337. 10.1017/s0033291711002315 PubMed DOI
Helmeke, C. , Ovtscharoff, W., Jr. , Poeggel, G. , & Braun, K. (2001). Juvenile emotional experience alters synaptic inputs on pyramidal neurons in the anterior cingulate cortex. Cerebral Cortex, 11(8), 717–727. 10.1093/cercor/11.8.717 PubMed DOI
Hogstrom, L. J. , Westlye, L. T. , Walhovd, K. B. , & Fjell, A. M. (2013). The structure of the cerebral cortex across adult life: Age‐related patterns of surface area, thickness, and gyrification. Cerebral Cortex, 23(11), 2521–2530. 10.1093/cercor/bhs231 PubMed DOI
Janssen, A. B. , Kertes, D. A. , McNamara, G. I. , Braithwaite, E. C. , Creeth, H. D. , Glover, V. I. , & John, R. M. (2016). A role for the placenta in programming maternal mood and childhood behavioural disorders. Journal of Neuroendocrinology, 28(8). 10.1111/jne.12373 PubMed DOI PMC
Kertes, D. A. , Kamin, H. S. , Hughes, D. A. , Rodney, N. C. , Bhatt, S. , & Mulligan, C. J. (2016). Prenatal maternal stress predicts methylation of genes regulating the hypothalamic‐pituitary‐adrenocortical system in mothers and newborns in the Democratic Republic of Congo. Child Development, 87(1), 61–72. 10.1111/cdev.12487 PubMed DOI PMC
Kesler, S. R. , Vohr, B. , Schneider, K. C. , Katz, K. H. , Makuch, R. W. , Reiss, A. L. , & Ment, L. R. (2006). Increased temporal lobe gyrification in preterm children. Neuropsychologia, 44(3), 445–453. 10.1016/j.neuropsychologia.2005.05.015 PubMed DOI
Kessler, R. C. , Berglund, P. , Demler, O. , Jin, R. , Merikangas, K. R. , & Walters, E. E. (2005). Lifetime prevalence and age‐of‐onset distributions of DSM‐IV disorders in the National Comorbidity Survey Replication. Archives of General Psychiatry, 62(6), 593–602. 10.1001/archpsyc.62.6.593 PubMed DOI
Kinney, D. K. , Munir, K. M. , Crowley, D. J. , & Miller, A. M. (2008). Prenatal stress and risk for autism. Neuroscience and Biobehavioral Reviews, 32(8), 1519–1532. 10.1016/j.neubiorev.2008.06.004 PubMed DOI PMC
Kornstein, S. G. , Schatzberg, A. F. , Thase, M. E. , Yonkers, K. A. , McCullough, J. P. , Keitner, G. I. , … Keller, M. B. (2000). Gender differences in chronic major and double depression. Journal of Affective Disorders, 60(1), 1–11. PubMed
Li, G. , Wang, L. , Shi, F. , Lyall, A. E. , Lin, W. , Gilmore, J. H. , & Shen, D. (2014). Mapping longitudinal development of local cortical Gyrification in infants from birth to 2 years of age. The Journal of Neuroscience, 34, 4228–4238. PubMed PMC
Li, G. , Nie, J. , Shi, F. , Lin, W. , Gilmore, J. H. , & Shen, D. (2013). Mapping region‐specific longitudinal cortical surface expansion from birth to 2 years of age. Cerebral Cortex, 23, 2724–2733. PubMed PMC
Lupien, S. J. (2009). Brains under stress. Canadian Journal of Psychiatry, 54(1), 4–5. 10.1177/070674370905400103 PubMed DOI
Mareckova, K. , Klasnja, A. , Andryskova, L. , Brazdil, M. , & Paus, T. (2019). Developmental origins of depression‐related white matter properties: Findings from a prenatal birth cohort. Human Brain Mapping, 40(4), 1155–1163. 10.1002/hbm.24435 PubMed DOI PMC
Mareckova, K. , Klasnja, A. , Bencurova, P. , Andryskova, L. , Brazdil, M. , & Paus, T. (2019). Prenatal stress, mood, and gray matter volume in young adulthood. Cerebral Cortex, 29(3), 1244–1250. 10.1093/cercor/bhy030 PubMed DOI PMC
Maselko, J. , Sikander, S. , Bhalotra, S. , Bangash, O. , Ganga, N. , Mukherjee, S. , … Rahman, A. (2015). Effect of an early perinatal depression intervention on long‐term child development outcomes: Follow‐up of the thinking healthy Programme randomised controlled trial. Lancet Psychiatry, 2(7), 609–617. 10.1016/s2215-0366(15)00109-1 PubMed DOI
McNair, D. M. , Lorr, M. , & Droppleman, L. F. (1971). Manual for the profile of mood states. San Diego, CA: Educational and Industrial Testing Services.
Molent, C. , Maggioni, E. , Cecchetto, F. , Garzitto, M. , Piccin, S. , Bonivento, C. , … Brambilla, P. (2018). Reduced cortical thickness and increased gyrification in generalized anxiety disorder: A 3 T MRI study. Psychological Medicine, 48(12), 2001–2010. 10.1017/s003329171700352x PubMed DOI
Monroy, E. , Hernandez‐Torres, E. , & Flores, G. (2010). Maternal separation disrupts dendritic morphology of neurons in prefrontal cortex, hippocampus, and nucleus accumbens in male rat offspring. Journal of Chemical Neuroanatomy, 40(2), 93–101. 10.1016/j.jchemneu.2010.05.005 PubMed DOI
Nathanielsz, P. W. , Berghorn, K. A. , Derks, J. B. , Giussani, D. A. , Docherty, C. , Unno, N. , … Nijland, M. J. (2003). Life before birth: Effects of cortisol on future cardiovascular and metabolic function. Acta Paediatrica, 92(7), 766–772. PubMed
Nishikuni, K. , & Ribas, G. C. (2013). Study of fetal and postnatal morphological development of the brain sulci. Journal of Neurosurgery. Pediatrics, 11(1), 1–11. 10.3171/2012.9.peds12122 PubMed DOI
Nixon, N. L. , Liddle, P. F. , Nixon, E. , Worwood, G. , Liotti, M. , & Palaniyappan, L. (2014). Biological vulnerability to depression: Linked structural and functional brain network findings. The British Journal of Psychiatry, 204, 283–289. 10.1192/bjp.bp.113.129965 PubMed DOI
Nyenhuis, D. L. , Yamamoto, C. , Luchetta, T. , Terrien, A. , & Parmentier, A. (1999). Adult and geriatric normative data and validation of the profile of mood states. Journal of Clinical Psychology, 55(1), 79–86. https://doi.org/10.1002/(sici)1097-4679(199901)55:1<79::aid-jclp8>3.0.co;2-7 PubMed
O'Connor, T. G. , Heron, J. , Golding, J. , & Glover, V. (2003). Maternal antenatal anxiety and behavioural/emotional problems in children: A test of a programming hypothesis. Journal of Child Psychology and Psychiatry, 44(7), 1025–1036. 10.1111/1469-7610.00187 PubMed DOI
Papini, C. , Palaniyappan, L. , Kroll, J. , Froudist‐Walsh, S. , Murray, R. M. , & Nosarti, C. (2020). Altered cortical Gyrification in adults who were born very preterm and its associations with cognition and mental health. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 5, 640–650. 10.1016/j.bpsc.2020.01.006 PubMed DOI
Pearson, R. M. , Evans, J. , Kounali, D. , Lewis, G. , Heron, J. , Ramchandani, P. G. , … Stein, A. (2013). Maternal depression during pregnancy and the postnatal period: Risks and possible mechanisms for offspring depression at age 18 years. JAMA Psychiatry, 70(12), 1312–1319. 10.1001/jamapsychiatry.2013.2163 PubMed DOI PMC
Peng, D. , Shi, F. , Li, G. , Fralick, D. , Shen, T. , Qiu, M. , … Fang, Y. (2015). Surface vulnerability of cerebral cortex to major depressive disorder. PLoS One, 10(3), e0120704 10.1371/journal.pone.0120704 PubMed DOI PMC
Piler, P. , Kandrnal, V. , Kukla, L. , Andryskova, L. , Svancara, J. , Jarkovsky, J. , … Klanova, J. (2017). Cohort profile: The European longitudinal study of pregnancy and childhood (ELSPAC) in The Czech Republic. International Journal of Epidemiology, 46(5), 1379–1379f. 10.1093/ije/dyw091 PubMed DOI PMC
Pinzon‐Parra, C. , Vidal‐Jimenez, B. , Camacho‐Abrego, I. , Flores‐Gomez, A. A. , Rodriguez‐Moreno, A. , & Flores, G. (2019). Juvenile stress causes reduced locomotor behavior and dendritic spine density in the prefrontal cortex and basolateral amygdala in Sprague‐Dawley rats. Synapse, 73(1), e22066 10.1002/syn.22066 PubMed DOI
Prenoveau, J. M. , Craske, M. G. , West, V. , Giannakakis, A. , Zioga, M. , Lehtonen, A. , … Stein, A. (2017). Maternal postnatal depression and anxiety and their association with child emotional negativity and behavior problems at two years. Developmental Psychology, 53(1), 50–62. 10.1037/dev0000221 PubMed DOI PMC
Pryce, C. R. , Aubert, Y. , Maier, C. , Pearce, P. C. , & Fuchs, E. (2011). The developmental impact of prenatal stress, prenatal dexamethasone and postnatal social stress on physiology, behaviour and neuroanatomy of primate offspring: Studies in rhesus macaque and common marmoset. Psychopharmacology, 214(1), 33–53. 10.1007/s00213-010-1989-2 PubMed DOI PMC
Rakic, P. (2009). Evolution of the neocortex: A perspective from developmental biology. Nature Reviews. Neuroscience, 10(10), 724–735. 10.1038/nrn2719 PubMed DOI PMC
Raznahan, A. , Shaw, P. , Lalonde, F. , Stockman, M. , Wallace, G. L. , Greenstein, D. , … Giedd, J. N. (2011). How does your cortex grow? The Journal of Neuroscience, 31(19), 7174–7177. 10.1523/jneurosci.0054-11.2011 PubMed DOI PMC
Rubin, L. P. (2016). Maternal and pediatric health and disease: Integrating biopsychosocial models and epigenetics. Pediatric Research, 79(1–2), 127–135. 10.1038/pr.2015.203 PubMed DOI
Sandman, C. A. , Davis, E. P. , Buss, C. , & Glynn, L. M. (2012). Exposure to prenatal psychobiological stress exerts programming influences on the mother and her fetus. Neuroendocrinology, 95(1), 7–21. 10.1159/000327017 PubMed DOI PMC
Schaer, M. , Cuadra, M. B. , Tamarit, L. , Lazeyras, F. , Eliez, S. , & Thiran, J. P. (2008). A surface‐based approach to quantify local cortical gyrification. IEEE Transactions on Medical Imaging, 27(2), 161–170. 10.1109/tmi.2007.903576 PubMed DOI
Scheinost, D. , Sinha, R. , Cross, S. N. , Kwon, S. H. , Sze, G. , Constable, R. T. , & Ment, L. R. (2017). Does prenatal stress alter the developing connectome? Pediatric Research, 81(1–2), 214–226. 10.1038/pr.2016.197 PubMed DOI PMC
Schmitgen, M. M. , Depping, M. S. , Bach, C. , Wolf, N. D. , Kubera, K. M. , Vasic, N. , … Wolf, R. C. (2019). Aberrant cortical neurodevelopment in major depressive disorder. Journal of Affective Disorders, 243, 340–347. 10.1016/j.jad.2018.09.021 PubMed DOI
Schroeder, M. , Sultany, T. , & Weller, A. (2013). Prenatal stress effects on emotion regulation differ by genotype and sex in prepubertal rats. Developmental Psychobiology, 55(2), 176–192. 10.1002/dev.21010 PubMed DOI
Sun, T. , & Hevner, R. F. (2014). Growth and folding of the mammalian cerebral cortex: From molecules to malformations. Nature Reviews. Neuroscience, 15(4), 217–232. 10.1038/nrn3707 PubMed DOI PMC
Tabachnick, B. G. , & Fidell, L. S. (2000). Using multivariate statistics (4th ed.). Needham Heights, MA: Allyn & Bacon.
Teicher, M. H. , Samson, J. A. , Polcari, A. , & McGreenery, C. E. (2006). Sticks, stones, and hurtful words: Relative effects of various forms of childhood maltreatment. The American Journal of Psychiatry, 163(6), 993–1000. 10.1176/ajp.2006.163.6.993 PubMed DOI
Teicher, M. H. , Tomoda, A. , & Andersen, S. L. (2006). Neurobiological consequences of early stress and childhood maltreatment: Are results from human and animal studies comparable? Annals of the new York Academy of Sciences, 1071, 313–323. 10.1196/annals.1364.024 PubMed DOI
van Os, J. , Jones, P. , Lewis, G. , Wadsworth, M. , & Murray, R. (1997). Developmental precursors of affective illness in a general population birth cohort. Archives of General Psychiatry, 54(7), 625–631. PubMed
Watson, J. B. , Mednick, S. A. , Huttunen, M. , & Wang, X. (1999). Prenatal teratogens and the development of adult mental illness. Development and Psychopathology, 11(3), 457–466. PubMed
Weinberg . (2001). Yeo‐Johnson power transformations.
Weinstock, M. (2007). Gender differences in the effects of prenatal stress on brain development and behaviour. Neurochemical Research, 32(10), 1730–1740. 10.1007/s11064-007-9339-4 PubMed DOI
Wen, D. J. , Poh, J. S. , Ni, S. N. , Chong, Y. S. , Chen, H. , Kwek, K. , … Qiu, A. (2017). Influences of prenatal and postnatal maternal depression on amygdala volume and microstructure in young children. Translational Psychiatry, 7(4), e1103 10.1038/tp.2017.74 PubMed DOI PMC
White, T. , Su, S. , Schmidt, M. , Kao, C. Y. , & Sapiro, G. (2010). The development of gyrification in childhood and adolescence. Brain and Cognition, 72(1), 36–45. 10.1016/j.bandc.2009.10.009 PubMed DOI PMC
Yong Ping, E. , Laplante, D. P. , Elgbeili, G. , Hillerer, K. M. , Brunet, A. , O'Hara, M. W. , & King, S. (2015). Prenatal maternal stress predicts stress reactivity at 2(1/2) years of age: The Iowa flood study. Psychoneuroendocrinology, 56, 62–78. 10.1016/j.psyneuen.2015.02.015 PubMed DOI
Zhang, Y. , Inder, T. E. , Neil, J. J. , Dierker, D. L. , Alexopoulos, D. , Anderson, P. J. , & Van Essen, D. C. (2015). Cortical structural abnormalities in very preterm children at 7 years of age. NeuroImage, 109, 469–479. 10.1016/j.neuroimage.2015.01.005 PubMed DOI PMC
Zhang, Y. , Yu, C. , Zhou, Y. , Li, K. , Li, C. , & Jiang, T. (2009). Decreased gyrification in major depressive disorder. Neuroreport, 20(4), 378–380. 10.1097/WNR.0b013e3283249b34 PubMed DOI
Zilles, K. , Armstrong, E. , Schleicher, A. , & Kretschmann, H. J. (1988). The human pattern of gyrification in the cerebral cortex. Anatomy and embryology (Berlin), 179(2), 173–179. PubMed
Zilles, K. , Palomero‐Gallagher, N. , & Amunts, K. (2013). Development of cortical folding during evolution and ontogeny. Trends in Neurosciences, 36(5), 275–284. 10.1016/j.tins.2013.01.006 PubMed DOI
Zilles, K. , Schleicher, A. , Langemann, C. , Amunts, K. , Morosan, P. , Palomero‐Gallagher, N. , … Roland, P. E. (1997). Quantitative analysis of sulci in the human cerebral cortex: Development, regional heterogeneity, gender difference, asymmetry, intersubject variability and cortical architecture. Human Brain Mapping, 5(4), 218–221. https://doi.org/10.1002/(sici)1097-0193(1997)5:4<218::aid-hbm2>3.0.co;2-6 PubMed
Prenatal stress and its association with amygdala-related structural covariance patterns in youth