Abstract
Birth is often seen as the starting point for studying effects of the environment on human development, with much research focused on the capacities of young infants. However, recent imaging advances have revealed that the complex behaviours of the fetus and the uterine environment exert influence. Birth is now viewed as a punctuate event along a developmental pathway of increasing autonomy of the child from their mother. Here we highlight (1) increasing physiological autonomy and perceptual sensitivity in the fetus, (2) physiological and neurochemical processes associated with birth that influence future behaviour, (3) the recalibration of motor and sensory systems in the newborn to adapt to the world outside the womb and (4) the effect of the prenatal environment on later infant behaviours and brain function. Taken together, these lines of evidence move us beyond nature–nurture issues to a developmental human lifespan view beginning within the womb.
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References
de Haan, M. D. H., Dumontheil, I. & Johnson, M. H. Developmental Cognitive Neuroscience: An Introduction 5th edn (Wiley, 2023).
Maccari, S. et al. Early-life experiences and the development of adult diseases with a focus on mental illness: the human birth theory. Neuroscience 342, 232–251 (2017).
Tinbergen, N. The Study of Instinct (Oxford Univ. Press, 1951).
Gottlieb, G. Social induction of malleability in ducklings: sensory basis and psychological mechanism. Anim. Behav. 45, 707–719 (1993).
Lickliter, R. & Lewkowicz, D. J. Intersensory experience and early perceptual development: attenuated prenatal sensory stimulation affects postnatal auditory and visual responsiveness in bobwhite quail chicks (Colinus virginianus). Dev. Psychol. 31, 609–618 (1995).
Lickliter, R. & Gottlieb, G. Visually imprinted maternal preference in ducklings is redirected by social interaction with siblings. Dev. Psychobiol. 19, 265–277 (1986).
Bolhuis, J. J., Johnson, M. H. & Horn, G. Effects of early experience on the development of filial preferences in the domestic chick. Dev. Psychobiol. 18, 299–308 (1985).
Spelke, E. S. & Kinzler, K. D. Core knowledge. Dev. Sci. 10, 89–96 (2007).
Fiser, J. & Aslin, R. N. Statistical learning of new visual feature combinations by infants. Proc. Natl Acad. Sci. USA 99, 15822–15826 (2002).
Prechtl, H. F. R. Continuity of Neural Functions from Prenatal to Postnatal Life (Cambridge Univ. Press, 1984).
Lickliter, R. & Bahrick, L. E. in Fetal Development: Research on Brain and Behavior, Environmental Influences, and Emerging Technologies (eds Reissland, N. & Kisilevsky, B. S.) 3–14 (Springer, 2016).
Polese, D. et al. The newborn’s reaction to light as the determinant of the brain’s activation at human birth. Front. Integr. Neurosci. 16, 933426 (2022).
Kisilvesky, B. S. & Muir, D. W. Human fetal and subsequent newborn responses to sound and vibration. Infant Behav. Dev. 14, 1–26 (1991).
Stanojevic, M., Zaputovic, S. & Bosnjak, A. P. Continuity between fetal and neonatal neurobehavior. Semin. Fetal Neonatal Med. 17, 324–329 (2012).
De Asis-Cruz, J. et al. Global network organization of the fetal functional connectome. Cereb. Cortex 31, 3034–3046 (2021).
Doria, V. et al. Emergence of resting state networks in the preterm human brain. Proc. Natl Acad. Sci. USA 107, 20015–20020 (2010).
Stiles, J. & Jernigan, T. L. The basics of brain development. Neuropsychol. Rev. 20, 327–348 (2010).
Humphreys, K. L. & Salo, V. C. Expectable environments in early life. Curr. Opin. Behav. Sci. 36, 115–119 (2020).
Mayer, C. & Joseph, K. S. Fetal growth: a review of terms, concepts and issues relevant to obstetrics. Ultrasound Obstet. Gynecol. 41, 136–145 (2013).
Iñiguez, C. et al. Maternal smoking during pregnancy and fetal biometry: the INMA Mother and Child Cohort Study. Am. J. Epidemiol. 178, 1067–1075 (2013).
Jaddoe, V. W. V. et al. Maternal smoking and fetal growth characteristics in different periods of pregnancy: the generation R study. Am. J. Epidemiol. 165, 1207–1215 (2007).
Reissland, N. et al. Prenatal effects of maternal nutritional stress and mental health on the fetal movement profile. Arch. Gynecol. Obstet. 302, 65–75 (2020).
De Asis-Cruz, J. et al. Examining the relationship between fetal cortical thickness, gestational age, and maternal psychological distress. Dev. Cogn. Neurosci. 63, 101282 (2023).
Lebit, D. F.-D. & Vladareanu, P. D. R. The role of 4D ultrasound in the assessment of fetal behaviour. Maedica 6, 120–127 (2011).
Reissland, N., Froggatt, S., Reames, E. & Girkin, J. Effects of maternal anxiety and depression on fetal neuro-development. J. Affect. Disord. 241, 469–474 (2018).
Parma, V., Brasselet, R., Zoia, S., Bulgheroni, M. & Castiello, U. The origin of human handedness and its role in pre-birth motor control. Sci. Rep. 7, 16804 (2017).
Shuffrey, L. C. et al. Fetal heart rate, heart rate variability, and heart rate/movement coupling in the Safe Passage Study. J. Perinatol. 39, 608–618 (2019).
Dipietro, J. A., Voegtline, K. M., Pater, H. A. & Costigan, K. A. Predicting child temperament and behavior from the fetus. Dev. Psychopathol. 30, 855–870 (2018).
Namburete, A. I. L. et al. Learning-based prediction of gestational age from ultrasound images of the fetal brain. Med. Image Anal. 21, 72–86 (2015).
Gao, Y. & Alison Noble, J. in Medical Image Computing and Computer-Assisted Intervention—MICCAI 2017, 305–313 (Springer, 2017).
De Asis-Cruz, J., Barnett, S. D., Kim, J. H. & Limperopoulos, C. Functional connectivity-derived optimal gestational-age cut points for fetal brain network maturity. Brain Sci. 11, 2076–3425 (2021).
Karolis, V. R. et al. Maturational networks of human fetal brain activity reveal emerging connectivity patterns prior to ex-utero exposure. Commun. Biol. 6, 661 (2023).
Spann, M. N. et al. Association of maternal prepregnancy body mass index with fetal growth and neonatal thalamic brain connectivity among adolescent and young women. JAMA Netw. Open 3, e2024661 (2020).
Norr, M. E., Hect, J. L., Lenniger, C. J., Van den Heuvel, M. & Thomason, M. E. An examination of maternal prenatal BMI and human fetal brain development. J. Child Psychol. Psychiatry 62, 458–469 (2021).
Thomason, M. E., Hect, J. L., Waller, R. & Curtin, P. Interactive relations between maternal prenatal stress, fetal brain connectivity, and gestational age at delivery. Neuropsychopharmacology 46, 1839–1847 (2021).
van den Heuvel, M. I. et al. Maternal stress during pregnancy alters fetal cortico-cerebellar connectivity in utero and increases child sleep problems after birth. Sci. Rep. 11, 2228 (2021).
Ji, L., Hendrix, C. L. & Thomason, M. E. Empirical evaluation of human fetal fMRI preprocessing steps. Netw. Neurosci. 6, 702–721 (2022).
Thomason, M., Austin, A. & Hendrix, C. Fetal amygdala functional connectivity relates to autism spectrum disorder traits at age 3. Biol. Psychiatry 89, S29 (2021).
Alkandari, F., Ellahi, A., Aucott, L., Devereux, G. & Turner, S. Fetal ultrasound measurements and associations with postnatal outcomes in infancy and childhood: a systematic review of an emerging literature. J. Epidemiol. Community Health 69, 41–48 (2015).
Montagu, A. Touching: The Human Significance of the Skin (Harper and Row, 1978).
Zoia, S. et al. Evidence of early development of action planning in the human foetus: a kinematic study. Exp. Brain Res. 176, 217–226 (2007).
Reissland, N., & Austen, J. in Reach-to-Grasp Behavior: Brain, Behavior, and Modelling Across the Life Span (eds Corbetta, D. & Santello, M.) 3–17 (Routledge, 2018).
de Vries, J. I., Visser, G. H., Mulder, E. J. & Prechtl, H. F. Diurnal and other variations in fetal movement and heart rate patterns at 20–22 weeks. Early Hum. Dev. 15, 333–348 (1987).
Kostović, I. & Jovanov-Milosević, N. The development of cerebral connections during the first 20–45 weeks’ gestation. Semin. Fetal Neonatal Med. 11, 415–422 (2006).
Piontelli, A. et al. in Development of Normal Fetal Movements: The Last 15 Weeks of Gestation (ed. Piontelli, A.) 41–51 (Springer, 2015).
Išasegi, I. Ž., Krsnik, Ž. & Kostović, I. in Factors Affecting Neurodevelopment (eds. Martin, C. R. et al.) 299–307 (Elsevier, 2021).
Ustun, B., Covey, J. & Reissland, N. Chemosensory continuity from prenatal to postnatal life in humans: a systematic review and meta-analysis. PLoS ONE 18, e0283314 (2023).
Lagercrantz, H. in Infant Brain Development: Formation of the Mind and the Emergence of Consciousness (ed. Lagercrantz, H.) 43–52 (Springer, 2016).
DiPietro, J. A., Hodgson, D. M., Costigan, K. A., Hilton, S. C. & Johnson, T. R. Development of fetal movement–fetal heart rate coupling from 20 weeks through term. Early Hum. Dev. 44, 139–151 (1996).
Lüchinger, A. B., Hadders-Algra, M., van Kan, C. M. & de Vries, J. I. P. Fetal onset of general movements. Pediatr. Res. 63, 191–195 (2008).
Zoia, S. et al. The development of upper limb movements: from fetal to post-natal life. PLoS ONE 8, e80876 (2013).
Ferrari, G. A. et al. Ultrasonographic investigation of human fetus responses to maternal communicative and non-communicative stimuli. Front. Psychol. 7, 354 (2016).
Reissland, N., Francis, B., Buttanshaw, L., Austen, J. M. & Reid, V. Do fetuses move their lips to the sound that they hear? An observational feasibility study on auditory stimulation in the womb. Pilot Feasibility Stud. 2, 14 (2016).
Myowa-Yamakoshi, M. & Takeshita, H. Do human fetuses anticipate self-oriented actions? A study by four-dimensional (4D) ultrasonography. Infancy 10, 289–301 (2006).
Reissland, N., Francis, B., Aydin, E., Mason, J. & Schaal, B. The development of anticipation in the fetus: a longitudinal account of human fetal mouth movements in reaction to and anticipation of touch. Dev. Psychobiol. 56, 955–963 (2014).
Fagard, J., Esseily, R., Jacquey, L., O’Regan, K. & Somogyi, E. Fetal origin of sensorimotor behavior. Front. Neurorobot. 12, 23 (2018).
Morton, S. U. & Brodsky, D. Fetal physiology and the transition to extrauterine life. Clin. Perinatol. 43, 395–407 (2016).
Lecanuet, J. P. & Schaal, B. Fetal sensory competencies. Eur. J. Obstet. Gynecol. Reprod. Biol. 68, 1–23 (1996).
Verbruggen, S. W. et al. Stresses and strains on the human fetal skeleton during development. J. R. Soc. Interface 15, 20170593 (2018).
Simion, F., Regolin, L. & Bulf, H. A predisposition for biological motion in the newborn baby. Proc. Natl Acad. Sci. USA 105, 809–813 (2008).
Del Giudice, M. Alone in the dark? Modeling the conditions for visual experience in human fetuses. Dev. Psychobiol. 53, 214–219 (2011).
Dunn, K., Reissland, N. & Reid, V. M. The functional foetal brain: a systematic preview of methodological factors in reporting foetal visual and auditory capacity. Dev. Cogn. Neurosci. 13, 43–52 (2015).
Reppert, S. M., Weaver, D. R. & Godson, C. Melatonin receptors step into the light: cloning and classification of subtypes. Trends Pharmacol. Sci. 17, 100–102 (1996).
Bolnick, J. M., Garcia, G., Fletcher, B. G. & Rayburn, W. F. Cross-over trial of fetal heart rate response to halogen light and vibroacoustic stimulation. J. Matern. Fetal Neonatal Med. 19, 215–219 (2006).
Donovan, T., Dunn, K., Penman, A., Young, R. J. & Reid, V. M. Fetal eye movements in response to a visual stimulus. Brain Behav. 10, e01676 (2020).
Reid, V. M. et al. The human fetus preferentially engages with face-like visual stimuli. Curr. Biol. 28, 824 (2018).
Scheel, A. M., Ritchie, S. J., Brown, N. J. & Jacques, S. L. Methodological problems in a study of fetal visual perception. Curr. Biol. 28, R594–R596 (2018).
Reissland, N., Wood, R., Einbeck, J. & Lane, A. Effects of maternal mental health on fetal visual preference for face-like compared to non-face like light stimulation. Early Hum. Dev. 151, 105227 (2020).
Hepper, P. G. & Shahidullah, B. S. Development of fetal hearing. Arch. Dis. Child. Fetal Neonatal Ed. 71, F81–F87 (1994).
Lecanuet, J. P. et al. What sounds reach fetuses: biological and nonbiological modeling of the transmission of pure tones. Dev. Psychobiol. 33, 203–219 (1998).
Moore, J. K. & Linthicum, F. H. Jr. The human auditory system: a timeline of development. Int. J. Audiol. 46, 460–478 (2007).
Groome, L. J. et al. Behavioral state affects heart rate response to low-intensity sound in human fetuses. Early Hum. Dev. 54, 39–54 (1999).
Kisilevsky, B. S. et al. Effects of experience on fetal voice recognition. Psychol. Sci. 14, 220–224 (2003).
Morokuma, S. et al. Developmental change in fetal response to repeated low-intensity sound. Dev. Sci. 11, 47–52 (2008).
Draganova, R., Eswaran, H., Murphy, P., Lowery, C. & Preissl, H. Serial magnetoencephalographic study of fetal and newborn auditory discriminative evoked responses. Early Hum. Dev. 83, 199–207 (2007).
Winkler, I. et al. Newborn infants can organize the auditory world. Proc. Natl Acad. Sci. USA 100, 11812–11815 (2003).
Busnel, M. C. et al. Effects of mother’s pertinent addressed speech on the fetal heart rate: a spectral analysis study. 82. Pediatr. Res. 39, 16 (1996).
Voegtline, K. M., Costigan, K. A., Pater, H. A. & DiPietro, J. A. Near-term fetal response to maternal spoken voice. Infant Behav. Dev. 36, 526–533 (2013).
Moon, C. M. & Fifer, W. P. Evidence of transnatal auditory learning. J. Perinatol. 20, S37–S44 (2000).
Krueger, C. A., Cave, E. C. & Garvan, C. Fetal response to live and recorded maternal speech. Biol. Res. Nurs. 17, 112–120 (2015).
Fernald, A. Expanded Intonation Contours in Mothers’ Speech to Newborn (Univ. of Oregon, 1979).
Webb, A. R., Heller, H. T., Benson, C. B. & Lahav, A. Mother’s voice and heartbeat sounds elicit auditory plasticity in the human brain before full gestation. Proc. Natl Acad. Sci. USA 112, 3152–3157 (2015).
DeCasper, A. J. & Fifer, W. P. Of human bonding: newborns prefer their mothers’ voices. Science 208, 1174–1176 (1980).
Carvalho, M. E. S. et al. Vocal responsiveness of preterm infants to maternal infant-directed speaking and singing during skin-to-skin contact (kangaroo care) in the NICU. Infant Behav. Dev. 57, 101332 (2019).
Masek, L. R. et al. Where language meets attention: how contingent interactions promote learning. Dev. Rev. 60, 100961 (2021).
Meltzoff, A. N. & Moore, M. K. in The Body and the Self 43–69 (1995).
Shultz, S., Klin, A. & Jones, W. Neonatal transitions in social behavior and their implications for autism. Trends Cogn. Sci. 22, 452–469 (2018).
Gopnik, A. The Philosophical Baby: What Children’s Minds Tell Us about Truth, Love and the Meaning of Life (Random House, 2009).
Mampe, B., Friederici, A. D., Christophe, A. & Wermke, K. Newborns’ cry melody is shaped by their native language. Curr. Biol. 19, 1994–1997 (2009).
Moon, C., Lagercrantz, H. & Kuhl, P. K. Language experienced in utero affects vowel perception after birth: a two-country study. Acta Paediatr. 102, 156–160 (2013).
Mariani, B. et al. Prenatal experience with language shapes the brain. Sci. Adv. 9, eadj3524 (2023).
Wu, R., Gopnik, A., Richardson, D. C. & Kirkham, N. Z. Infants learn about objects from statistics and people. Dev. Psychol. 47, 1220–1229 (2011).
Nelson, C. A. 3rd & Gabard-Durnam, L. J. Early adversity and critical periods: neurodevelopmental consequences of violating the expectable environment. Trends Neurosci. 43, 133–143 (2020).
Yadav, A. et al. Fetal growth trajectories and measures of insulin resistance in young adults. J. Clin. Endocrinol. Metab. 108, e861–e870 (2023).
Morgan, J. E. et al. Prenatal maternal C-reactive protein prospectively predicts child executive functioning at ages 4–6 years. Dev. Psychobiol. 62, 1111–1123 (2020).
Conradt, E., Lester, B. M., Appleton, A. A., Armstrong, D. A. & Marsit, C. J. The roles of DNA methylation of NR3C1 and 11β-HSD2 and exposure to maternal mood disorder in utero on newborn neurobehavior. Epigenetics 8, 1321–1329 (2013).
Lenniger, C. & Espinoza-Heredia, C. Associations between prenatal maternal cortisol levels and the developing human brain. Biologicals (2020).
Barker, D. J. P. The developmental origins of chronic adult disease. Acta Paediatr. Suppl. 93, 26–33 (2004).
Ustun, B., Reissland, N., Covey, J., Schaal, B. & Blissett, J. Flavor sensing in utero and emerging discriminative behaviors in the human fetus. Psychol. Sci. 33, 1651–1663 (2022).
Seckl, J. R. & Holmes, M. C. Mechanisms of disease: glucocorticoids, their placental metabolism and fetal ‘programming’ of adult pathophysiology. Nat. Clin. Pract. Endocrinol. Metab. 3, 479–488 (2007).
Duffy, A. R., Schminkey, D. L., Groer, M. W., Shelton, M. & Dutra, S. Comparison of hair cortisol levels and perceived stress in mothers who deliver at preterm and term. Biol. Res. Nurs. 20, 292–299 (2018).
Lewis, A. J., Austin, E., Knapp, R., Vaiano, T. & Galbally, M. Perinatal maternal mental health, fetal programming and child development. Healthcare (Basel) 3, 1212–1227 (2015).
Arduini, D., Rizzo, G., Romanini, C. & Mancuso, S. Fetal blood flow velocity waveforms as predictors of growth retardation. Obstet. Gynecol. 70, 7–10 (1987).
O’Donnell, K. J. et al. Maternal prenatal anxiety and downregulation of placental 11β-HSD2. Psychoneuroendocrinology 37, 818–826 (2012).
Davis, E. P., Glynn, L. M., Waffarn, F. & Sandman, C. A. Prenatal maternal stress programs infant stress regulation. J. Child Psychol. Psychiatry 52, 119–129 (2011).
Bonamy, A.-K. E., Parikh, N. I., Cnattingius, S., Ludvigsson, J. F. & Ingelsson, E. Birth characteristics and subsequent risks of maternal cardiovascular disease: effects of gestational age and fetal growth. Circulation 124, 2839–2846 (2011).
Calkins, K. & Devaskar, S. U. Fetal origins of adult disease. Curr. Probl. Pediatr. Adolesc. Health Care 41, 158–176 (2011).
Simmons, R. Epigenetics and maternal nutrition: nature v. nurture. Proc. Nutr. Soc. 70, 73–81 (2011).
De Asis-Cruz, J. & Limperopoulos, C. Harnessing the power of advanced fetal neuroimaging to understand in utero footprints for later neuropsychiatric disorders. Bio. Psychiatry 93, e2022.11.019 (2022).
Narang, K. et al. Impact of asymptomatic and mild COVID-19 infection on fetal growth during pregnancy. Eur. J. Obstet. Gynecol. Reprod. Biol. 281, 63–67 (2023).
Goin, D. E. et al. Maternal experience of multiple hardships and fetal growth: extending environmental mixtures methodology to social exposures. Epidemiology 32, 18–26 (2021).
Smarr, M. M. et al. Comparison of fetal growth by maternal prenatal acetaminophen use. Pediatr. Res. 86, 261–268 (2019).
Lehrner, A. et al. Maternal PTSD associates with greater glucocorticoid sensitivity in offspring of Holocaust survivors. Psychoneuroendocrinology 40, 213–220 (2014).
Schlotz, W., Godfrey, K. M. & Phillips, D. I. Prenatal origins of temperament: fetal growth, brain structure, and inhibitory control in adolescence. PLoS ONE 9, e96715 (2014).
Pierozan, P. & Karlsson, O. Mitotically heritable effects of BMAA on striatal neural stem cell proliferation and differentiation. Cell Death Dis. 10, 478 (2019).
Vasung, L. et al. Association between quantitative MR markers of cortical evolving organization and gene expression during human prenatal brain development. Cereb. Cortex 31, 3610–3621 (2021).
Rosa, M. J. et al. Identifying sensitive windows for prenatal particulate air pollution exposure and mitochondrial DNA content in cord blood. Environ. Int. 98, 198–203 (2017).
Bose, S. et al. Prenatal nitrate exposure and childhood asthma. Influence of maternal prenatal stress and fetal sex. Am. J. Respir. Crit. Care Med. 196, 1396–1403 (2017).
Nasreen, H.-E., Kabir, Z. N., Forsell, Y. & Edhborg, M. Impact of maternal depressive symptoms and infant temperament on early infant growth and motor development: results from a population based study in Bangladesh. J. Affect. Disord. 146, 254–261 (2013).
Barker, E. D., Kirkham, N., Ng, J. & Jensen, S. K. G. Prenatal maternal depression symptoms and nutrition, and child cognitive function. Br. J. Psychiatry 203, 417–421 (2013).
Bauer, A. et al. Perinatal depression and child development: exploring the economic consequences from a South London cohort. Psychol. Med. 45, 51–61 (2015).
Cao-Lei, L. et al. Prenatal stress and epigenetics. Neurosci. Biobehav. Rev. 117, 198–210 (2020).
Maxwell, S. D., Fineberg, A. M., Drabick, D. A., Murphy, S. K. & Ellman, L. M. Maternal prenatal stress and other developmental risk factors for adolescent depression: spotlight on sex differences. J. Abnorm. Child Psychol. 46, 381–397 (2018).
Walhovd, K. B. et al. Long-term influence of normal variation in neonatal characteristics on human brain development. Proc. Natl Acad. Sci. USA 109, 20089–20094 (2012).
Fjell, A. M. et al. Continuity and discontinuity in human cortical development and change from embryonic stages to old age. Cereb. Cortex 29, 3879–3890 (2019).
King, S., Dancause, K., Turcotte-Tremblay, A.-M., Veru, F. & Laplante, D. P. Using natural disasters to study the effects of prenatal maternal stress on child health and development. Birth Defects Res. C 96, 273–288 (2012).
Cao-Lei, L. et al. DNA methylation mediates the effect of maternal cognitive appraisal of a disaster in pregnancy on the child’s C-peptide secretion in adolescence: Project Ice Storm. PLoS ONE 13, e0192199 (2018).
van den Heuvel, M. I. et al. Intergenerational transmission of maternal childhood maltreatment prior to birth: effects on human fetal amygdala functional connectivity. J. Am. Acad. Child Adolesc. Psychiatry 62, 1134–1146 (2023).
Mink, J., Boutron-Ruault, M.-C., Charles, M.-A., Allais, O. & Fagherazzi, G. Associations between early-life food deprivation during World War II and risk of hypertension and type 2 diabetes at adulthood. Sci. Rep. 10, 5741 (2020).
Opler, M. G. A. & Susser, E. S. Fetal environment and schizophrenia. Environ. Health Perspect. 113, 1239–1242 (2005).
Poehlmann, J. et al. Emerging self-regulation in toddlers born preterm or low birth weight: differential susceptibility to parenting? Dev. Psychopathol. 23, 177–193 (2011).
Batalle, D. et al. Early development of structural networks and the impact of prematurity on brain connectivity. Neuroimage 149, 379–392 (2017).
Haartsen, R., Jones, E. J. H. & Johnson, M. H. Human brain development over the early years. Curr. Opin. Behav. Sci. 10, 149–154 (2016).
Monk, C. et al. Distress during pregnancy: epigenetic regulation of placenta glucocorticoid-related genes and fetal neurobehavior. Am. J. Psychiatry 173, 705–713 (2016).
Turco, M. Y. & Moffett, A. Development of the human placenta. Development 146, dev163428 (2019).
Monk, C. et al. Effects of maternal breathing rate, psychiatric status, and cortisol on fetal heart rate. Dev. Psychobiol. 53, 221–233 (2011).
Mears, K., McAuliffe, F., Grimes, H. & Morrison, J. J. Fetal cortisol in relation to labour, intrapartum events and mode of delivery. J. Obstet. Gynaecol. 24, 129–132 (2004).
Sandman, C. A. et al. Elevated maternal cortisol early in pregnancy predicts third trimester levels of placental corticotropin releasing hormone (CRH): priming the placental clock. Peptides 27, 1457–1463 (2006).
Steer, P. & Flint, C. ABC of labour care: physiology and management of normal labour. Br. Med. J. 318, 793–796 (1999).
Sinding, M. et al. Reduced placental oxygenation during subclinical uterine contractions as assessed by BOLD MRI. Placenta 39, 16–20 (2016).
Jonsson, M. et al. Implementation of a revised classification for intrapartum fetal heart rate monitoring and association to birth outcome: a national cohort study. Acta Obstet. Gynecol. Scand. 101, 183–192 (2022).
Gao, Y. & Raj, J. U. Regulation of the pulmonary circulation in the fetus and newborn. Physiol. Rev. 90, 1291–1335 (2010).
Tribe, R. M. et al. Parturition and the perinatal period: can mode of delivery impact on the future health of the neonate? J. Physiol. 596, 5709–5722 (2018).
Masukume, G. et al. Caesarean section delivery and childhood obesity in a British longitudinal cohort study. PLoS ONE 14, e0223856 (2019).
Chien, L.-N., Lin, H.-C., Shao, Y.-H. J., Chiou, S.-T. & Chiou, H.-Y. Risk of autism associated with general anesthesia during cesarean delivery: a population-based birth-cohort analysis. J. Autism Dev. Disord. 45, 932–942 (2015).
Uchitel, J., Vanhatalo, S. & Austin, T. Early development of sleep and brain functional connectivity in term-born and preterm infants. Pediatr. Res. 91, 771–786 (2022).
Leung, M. P., Thompson, B., Black, J., Dai, S. & Alsweiler, J. M. The effects of preterm birth on visual development. Clin. Exp. Optom. 101, 4–12 (2018).
Emberson, L. L., Boldin, A. M., Riccio, J. E., Guillet, R. & Aslin, R. N. Deficits in top-down sensory prediction in infants at risk due to premature birth. Curr. Biol. 27, 431–436 (2017).
Burstein, O., Zevin, Z. & Geva, R. Preterm birth and the development of visual attention during the first 2 years of life: a systematic review and meta-analysis. JAMA Netw. Open 4, e213687 (2021).
Ream, M. A. & Lehwald, L. Neurologic consequences of preterm birth. Curr. Neurol. Neurosci. Rep. 18, 48 (2018).
Bartocci, M. Moderately and late preterms have problem recognizing faces after birth. J. Pediatr. 93, 4–5 (2017).
Ball, G. et al. Rich-club organization of the newborn human brain. Proc. Natl Acad. Sci. USA 111, 7456–7461 (2014).
Knickmeyer, R. C. et al. Impact of sex and gonadal steroids on neonatal brain structure. Cereb. Cortex 24, 2721–2731 (2014).
Knickmeyer, R. C. et al. Impact of demographic and obstetric factors on infant brain volumes: a population neuroscience study. Cereb. Cortex 27, 5616–5625 (2017).
Stewart, C. J. et al. Cesarean or vaginal birth does not impact the longitudinal development of the gut microbiome in a cohort of exclusively preterm infants. Front. Microbiol. 8, 1008 (2017).
Widström, A.-M., Brimdyr, K., Svensson, K., Cadwell, K. & Nissen, E. A plausible pathway of imprinted behaviors: skin-to-skin actions of the newborn immediately after birth follow the order of fetal development and intrauterine training of movements. Med. Hypotheses 134, 109432 (2020).
Kota, S. K. et al. Endocrinology of parturition. Indian J. Endocrinol. Metab. 17, 50–59 (2013).
Soma-Pillay, P., Nelson-Piercy, C., Tolppanen, H. & Mebazaa, A. Physiological changes in pregnancy. Cardiovasc. J. Afr. 27, 89–94 (2016).
Cuneo, B. F. Outcome of fetal cardiac defects. Curr. Opin. Pediatr. 18, 490–496 (2006).
Kukka, A. J. et al. Observational study comparing heart rate in crying and non-crying but breathing infants at birth. BMJ Paediatr. Open 7, e001886 (2023).
Widström, A.-M. et al. Newborn behaviour to locate the breast when skin-to-skin: a possible method for enabling early self-regulation. Acta Paediatr. 100, 79–85 (2011).
Hym, C. et al. Newborns modulate their crawling in response to their native language but not another language. Dev. Sci. 26, e13248 (2023).
Varendi, H., Porter, R. H. & Winberg, J. The effect of labor on olfactory exposure learning within the first postnatal hour. Behav. Neurosci. 116, 206–211 (2002).
Zanardo, V., Volpe, F., de Luca, F. & Straface, G. A temperature gradient may support mother-infant thermal identification and communication in the breast crawl from birth to breastfeeding. Acta Paediatr. 106, 1596–1599 (2017).
Keven, N. & Akins, K. A. Neonatal imitation in context: sensorimotor development in the perinatal period. Behav. Brain Sci. 40, e381 (2017).
Bartocci, M. et al. Activation of olfactory cortex in newborn infants after odor stimulation: a functional near-infrared spectroscopy study. Pediatr. Res. 48, 18–23 (2000).
Linn��r, A. et al. Immediate skin-to-skin contact is feasible for very preterm infants but thermal control remains a challenge. Acta Paediatr. 109, 697–704 (2020).
Bergman, N. J., Ludwig, R. J. & Westrup, B. Nurturescience versus neuroscience: a case for rethinking perinatal mother–infant behaviors and relationship. Birth Defects 111, 1110–1127 (2019).
von Hofsten, C. & Rönnqvist, L. The structuring of neonatal arm movements. Child Dev. 64, 1046–1057 (1993).
Chinn, L. K., Noonan, C. F. & Lockman, J. J. The human face becomes mapped as a sensorimotor reaching space during the first year. Child Dev. 92, 760–773 (2021).
Meltzoff, A. N. & Moore, M. K. Newborn infants imitate adult facial gestures. Child Dev. 54, 702–709 (1983).
Oostenbroek, J. et al. Re-evaluating the neonatal imitation hypothesis. Dev. Sci. 22, e12720 (2019).
Wörmann, V., Holodynski, M., Kärtner, J. & Keller, H. A cross-cultural comparison of the development of the social smile: a longitudinal study of maternal and infant imitation in 6- and 12-week-old infants. Infant Behav. Dev. 35, 335–347 (2012).
Hym, C. et al. Newborn crawling and rooting in response to maternal breast odor. Dev. Sci. 24, e13061 (2021).
Marlier, L., Schaal, B. & Soussignan, R. Neonatal responsiveness to the odor of amniotic and lacteal fluids: a test of perinatal chemosensory continuity. Child Dev. 69, 611–623 (1998).
Meltzoff, A. N. & Moore, M. K. in Developmental Neurocognition: Speech and Face Processing in the First Year of Life (eds de Boysson-Bardies, B. et al.) 211–225 (Springer, 1993).
Orioli, G., Bremner, A. J. & Farroni, T. Multisensory perception of looming and receding objects in human newborns. Curr. Biol. 28, R1294–R1295 (2018).
Meltzoff, A. N., Saby, J. N. & Marshall, P. J. Neural representations of the body in 60‐day‐old human infants. Dev. Sci. 22, e12698 (2019).
van der Meer, A. L., van der Weel, F. R. & Lee, D. N. The functional significance of arm movements in neonates. Science 267, 693–695 (1995).
Moon, C., Cooper, R. P. & Fifer, W. P. Two-day-olds prefer their native language. Infant Behav. Dev. 16, 495–500 (1993).
Bobin-Bègue, A., Provasi, J., Marks, A. & Pouthas, V. Influence of auditory tempo on the endogenous rhythm of non-nutritive sucking. Eur. Rev. Appl. Psychol. 56, 239–245 (2006).
Gilmore, R. O. & Johnson, M. H. Body-centered representations for visually-guided action emerge during early infancy. Cognition 65, B1–B9 (1997).
Witherington, D. C., Overton, W. F., Lickliter, R., Marshall, P. J. & Narvaez, D. Metatheory and the primacy of conceptual analysis in developmental science. Hum. Dev. 61, 181–198 (2018).
Bornstein, M. H. in Parenting: Selected Writings of Marc H. Bornstein (ed. Bornstein, M. H.) 280–315 (Routledge, 2022).
Atkinson, J. & Braddick, O. Inferences about infants’ visual brain mechanisms. Vis. Neurosci. 30, 185–195 (2013).
Shen, G., Weiss, S. M., Meltzoff, A. N., Allison, O. N. & Marshall, P. J. Exploring developmental changes in infant anticipation and perceptual processing: EEG responses to tactile stimulation. Infancy.: Off. J. Int. Soc. Infant Stud. 27, 97–114 (2022).
Wiener, R. F. & Thurman, S. L. in Reach-to-Grasp Behavior: Brain, Behavior, and Modelling Across the Life Span (eds Corbetta, D. & Santello, M.) 16–30 (Routledge, 2018).
Weiss, S. M., Meltzoff, A. N. & Marshall, P. J. Neural measures of anticipatory bodily attention in children: relations with executive function. Dev. Cogn. Neurosci. 34, 148–158 (2018).
Johnson, M. H. Functional brain development in humans. Nat. Rev. Neurosci. 6, 766–774 (2005).
Farroni, T., Csibra, G., Simion, F. & Johnson, M. H. Eye contact detection in humans from birth. Proc. Natl Acad. Sci. USA 99, 9602–9605 (2002).
Farroni, T. et al. Infant cortex responds to other humans from shortly after birth. Sci. Rep. 3, 2851 (2013).
Lloyd-Fox, S. et al. Social perception in infancy: a near infrared spectroscopy study. Child Dev. 80, 986–999 (2009).
Lloyd-Fox, S. et al. Cortical specialisation to social stimuli from the first days to the second year of life: a rural Gambian cohort. Dev. Cogn. Neurosci. 25, 92–104 (2017).
Gibbon, S. et al. Machine learning accurately classifies neural responses to rhythmic speech vs. non-speech from 8-week-old infant EEG. Brain Lang. 220, 104968 (2021).
Rekow, D. et al. Odor-driven face-like categorization in the human infant brain. Proc. Natl Acad. Sci. USA 118, e2014979118 (2021).
Shultz, S., Vouloumanos, A. & Pelphrey, K. The superior temporal sulcus differentiates communicative and noncommunicative auditory signals. J. Cogn. Neurosci. 24, 1224–1232 (2012).
Marshall, P. J., Houser, T. M. & Weiss, S. M. The shared origins of embodiment and development. Front. Syst. Neurosci. 15, 726403 (2021).
Csibra, G. & Gergely, G. Natural pedagogy as evolutionary adaptation. Philos. Trans. R. Soc. Lond. B 366, 1149–1157 (2011).
Piazza, E. A., Cohen, A., Trach, J. & Lew-Williams, C. Neural synchrony predicts children’s learning of novel words. Cognition 214, 104752 (2021).
Nguyen, T., Abney, D. H., Salamander, D., Bertenthal, B. I. & Hoehl, S. Proximity and touch are associated with neural but not physiological synchrony in naturalistic mother-infant interactions. Neuroimage 244, 118599 (2021).
Clackson, K., Wass, S., Georgieva, S. & Brightman, L. Do helpful mothers help? Effects of maternal scaffolding and infant engagement on cognitive performance. Front. Psychol. 10, 2661 (2019).
Wass, S. V., Clackson, K. & Leong, V. Increases in arousal are more long-lasting than decreases in arousal: on homeostatic failures during emotion regulation in infancy. Infancy 23, 628–649 (2018).
Gao, X., Aderemi, T. A., Zhou, B., Olanipekun, W. D. & Bassey, R. Influence of households’ socio-economic factors on maternal and under-five survival in Nigeria: implication for the sustainable development goal 3. Afr. J. Reprod. Health 27, 83–90 (2023).
Cassinelli, E. H. et al. Exploring health behaviours, attitudes and beliefs of women and men during the preconception and interconception periods: a cross-sectional study of adults on the island of ireland. Nutrients 15, 3832 (2023).
Aviv, E. C. et al. Prenatal prolactin predicts postnatal parenting attitudes and brain structure remodeling in first-time fathers. Psychoneuroendocrinology 156, 106332 (2023).
Golombok, S., Cook, R., Bish, A. & Murray, C. Families created by the new reproductive technologies: quality of parenting and social and emotional development of the children. Child Dev. 66, 285–298 (1995).
Katus, L. et al. Perceived stress during the prenatal period: assessing measurement invariance of the Perceived Stress Scale (PSS-10) across cultures and birth parity. Arch. Women Ment. Health 25, 633–640 (2022).
McNab, S. E. et al. The silent burden: a landscape analysis of common perinatal mental disorders in low- and middle-income countries. BMC Pregnancy Childbirth 22, 342 (2022).
Rylander, C., Odland, J. Ø. & Sandanger, T. M. Climate change and the potential effects on maternal and pregnancy outcomes: an assessment of the most vulnerable—the mother, fetus, and newborn child. Glob. Health Action 6, 19538 (2013).
Merz, E. C. et al. Socioeconomic disparities in chronic physiologic stress are associated with brain structure in children. Biol. Psychiatry 86, 921–929 (2019).
Imrie, S., Zadeh, S., Wylie, K. & Golombok, S. Children with trans parents: parent–child relationship quality and psychological well-being. Parent. Sci. Pract. 21, 185–215 (2021).
Golombok, S. et al. A longitudinal study of families formed through third-party assisted reproduction: mother-child relationships and child adjustment from infancy to adulthood. Dev. Psychol. 59, 1059–1073 (2023).
Peven, K. et al. Equity in newborn care, evidence from national surveys in low- and middle-income countries. Int. J. Equity Health 20, 132 (2021).
Gillespie, S. L., Christian, L. M., Alston, A. D. & Salsberry, P. J. Childhood stress and birth timing among African American women: cortisol as biological mediator. Psychoneuroendocrinology 84, 32–41 (2017).
Matthews, R. J. et al. Understanding ethnic inequalities in stillbirth rates: a UK population-based cohort study. BMJ Open 12, e057412 (2022).
Aydin, E. et al. COVID-19 in the context of pregnancy, infancy and parenting (CoCoPIP) study: protocol for a longitudinal study of parental mental health, social interactions, physical growth and cognitive development of infants during the pandemic. BMJ Open 12, e053800 (2022).
Roder-DeWan, S. et al. Health system redesign for maternal and newborn survival: rethinking care models to close the global equity gap. BMJ Glob. Health 5, e002539 (2020).
Spann, M. N. et al. The effects of experience of discrimination and acculturation during pregnancy on the developing offspring brain. Neuropsychopharmacology https://doi.org/10.1038/s41386-023-01765-3 (2023).
Sagiv, S. K. et al. Prenatal organochlorine exposure and measures of behavior in infancy using the Neonatal Behavioral Assessment Scale (NBAS). Environ. Health Perspect. 116, 666–673 (2008).
Alipio, J. B. et al. Perinatal fentanyl exposure leads to long-lasting impairments in somatosensory circuit function and behavior. J. Neurosci. 41, 3400–3417 (2021).
Fernandez-Gonzalez, S. et al. Study of the fetal and maternal microbiota in pregnant women with intrauterine growth restriction and its relationship with inflammatory biomarkers: a case-control study protocol (SPIRIT compliant). Medicine 99, e22722 (2020).
Alvarenga, P., Ángeles Cerezo, M. & Kuchirko, Y. The Maternal Sensitivity Program: A Model for Promoting Infant Development in Challenging Contexts (Springer, 2021).
Acknowledgements
S.M.W. and S.L.-F. are supported by a UKRI Future Leaders fellowship (grant MR/S018425/1). M.H.J. is supported by a Medical Research Council Programme Grant (MR/T003057/1) to M.H.J. The views expressed are those of the authors and not necessarily those of the MRC or the UKRI.
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Meredith Weiss, S., Aydin, E., Lloyd-Fox, S. et al. Trajectories of brain and behaviour development in the womb, at birth and through infancy. Nat Hum Behav (2024). https://doi.org/10.1038/s41562-024-01896-7
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DOI: https://doi.org/10.1038/s41562-024-01896-7