Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-24T02:48:36.533Z Has data issue: false hasContentIssue false
  • English
  • Français

Prenatal maternal psychological distress and fetal developmental trajectories: associations with infant temperament

Published online by Cambridge University Press:  11 January 2021

Mariann A. Howland ,
Curt A. Sandman ,
Elysia Poggi Davis  and
Laura M. Glynn
Mariann A. Howland*
Affiliation:
Institute of Child Development, University of Minnesota, Minneapolis, MN, USA
Curt A. Sandman
Affiliation:
Department of Psychiatry & Human Behavior, University of California, Irvine, CA, USA
Elysia Poggi Davis
Affiliation:
Department of Psychiatry & Human Behavior, University of California, Irvine, CA, USA Department of Psychology, University of Denver, Denver, CO, USA
Laura M. Glynn
Affiliation:
Department of Psychology, Chapman University, Orange, CA, USA
*
Author for Correspondence: Mariann Howland, Institute of Child Development, University of Minnesota, 51 East River Parkway, Minneapolis, MN55455; E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Associations between prenatal maternal psychological distress and offspring developmental outcomes are well documented, yet relatively little research has examined links between maternal distress and development in utero, prior to postpartum influences. Fetal heart rate (FHR) parameters are established indices of central and autonomic nervous system maturation and function which demonstrate continuity with postnatal outcomes. This prospective, longitudinal study of 149 maternal–fetal pairs evaluated associations between prenatal maternal distress, FHR parameters, and dimensions of infant temperament. Women reported their symptoms of psychological distress at five prenatal visits, and FHR monitoring was conducted at the last three visits. Maternal report of infant temperament was collected at 3 and 6 months of age. Exposure to elevated prenatal maternal psychological distress was associated with higher late-gestation resting mean FHR (FHRM) among female but not male fetuses. Higher late-gestation FHRM was associated with lower infant orienting/regulation and with higher infant negative affectivity, and these associations did not differ by infant sex. A path analysis identified higher FHRM as one pathway by which elevated prenatal maternal distress was associated with lower orienting/regulation among female infants. Findings suggest that, for females, elevated maternal distress alters fetal development, with implications for postnatal function. Results also support the notion that, for both sexes, individual differences in regulation emerge prenatally and are maintained into infancy. Collectively, these findings underscore the utility of direct assessment of development in utero when examining if prenatal experiences are carried forward into postnatal life.

Keywords

fetalheart rateprenatalstresstemperament
Type
Special Section 2: Early Adversity and Development: Contributions from the Field
Information
Development and Psychopathology , Volume 32 , Special Issue 5: Early Adversity, Stress, and Neurobehavioral Development: Honoring Megan R. Gunnar's Contributions to Developmental Science , December 2020 , pp. 1685 - 1695
Check for updates
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adamson, B., Letourneau, N., & Lebel, C. (2018). Prenatal maternal anxiety and children's brain structure and function: A systematic review of neuroimaging studies. Journal of Affective Disorders, 241, 117–126. doi:10.1016/j.jad.2018.08.029CrossRefGoogle ScholarPubMed
Allister, L., Lester, B. M., Carr, S., & Liu, J. (2001). The effects of maternal depression on fetal heart rate response to vibroacoustic stimulation. Developmental Neuropsychology, 20, 639–651. doi:10.1207/S15326942DN2003_6CrossRefGoogle ScholarPubMed
American College of Obstetricians and Gynecologists. (2009). ACOG practice bulletin: Ultrasonography in pregnancy. Obstetrics & Gynecology, 113, 451–461.CrossRefGoogle Scholar
Barker, D. J. P. (1990). The fetal and infant origins of adult disease. British Medical Journal, 301, 1111. doi:10.1136/bmj.301.6761.1111CrossRefGoogle ScholarPubMed
Bartoń, K. (2019). MuMIn: Multi-model inference. R Package Version 1.43.15.Google Scholar
Bates, D., Mächler, M., Bolker, B. M., & Walker, S. C. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67, 1–48. doi:10.18637/jss.v067.i01CrossRefGoogle Scholar
Bornstein, M. H., DiPietro, J. A., Hahn, C. S., Painter, K., Haynes, O. M., & Costigan, K. A. (2002). Prenatal cardiac function and postnatal cognitive development: An exploratory study. Infancy, 3, 475–494. doi:10.1207/S15327078IN0304_04CrossRefGoogle Scholar
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, 633–638. doi:10.1016/j.earlhumdev.2009.08.001CrossRefGoogle ScholarPubMed
Bussières, E. L., Tarabulsy, G. M., Pearson, J., Tessier, R., Forest, J. C., & Giguère, Y. (2015). Maternal prenatal stress and infant birth weight and gestational age: A meta-analysis of prospective studies. Developmental Review, 36, 179–199. doi:10.1016/j.dr.2015.04.001CrossRefGoogle Scholar
Cicchetti, D., & Valentino, K. (2007). Toward the application of a multiple-levels-of-analysis perspective to research in development and psychopathology. In Masten, A. S. (Ed.), Minnesota Symposia on Child Psychology. Multilevel Dynamics in Developmental Psychopathology. (pp. 243–284). Mahwah, NJ: Erlbaum.Google Scholar
Cohen, S., & Williamson, G. M. (1988). Perceived stress in a probability sample of the U.S. In Spacapan, S. & Oskamp, S. (Eds.), The social psychology of health: Claremont Symposium on Applied Social Psychology, (pp. 31–67). Newbury Park, CA: Sage.Google Scholar
Dalton, K., Dawes, G. S., & Patrick, J. E. (1983). The autonomic nervous system and fetal heart rate variability. American Journal of Obstetrics and Gynecology, 146, 456–462.CrossRefGoogle ScholarPubMed
David, M., Hirsch, M., Karin, J., Toledo, E., & Akselrod, S. (2007). An estimate of fetal autonomic state by time-frequency analysis of fetal heart rate variability. Journal of Applied Physiology, 102, 1057–1064. doi:10.1152/japplphysiol.00114.2006CrossRefGoogle ScholarPubMed
Davis, E. P., Hankin, B. L., Glynn, L. M., Head, K., Kim, D. J., & Sandman, C. A. (2020). Prenatal maternal stress, child cortical thickness, and adolescent depressive symptoms. Child Development, 91, e432–e450. doi:10.1111/cdev.13252CrossRefGoogle ScholarPubMed
Dawes, G. S., Houghton, C. R. S., Redman, C. W. G., & Visser, G. H. A. (1982). Pattern of the normal human fetal heart rate. BJOG: An International Journal of Obstetrics & Gynaecology, 89, 276–284. doi:10.1111/j.1471-0528.1982.tb04696.xCrossRefGoogle ScholarPubMed
Dieter, J. N. I., Emory, E. K., Johnson, K. C., & Raynor, B. D. (2008). Maternal depression and anxiety effects on the human fetus: Preliminary findings and clinical implications. Infant Mental Health Journal, 29, 420–441. doi:10.1002/imhj.20192CrossRefGoogle ScholarPubMed
DiPietro, J. A. (2010). Maternal influences on the developing fetus. In AW Zimmerman and SL Connors (Eds.), Maternal Influences on Fetal Neurodevelopment: Clinical and Research Aspects. Publisher: Springer-Verlag: New York, NY.Google Scholar
DiPietro, J. A., Bornstein, M. H., Hahn, C. S., Costigan, K., & Achy-Brou, A. (2007). Fetal heart rate and variability: Stability and prediction to developmental outcomes in early childhood. Child Development, 78, 1788–1798. doi:10.1111/j.1467-8624.2007.01099.xCrossRefGoogle ScholarPubMed
DiPietro, J. A., Caulfield, L. E., Costigan, K. A., Merialdi, M., Nguyen, R. H. N., Zavaleta, N., & Gurewitsch, E. D. (2004). Fetal neurobehavioral development: A tale of two cities. Developmental Psychology, 40, 445–456. doi:10.1037/0012-1649.40.3.445CrossRefGoogle ScholarPubMed
DiPietro, J. A., Costigan, K. A., & Gurewitsch, E. D. (2003). Fetal response to induced maternal stress. Early Human Development, 74, 125–138. doi:10.1016/j.earlhumdev.2003.07.001CrossRefGoogle ScholarPubMed
DiPietro, J. A., Costigan, K. A., & Pressman, E. K. (2002a). Fetal state concordance predicts infant state regulation. Early Human Development, 68, 1–13. doi:10.1016/S0378-3782(02)00006-3CrossRefGoogle Scholar
DiPietro, J. A., Costigan, K. A., Pressman, E. K., & Doussard-Roosevelt, J. A. (2000). Antenatal origins of individual differences in heart rate. Developmental Psychobiology, 37, 221–228. doi:10.1002/1098-2302(2000)37:43.0.co;2-a3.0.CO;2-A>CrossRefGoogle ScholarPubMed
DiPietro, J. A., Costigan, K. A., & Voegtline, K. M. (2015). Studies in fetal behavior: Revisited, renewed, and reimagined. Monographs of the Society for Research in Child Development, 80, 1–151. doi:10.1111/mono.v80.3Google ScholarPubMed
DiPietro, J. A., Ghera, M. M., & Costigan, K. A. (2008). Prenatal origins of temperamental reactivity in early infancy. Early Human Development, 84, 569–575. doi:10.1016/j.earlhumdev.2008.01.004CrossRefGoogle ScholarPubMed
DiPietro, J. A., Hilton, S. C., Hawkins, M., Costigan, K. A., & Pressman, E. K. (2002b). Maternal stress and affect influence fetal neurobehavioral development. Developmental Psychology, 38, 659–668. doi:10.1037/0012-1649.38.5.659CrossRefGoogle Scholar
DiPietro, J. A., Hodgson, D. M., Costigan, K. A., Hilton, S. C., & Johnson, T. R. B. (1996a). Fetal neurobehavioral development. Child Development, 67, 2553–2567. doi:10.1111/j.1467-8624.1996.tb01874.xCrossRefGoogle Scholar
DiPietro, J. A., Hodgson, D. M., Costigan, K. A., & Johnson, T. R. B. (1996b). Fetal antecedents of infant temperament. Child Development, 67, 2568–2583. doi:10.1111/j.1467-8624.1996.tb01875.xCrossRefGoogle Scholar
DiPietro, J. A., Kivlighan, K. T., Costigan, K. A., Rubin, S. E., Shiffler, D. E., Henderson, J. L., & Pillion, J. P. (2010). Prenatal antecedents of newborn neurological maturation. Child Development, 81, 115–130. doi:10.1111/j.1467-8624.2009.01384.xCrossRefGoogle ScholarPubMed
DiPietro, J. A., Voegtline, K. M., Pater, H. A., & Costigan, K. A. (2018). Predicting child temperament and behavior from the fetus. Development and Psychopathology, 30, 855–870. doi:10.1017/S0954579418000482CrossRefGoogle ScholarPubMed
Doyle, C., & Cicchetti, D. (2018). Future directions in prenatal stress research: Challenges and opportunities related to advancing our understanding of prenatal developmental origins of risk for psychopathology. Development and psychopathology, 30, 721–724. doi:10.1017/S095457941800069XCrossRefGoogle ScholarPubMed
Doyle, C., Werner, E., Feng, T., Lee, S., Altemus, M., Isler, J. R., & Monk, C. (2015). Pregnancy distress gets under fetal skin: Maternal ambulatory assessment & sex differences in prenatal development. Developmental Psychobiology, 57, 855–870. doi:10.1002/dev.21317CrossRefGoogle ScholarPubMed
Emory, E. K., & Noonan, J. R. (1984). Fetal cardiac responding: A correlate of birth weight and neonatal behavior. Child Development, 55, 1651–1657. doi:10.2307/1130035CrossRefGoogle ScholarPubMed
Figueiredo, B., Pinto, T. M., Pacheco, A., & Field, T. (2017). Fetal heart rate variability mediates prenatal depression effects on neonatal neurobehavioral maturity. Biological Psychology, 123, 294–301. doi:10.1016/j.biopsycho.2016.10.013CrossRefGoogle ScholarPubMed
Forman, D. R., O'Hara, M. W., Larsen, K., Coy, K. C., Gorman, L. L., & Stuart, S. (2003). Infant emotionality: Observational methods and the validity of maternal reports. Infancy, 4, 541–565. doi:10.1207/S15327078IN0404_08CrossRefGoogle Scholar
Gartstein, M. A., & Rothbart, M. K. (2003). Studying infant temperament via the Revised Infant Behavior Questionnaire. Infant Behavior and Development, 26, 64–86. doi:10.1016/S0163-6383(02)00169-8CrossRefGoogle Scholar
Glover, V., & Hill, J. (2012). Sex differences in the programming effects of prenatal stress on psychopathology and stress responses: An evolutionary perspective. Physiology and Behavior, 106, 736–740. doi:10.1016/j.physbeh.2012.02.011CrossRefGoogle Scholar
Glynn, L. M., Howland, M. A., Sandman, C. A., Davis, E. P., Phelan, M., Baram, T. Z., & Stern, H. S. (2018). Prenatal maternal mood patterns predict child temperament and adolescent mental health. Journal of Affective Disorders, 228, 83–90. doi:10.1016/j.jad.2017.11.065CrossRefGoogle ScholarPubMed
Glynn, L. M., & Sandman, C. A. (2012). Sex moderates associations between prenatal glucocorticoid exposure and human fetal neurological development. Developmental Science, 15, 601–610. doi:10.1111/j.1467-7687.2012.01159.xCrossRefGoogle ScholarPubMed
Gunnar, M. R. (1990). The psychobiology of infant temperament. In Colombo, J. & Fagan, J. (Eds.), Individual differences in infancy: Reliability, stability and prediction (pp. 387–410). Hillsdale, NJ: Erlbaum.Google Scholar
Hane, A. A., Fox, N. A., Polak-Toste, C., Ghera, M. M., & Guner, B. M. (2006). Contextual basis of maternal perceptions of infant temperament. Developmental Psychology, 42, 1077–1088. doi:10.1037/0012-1649.42.6.1077CrossRefGoogle ScholarPubMed
Hobel, C. J. (1982). Identifying the patient at risk. In Bolognese, S. R. J. & Schneider, R. J. (Eds.), Perinatal medicine: Management of the high risk fetus and neonate (pp. 3–28). Baltimore, MA: Williams & Wilkins.Google Scholar
Howland, M. A., Sandman, C. A., & Glynn, L. M. (2017). Developmental origins of the human hypothalamic-pituitary-adrenal axis. Expert Review of Endocrinology and Metabolism, 12, 321–339. doi:10.1080/17446651.2017.1356222CrossRefGoogle ScholarPubMed
Johnson, V. C., Olino, T. M., Klein, D. N., Dyson, M. W., Bufferd, S. J., Durbin, C. E., … Hayden, E. P. (2016). A longitudinal investigation of predictors of the association between age 3 and age 6 behavioural inhibition. Journal of Research in Personality, 63, 51–61. doi:10.1016/j.jrp.2016.04.008CrossRefGoogle ScholarPubMed
Kim, D. J., Davis, E. P., Sandman, C. A., Sporns, O., O'Donnell, B. F., Buss, C., & Hetrick, W. P. (2014). Longer gestation is associated with more efficient brain networks in preadolescent children. NeuroImage, 100, 619–627. doi:10.1016/j.neuroimage.2014.06.048CrossRefGoogle ScholarPubMed
Kingston, D., McDonald, S., Austin, M. P., & Tough, S. (2015). Association between prenatal and postnatal psychological distress and toddler cognitive development: A systematic review. PLoS ONE, 10, e0126929. doi:10.1371/journal.pone.0126929CrossRefGoogle ScholarPubMed
Kinsella, M. T., & Monk, C. (2009). Impact of maternal stress, depression and anxiety on fetal neurobehavioral development. Clinical Obstetrics and Gynecology, 52, 425–440. doi:10.1097/GRF.0b013e3181b52df1CrossRefGoogle ScholarPubMed
Kisilevsky, B. S., & Low, J. A. (1998). Human fetal behavior: 100 years of study. Developmental Review, 18, 1–29. doi:10.1006/drev.1998.0452CrossRefGoogle Scholar
Lüdecke, D. (2020). sjstats: Collection of convenient functions for common statistical computations. R Package Version 0.17.8.Google Scholar
Madigan, S., Oatley, H., Racine, N., Fearon, R. M. P., Schumacher, L., Akbari, E., … Tarabulsy, G. M. (2018). A meta-analysis of maternal prenatal depression and anxiety on child socioemotional development. Journal of the American Academy of Child and Adolescent Psychiatry, 22, 491–495. doi:10.1016/j.jaac.2018.06.012Google Scholar
Martin, C. B. (1978). Regulation of the fetal heart rate and genesis of FHR patterns. Seminars in perinatology, 2, 131–146.Google ScholarPubMed
Masten, A. S., & Cicchetti, D. (2010). Developmental cascades. Development and Psychopathology, 22, 491–495. doi:10.1017/S0954579410000222CrossRefGoogle ScholarPubMed
Monk, C., Fifer, W. P., Myers, M. M., Bagiella, E., Duong, J. K., Chen, I. S., … Altincatal, A. (2011). Effects of maternal breathing rate, psychiatric status, and cortisol on fetal heart rate. Developmental Psychobiology, 53, 221–233. doi:10.1002/dev.20513CrossRefGoogle ScholarPubMed
Monk, C., Fifer, W. P., Myers, M. M., Sloan, R. P., Trien, L., & Hurtado, A. (2000). Maternal stress responses and anxiety during pregnancy: Effects on fetal heart rate. Developmental Psychobiology, 36, 67–77. doi:10.1002/(SICI)1098-2302(200001)36:13.0.CO;2-C3.0.CO;2-C>CrossRefGoogle ScholarPubMed
Monk, C., Myers, M. M., Sloan, R. P., Ellman, L. M., & Fifer, W. P. (2003). Effects of women's stress-elicited physiological activity and chronic anxiety on fetal heart rate. Journal of Developmental and Behavioral Pediatrics, 24, 32–38. doi:10.1097/00004703-200302000-00008CrossRefGoogle ScholarPubMed
Monk, C., Sloan, R. P., Myers, M. M., Ellman, L., Werner, E., Jeon, J., … Fifer, W. P. (2004). Fetal heart rate reactivity differs by women's psychiatric status: An early marker for developmental risk? Journal of the American Academy of Child and Adolescent Psychiatry, 43, 283–290. doi:10.1097/00004583-200403000-00009CrossRefGoogle ScholarPubMed
Nijhuis, J. G., Swaab, , Visser, , Heuser, , Finch, , Brosens, , & Eskes, . (2003). Fetal behavior. Neurobiology of Aging, 24, S41–S46. doi:10.1016/S0197-4580(03)00054-XCrossRefGoogle ScholarPubMed
O'Connor, T. G., Monk, C., & Burke, A. S. (2016). Maternal affective illness in the perinatal period and child development: Findings on developmental timing, mechanisms, and intervention. Current Psychiatry Reports, 18, 24. doi:10.1007/s11920-016-0660-yCrossRefGoogle ScholarPubMed
O'Donnell, K. J., Glover, V., Barker, E. D., & O'Connor, T. G. (2014). The persisting effect of maternal mood in pregnancy on childhood psychopathology. Development and Psychopathology, 26, 393–403. doi:10.1017/S0954579414000029CrossRefGoogle ScholarPubMed
O'Donnell, K. J., & Meaney, M. J. (2017). Fetal origins of mental health: The developmental origins of health and disease hypothesis. American Journal of Psychiatry, 174, 319–328. doi:10.1176/appi.ajp.2016.16020138CrossRefGoogle ScholarPubMed
Parade, S. H., & Leerkes, E. M. (2008). The reliability and validity of the Infant Behavior Questionnaire-Revised. Infant Behavior and Development, 31, 637–646. doi:10.1016/j.infbeh.2008.07.009CrossRefGoogle ScholarPubMed
Putnam, S. P., Rothbart, M. K., & Gartstein, M. A. (2008). Homotypic and heterotypic continuity of fine-grained temperament during infancy, toddlerhood, and early childhood. Infant and Child Development, 17, 387–405. doi:10.1002/icd.582CrossRefGoogle Scholar
Rice, F., Harold, G. T., Boivin, J., Van Den Bree, M., Hay, D. F., & Thapar, A. (2010). The links between prenatal stress and offspring development and psychopathology: Disentangling environmental and inherited influences. Psychological Medicine, 40, 335–345. doi:10.1017/S0033291709005911CrossRefGoogle ScholarPubMed
Rosseel, Y. (2012). Lavaan: An R package for structural equation modeling. Journal of Statistical Software, 48, 1–36. doi:10.18637/jss.v048.i02CrossRefGoogle Scholar
Rothbart, M. K., & Bates, J. E. (2007). Temperament. Handbook of Child Psychology, In Damon, W. & Eisenberg, N. (Eds.), Handbook of child psychology: Vol. 3. Social, emotional, and personality development (pp. 105–176). New York: Wiley.Google Scholar
Sandman, C. A. (2015). Mysteries of the human fetus revealed. Monographs of the Society for Research in Child Development, 80, 124–137. doi:10.1111/mono.12190CrossRefGoogle ScholarPubMed
Sandman, C. A., Buss, C., Head, K., & Davis, E. P. (2015). Fetal exposure to maternal depressive symptoms is associated with cortical thickness in late childhood. Biological Psychiatry, 77, 324–334. doi:10.1016/j.biopsych.2014.06.025CrossRefGoogle ScholarPubMed
Sandman, C. A., Cordova, C. J., Davis, E. P., Glynn, L. M., & Buss, C. (2011). Patterns of fetal heart rate response at 30 weeks gestation predict size at birth. Journal of Developmental Origins of Health and Disease, 2, 212–217. doi:10.1017/S2040174411000250CrossRefGoogle ScholarPubMed
Sandman, C. A., Glynn, L. M., & Davis, E. P. (2013). Is there a viability-vulnerability tradeoff? Sex differences in fetal programming. Journal of Psychosomatic Research, 75, 327–335. doi:10.1016/j.jpsychores.2013.07.009CrossRefGoogle Scholar
Sandman, C. A., Glynn, L. M., & Davis, E. P. (2016). Neurobehavioral consequences of fetal exposure to gestational stress. In B. S. Kisilevsky & N. Reissland (Eds.), Fetal Development: Research on Brain and Behavior, Environmental Influences, and Emerging Technologies, (pp. 229–265). New York: Springer.CrossRefGoogle Scholar
Sandman, C. A., Glynn, L., Wadhwa, P. D., Chicz-DeMet, A., Porto, M., & Garite, T. (2003). Maternal hypothalamic-pituitary-adrenal disregulation during the third trimester influences human fetal responses. Developmental Neuroscience, 25, 41–49. doi:10.1159/000071467CrossRefGoogle ScholarPubMed
Sandman, C. A., Wadhwa, P. D., Chicz-DeMet, A., Porto, M., & Garite, T. J. (1999). Maternal corticotropin-releasing hormone and habituation in the human fetus. Developmental Psychobiology, 34, 163–173. doi: 10.1002/(sici)1098-2302(199904)34:33.0.co;2-93.0.CO;2-9>CrossRefGoogle ScholarPubMed
Sandman, C. A., Wadhwa, P., Hetrick, W., Porto, M., & Peeke, H. V. S. (1997). Human fetal heart rate dishabituation between thirty and thirty-two weeks gestation. Child Development, 68, 1031–1040. doi:10.1111/j.1467-8624.1997.tb01982.xCrossRefGoogle ScholarPubMed
Santor, D. A., & Coyne, J. C. (1997). Shortening the CES-D to improve its ability to detect cases of depression. Psychological Assessment, 9, 233–243. doi:10.1037/1040-3590.9.3.233CrossRefGoogle Scholar
Snidman, N., Kagan, J., Riordan, L., & Shannon, D. C. (1995). Cardiac function and behavioral reactivity during infancy. Psychophysiology, 32, 199–207. doi:10.1111/j.1469-8986.1995.tb02949.xCrossRefGoogle ScholarPubMed
Spielberger, C. D., Jacobs, G., Crane, R., & Russell, S. (1979). Preliminary manual for the state-trait personality inventory (STPI). Unpublished Manuscript University of South Florida Tampa. doi:10.1111/j.1744-7402.2009.02409.xCrossRefGoogle Scholar
Spielberger, C. D., & Reheiser, E. C. (2009). Assessment of emotions: Anxiety, anger, depression, and curiosity. Applied Psychology: Health and Well-Being, 1, 271–302. doi:10.1111/j.1758-0854.2009.01017.xGoogle Scholar
Thomason, M. E., Hect, J., Waller, R., Manning, J. H., Stacks, A. M., Beeghly, M., … Romero, R. (2018). Prenatal neural origins of infant motor development: Associations between fetal brain and infant motor development. Development and Psychopathology, 30, 763–772. doi:10.1017/S095457941800072XCrossRefGoogle ScholarPubMed
van den Heuvel, M. I., & Thomason, M. E. (2016). Functional connectivity of the human brain in utero. Trends in Cognitive Sciences, 20, 931–939. doi:10.1016/j.tics.2016.10.001CrossRefGoogle ScholarPubMed
Van Leeuwen, P., Lange, S., Bettermann, H., Grönemeyer, D., & Hatzmann, W. (1999). Fetal heart rate variability and complexity in the course of pregnancy. Early Human Development, 54, 259–269. doi:10.1016/S0378-3782(98)00102-9CrossRefGoogle ScholarPubMed
Weinstock, M. (2008). The long-term behavioural consequences of prenatal stress. Neuroscience and Biobehavioral Reviews, 32, 1073–1086. doi:10.1016/j.neubiorev.2008.03.002CrossRefGoogle ScholarPubMed
Werner, E. A., Myers, M. M., Fifer, W. P., Cheng, B., Fang, Y., Allen, R., & Monk, C. (2007). Prenatal predictors of infant temperament. 49, 474-484. Developmental Psychobiology, doi:10.1002/dev.20232CrossRefGoogle ScholarPubMed
Yoshizato, T., Koyanagi, T., Takashima, T., Satoh, S., Akazawa, K., & Nakano, H. (1994). The relationship between age-related heart rate changes and developing brain function: a model of anencephalic human fetuses in utero. Early Human Development, 36, 101–112. doi:10.1016/0378-3782(94)90037-XCrossRefGoogle Scholar