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Growth and Development Following Prenatal Stress Exposure in Primates: An Examination of Ontogenetic Vulnerability
Abstract
Previous studies have found that stressful events during pregnancy can influence the developing fetus, resulting in attentional and neuromotor problems. This prospective study examined whether periods of vulnerability exist for neurobehavioral impairments associated with prenatal stress, using a nonhuman primate model. Twenty-eight rhesus monkey infants were born to mothers in 3 groups: (1) early gestation stress involving mild psychological stress from gestational days 45–90, (2) mid-late gestation stress from days 90–145, and (3) undisturbed controls. Infants were separated from their mothers on days 4, 9, 15, and 22 (±1) postpartum for growth and neurobehavioral assessments. Results indicated that infants from the early gestation stress condition weighed less than infants from mothers stressed during mid-late gestation. Moreover, whereas both groups scored lower than controls on measures of attention and neuromotor maturity, early gestation stress was associated with more pronounced and more pervasive motor impairments than mid-late gestation stress. These results suggest sensitivity to prenatal stress effects peaks during early gestation, tapering off during mid-late gestation. Clarifying the period of greatest vulnerability to prenatal stress moves toward elucidating the underlying mechanism for prenatal stress effects and may lead to more successful intervention and/or prevention.
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“This possibility has been supported by observations in rhesus monkeys, where prenatal exposure to the same stressor had greater effects on postnatal motor development if it occurred earlier in gestation, when neuronal migration was at its peak, than if it occurred in mid- to late gestation, when synaptogenesis was at its peak (Schneider et al., 1999).”
From High pregnancy anxiety during mid-gestation is associated with decreased gray matter density in 6-9-year-old children. (2010) · cites this paper as Schneider et al., 1999
In the citing paper
“Given that brain regions undergoing the most extensive maturation are thought to be the most vulnerable to insult (Schneider et al., 1999), we might expect differing effects of ELS based on developmental timing.”
From The effects of early life stress on reward processing (2018) · cites this paper as Schneider et al., 1999
Citations
Cites
Simultaneous Statistical Inference
Miller, R. G. (1981) · Springer series in statistics · doi:10.1007/978-1-4613-8122-8 · Cited by 5,608
Comparison of two modes of stress measurement: Daily hassles and uplifts versus major life events
Kanner, A. D., Coyne, J. C., Schaefer, C. A., & Lazarus, R. S. (1981) · Journal of Behavioral Medicine · doi:10.1007/bf00844845 · Cited by 3,128
Synaptogenesis in the Prefrontal Cortex of Rhesus Monkeys
Bourgeois, J.-P., Goldman-Rakic, P. S., & Rakic, P. (1994) · Cerebral Cortex · doi:10.1093/cercor/4.1.78 · Cited by 687
Bourgeois, J., & Rakic, P. (1993) · The Journal of Neuroscience · doi:10.1523/jneurosci.13-07-02801.1993 · Cited by 567
Moderate Prenatal Alcohol Exposure: Effects on Child IQ and Learning Problems at Age 7 1/2 Years
Streissguth, A. P., Barr, H. M., & Sampson, P. D. (1990) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.1990.tb01224.x · Cited by 547
Limits of Neurogenesis in Primates
RAKIC, P. T. (1985) · Science · doi:10.1126/science.3975601 · Cited by 510
Disorders of Neuronal Migration
Barth, P. G. (1987) · Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques · doi:10.1017/s031716710002610x · Cited by 433
Norbeck, J. S., & Tilden, V. P. (1983) · Journal of Health and Social Behavior · doi:10.2307/2136301 · Cited by 423
Sensitive periods in development: Structural characteristics and causal interpretations.
Bornstein, M. H. (1989) · Psychological Bulletin · doi:10.1037/0033-2909.105.2.179 · Cited by 377
Postnatal development of monoamine content and synthesis in the cerebral cortex of rhesus monkeys
Goldman, P. S., & Brown, R. M. (1982) · Developmental Brain Research · doi:10.1016/0165-3806(82)90146-8 · Cited by 285
Conceptualizations, measurement, and effects of prenatal maternal stress on birth outcomes
Lobel, M. (1994) · Journal of Behavioral Medicine · doi:10.1007/bf01857952 · Cited by 256
Psychosocial stress in pregnancy and its relation to low birth weight.
Newton, R., & Hunt, L. P. (1984) · BMJ · doi:10.1136/bmj.288.6425.1191 · Cited by 256
Changes in synaptic density in motor cortex of rhesus monkey during fetal and postnatal life
Zecevic, N., Bourgeois, J.-P., & Rakic, P. (1989) · Developmental Brain Research · doi:10.1016/0165-3806(89)90124-7 · Cited by 253
Long‐term effects of prenatal stress on HPA axis activity in juvenile rhesus monkeys
Clarke, A. S., Wittwer, D. J., Abbott, D. H., & Schneider, M. L. (1994) · Developmental Psychobiology · doi:10.1002/dev.420270502 · Cited by 245
Self-citationStress, anxiety, and birth outcomes: A critical review of the evidence.
Istvan, J. A. (1986) · Psychological Bulletin · doi:10.1037/0033-2909.100.3.331 · Cited by 216
Timing of Neuroblast Multiplication in Developing Human Brain
Dobbing, J., & Sands, J. (1970) · Nature · doi:10.1038/226639a0 · Cited by 206
Prenatal alcohol exposure and infant information processing ability.
Jacobson, S., Jacobson, J. L., Sokol, R. J., Martier, S., & Ager, J. W. (1993) · PubMed · Cited by 196
Prenatal stress has long‐term effects on behavioral responses to stress in juvenile rhesus monkeys
Clarke, A. S., & Schneider, M. L. (1993) · Developmental Psychobiology · doi:10.1002/dev.420260506 · Cited by 187
Self-citationPhysical growth of the rhesus monkey (Macaca mulatta)
WAGENEN, G. V., & CATCHPOLE, H. R. (1956) · American Journal of Physical Anthropology · doi:10.1002/ajpa.1330140219 · Cited by 180
Psychosocial influences on new born outcomes: A controlled prospective study
Pagel, M. D., SMILKSTEIN, G., Regen, H., & Montano, D. (1990) · Social Science & Medicine · doi:10.1016/0277-9536(90)90158-o · Cited by 180
Abnormalities of Pregnancy as a Function of Anxiety and Life Stress
Gorsuch, R. L., & Key, M. K. (1974) · Psychosomatic Medicine · doi:10.1097/00006842-197407000-00009 · Cited by 178
Schneider, M. L. (1992) · Developmental Psychobiology · doi:10.1002/dev.420250706 · Cited by 158
Self-citationSchneider, M. L., Coe, C. L., & Lubach, G. R. (1992) · Developmental Psychobiology · doi:10.1002/dev.420250604 · Cited by 145
Self-citationSchneider, M. L., & Suomi, S. J. (1992) · Infant Behavior and Development · doi:10.1016/0163-6383(92)80021-l · Cited by 141
Self-citationRepeated Social Stress during Pregnancy Impairs Neuromotor Development of the Primate Infant
Schneider, M. L., & Coe, C. L. (1993) · Journal of Developmental & Behavioral Pediatrics · doi:10.1097/00004703-199304000-00002 · Cited by 139
Self-citationNeonatal Behavioral Assessment Scale, 2nd ed.
Pavlakis, S. G. (1986) · Neurology · doi:10.1212/wnl.36.6.877 · Cited by 131
Experimental studies on congenital malformations
WILSON, J. G. (1959) · Journal of Chronic Diseases · doi:10.1016/0021-9681(59)90026-8 · Cited by 128
Synaptogenesis in Monkey Somatosensory Cortex
Zečević, N., & RAKIC, P. T. (1991) · Cerebral Cortex · doi:10.1093/cercor/1.6.510 · Cited by 122
Schneider, M. L. (1992) · Infant Behavior and Development · doi:10.1016/0163-6383(92)80009-j · Cited by 109
Self-citationPsychobiological Aspects of Life Stress
Frankenhaeuser, M. (1980) · Springer eBooks · doi:10.1007/978-1-4684-1042-6_10 · Cited by 106
Eyler, F. D., Behnke, M., Conlon, M., Woods, N. S., & Wobie, K. (1998) · PEDIATRICS · doi:10.1542/peds.101.2.237 · Cited by 104
Mechanism of nitrofen teratogenesis.
Manson, J. M. (1986) · Environmental Health Perspectives · doi:10.1289/ehp.8670137 · Cited by 93
Schneider, M. L., Moore, C. F., Suomi, S. J., & Champoux, M. (1991) · American Journal of Primatology · doi:10.1002/ajp.1350250302 · Cited by 86
Self-citationHormonal Response to Stress in the Squirrel Monkey (Saimiri sciureus)
Coe, C. L., Mendoza, S. P., Davidson, J. M., Smith, E. R., Dallman, M. F., & Levine, S. D. (2008) · Neuroendocrinology · doi:10.1159/000122792 · Cited by 83
Prenatal stress alters brain biogenic amine levels in primates
Schneider, M. L., Clarke, A. S., Kraemer, G. W., Roughton, E. C., Lubach, G. R., Rimm‐Kaufman, S. E., Schmidt, D. E., & Ebert, M. H. (1998) · Development and Psychopathology · doi:10.1017/s0954579498001679 · Cited by 81
Self-citationMaternal anxiety and neonatal wellbeing
Crandon, A. J. (1979) · Journal of Psychosomatic Research · doi:10.1016/0022-3999(79)90015-1 · Cited by 80
Childbirth education, maternal attitudes, and delivery
Zax, M., Sameroff, A. J., & Farnum, J. E. (1975) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(75)90525-6 · Cited by 74
Delayed Object Permanence Development in Prenatally Stressed Rhesus Monkey Infants (Macaca Mulatta)
Schneider, M. L. (1992) · The Occupational Therapy Journal of Research · doi:10.1177/153944929201200203 · Cited by 70
Self-citationNewell‐Morris, L. L., Fahrenbruch, C. E., & Sackett, G. P. (2009) · Biology of the Neonate · doi:10.1159/000243104 · Cited by 66
Schneider, M. L., Roughton, E. C., & Lubach, G. R. (1997) · Child Development · doi:10.1111/j.1467-8624.1997.tb01959.x · Cited by 63
Self-citationPsychological factors in preterm labor: critical review and theoretical synthesis
Omer, H., & Everly, G. S. (1988) · American Journal of Psychiatry · doi:10.1176/ajp.145.12.1507 · Cited by 55
Clarke, A. S., Soto, A. A., Bergholz, T. M., & Schneider, M. L. (1996) · Infant Behavior and Development · doi:10.1016/s0163-6383(96)90006-5 · Cited by 50
Self-citationSurvey of Protocols for Nursery-Rearing Infant Macaques
Ruppenthal, G. C. (1979) · Springer eBooks · doi:10.1007/978-1-4684-3477-4_13 · Cited by 49
Neonatal behavioral assessment.
Rs, I. (1990) · PubMed · Cited by 32
Farber, E. A., Vaughn, B. E., & Egeland, B. R. (1981) · Early Human Development · doi:10.1016/0378-3782(81)90034-7 · Cited by 28
The development of the frontal lobe. A view from the rear of the brain.
RAKIC, P. T. (1995) · PubMed · Cited by 28
Maternal Endocrine Activation During Pregnancy Alters Neurobehavioral State in Primate Infants
Roughton, E. C., Schneider, M. L., Bromley, L. J., & Coe, C. L. (1998) · American Journal of Occupational Therapy · doi:10.5014/ajot.52.2.90 · Cited by 26
Self-citationNeurophysiology: Plasticity in the visual cortex
Sillito, A. M. (1983) · Nature · doi:10.1038/303477a0 · Cited by 17
Maternal Stress during Pregnancy and the Behavior of the Offspring
HUTTUNEN, M. O. (1989) · Springer eBooks · doi:10.1007/978-1-4684-5634-9_15 · Cited by 12
Toward a more temporal view of organism-environment interaction.
Sackett, G. P. (2004) · American Psychological Association eBooks · doi:10.1037/10100-001 · Cited by 7
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Talge, N. M., Neal, C., Glover, V., & the Early Stress, T. R. A. P. S. N. F. A. N. E. O. C. A. A. M. H. (2007) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2006.01714.x · Cited by 1,349
Van den Bergh, B. R. H., Mulder, E. J. H., Mennes, M., & Glover, V. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.10.007 · Cited by 1,104
Prenatal maternal stress: effects on pregnancy and the (unborn) child
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Metadata
- Authors
- Schneider, M. L., Roughton, E. C., Koehler, A. J., & Lubach, G. R.
- Affiliations
- University of Wisconsin–Madison (US)
- ORCID
- Lubach, Gabriele R
- Venue
- Child Development
- Publisher
- Oxford University Press (OUP)
- Published
- 1999-03-01
- Volume
- 70
- Issue
- 2
- Pages
- 263-274
- ISSN
- 0009-3920 (ISSN-L)
- 1467-8624
- OpenAlex
- W1991706811
- Cited by
- 267
- References
- 50
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 1 · 2023: 2 · 2022: 3 · 2021: 6 · 2020: 7 · 2019: 11 · 2018: 10 · 2017: 5 · 2016: 7 · 2015: 13 · 2014: 12 · 2013: 12 · 2012: 21
- FWCI
- 12.66
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- Locations
- Child Development (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r03mh048417-02)
- U.S. Public Health Service (MCJ-009102)
- National Institute on Alcohol Abuse and Alcoholism (AA10079, R01AA010079)
- National Institute of Mental Health (MH48417)
- Topics
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Prenatal Substance Exposure Effects
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Keywords
- prenatal stress, rhesus monkeys, infant growth, neurobehavioral development, attention, neuromotor development, early pregnancy, maternal stress, maternal separation
- MeSH terms
- Animals, Animals, Newborn, Animals, Suckling, Birth Weight, Developmental Disabilities, Female, Handling, Psychological, Hydrocortisone, Macaca mulatta, Male, Motor Skills, Orientation, Pregnancy, Prenatal Exposure Delayed Effects, Stress, Psychological, Maternal Exposure
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