The DOI matches its Crossref record; 8 of the 8 references it cites were found in a registry or an index.
Influences of Caregiving on Development: A Sensitive Period for Biological Embedding of Predictability and Safety Cues
Abstract
Across species, caregivers exert a powerful influence on the neural and behavioral development of offspring. Increasingly, both animal and human research has highlighted specific patterns in caregivers’ behavior that may be especially important early in life, as well as neurobiological mechanisms linking early caregiving experiences with long-term affective behavior. Here we delineate evidence for an early sensitive period during infancy and toddlerhood when caregiver inputs that are predictable and associated with safety may become biologically embedded via influences on corticolimbic circuitry involved in emotion regulation. We propose that these caregiver signals prime corticolimbic circuitry to be receptive to later stage-specific caregiver influences, such as caregivers’ external regulation of children’s emotional reactivity. Following adversity that disrupts the predictability and safety associated with caregivers during this sensitive period, accelerated maturation of children’s corticolimbic circuitry may foreshorten the protracted period of plasticity and caregiver influence that is characteristic of humans. This work has implications for both prevention and intervention efforts targeting children exposed to adversity early in life.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“Decades of research have established infancy and early childhood as a period of particular importance, including the positive impacts of sensitive caregiving, access to material resources, and safe, stimulating environments on adaptive outcomes in childhood and beyond.5–8”
From Prenatal Social Determinants of Health: Narrative review of maternal environments and neonatal brain development (2024) · cites this paper as [6]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Attachment and development: A prospective, longitudinal study from birth to adulthood
Sroufe, L. A. (2005) · Attachment & Human Development · doi:10.1080/14616730500365928 · Cited by 1,685
Feldman, R. (2007) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2006.01701.x · Cited by 1,317 · cited 1×
“Indeed, both contingency of caregivers’ responsivity to infants (Gunnar, 1980) and synchrony in infantcaregiver behavior are key predictors of children’s developmental outcomes (Feldman, 2007).”
BackgroundCognitive Recovery in Socially Deprived Young Children: The Bucharest Early Intervention Project
Nelson, C. A., Zeanah, C. H., Fox, N. A., Marshall, P. J., Smyke, A. T., & Guthrie, D. (2007) · Science · doi:10.1126/science.1143921 · Cited by 951 · cited 1×
“…randomly assigned either to be placed in foster care or to remain in institutionalized care, have demonstrated that receiving stable and nurturing caregiving input in the first years of life is particularly influential for both short- and long-term developmental outcomes (Nelson et al., 2007).”
BackgroundMANLY, J. T., KIM, J. E., ROGOSCH, F. A., & CICCHETTI, D. (2001) · Development and Psychopathology · doi:10.1017/s0954579401004023 · Cited by 789
Hostinar, C. E., Sullivan, R. M., & Gunnar, M. R. (2014) · Psychological Bulletin · doi:10.1037/a0032671 · Cited by 739
McLaughlin, K. A., Sheridan, M. A., Tibu, F., Fox, N. A., Zeanah, C. H., & Nelson, C. A. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1423363112 · Cited by 426
Maternal presence serves as a switch between learning fear and attraction in infancy
Moriceau, S., & Sullivan, R. M. (2006) · Nature Neuroscience · doi:10.1038/nn1733 · Cited by 386
Critical period for acoustic preference in mice
Yang, E.-J., Lin, E. W., & Hensch, T. K. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1200705109 · Cited by 102
Research works printed but not linked: 26
- Bath K. G., Manzano-Nieves G., Goodwill H. (2016). Early life stress accelerates behavioral and neural maturation of the hippocampus in male mice. Hormones and Behavior, 82, 64–71. https://doi.org/10.1016/j.yhbeh.2016.04.010 · DOI
- Callaghan B. L., Gee D. G., Gabard-Durnam L., Telzer E. H., Humphreys K. L., Goff B., Shapiro M., Flannery J., Lumian D. S., Fareri D. S., Caldera C., Tottenham N. (2019). Decreased amygdala reactivity to parent cues protects against anxiety following early adversity: An examination across 3 years. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 4(7), 664–671. https://doi.org/10.1016/j.bpsc.2019.02.001 · DOI
- 10.1038/npp.2015.204 · DOI · Paper page
- Callaghan B. L., Tottenham N. (2016b). The stress acceleration hypothesis: Effects of early-life adversity on emotion circuits and behavior. Current Opinion in Behavioral Sciences, 7, 76–81. https://doi.org/10.1016/j.cobeha.2015.11.018 · DOI · Paper page
- 10.1002/dev.21969 · DOI
- Curley J. P., Champagne F. A. (2016). Influence of maternal care on the developing brain: Mechanisms, temporal dynamics and sensitive periods. Frontiers in Neuroendocrinology, 40, 52–66. https://doi.org/10.1016/j.yfrne.2015.11.001 · DOI
- 10.1007/s12110-009-9063-7 · DOI
- Gabard-Durnam L., McLaughlin K. A. (2020). Sensitive periods in human development: Charting a course for the future. Current Opinion in Behavioral Sciences, 36, 120–128. https://doi.org/10.1016/j.cobeha.2020.09.003 · DOI
- Gee D. G. (2016). Sensitive periods of emotion regulation: Influences of parental care on frontoamygdala circuitry and plasticity: Sensitive periods of emotion regulation. New Directions for Child and Adolescent Development, 2016(153), 87–110. https://doi.org/10.1002/cad.20166 · DOI
- Gee D. G., Gabard-Durnam L., Telzer E. H., Humphreys K. L., Goff B., Shapiro M., Flannery J., Lumian D. S., Fareri D. S., Caldera C., Tottenham N. (2014). Maternal buffering of human amygdala-prefrontal circuitry during childhood but not during adolescence. Psychological Science, 25(11), 2067–2078. https://doi.org/10.1177/0956797614550878 · DOI · Paper page
- Gee D. G., Gabard-Durnam L. J., Flannery J., Goff B., Humphreys K. L., Telzer E. H., Hare T. A., Bookheimer S. Y., Tottenham N. (2013). Early developmental emergence of human amygdala-prefrontal connectivity after maternal deprivation. Proceedings of the National Academy of Sciences, USA, 110(39), 15638–15643. https://doi.org/10.1073/pnas.1307893110 · DOI · Paper page
- Glynn L. M., Baram T. Z. (2019). The influence of unpredictable, fragmented parental signals on the developing brain. Frontiers in Neuroendocrinology, 53, Article 100736. https://doi.org/10.1016/j.yfrne.2019.01.002 · DOI
- 10.1007/s00429-018-1720-3 · DOI
- 10.1007/978-1-4684-1042-6_6 · DOI
- Lieberman A. F., 2015, Don’t hit my mommy! A manual for child-parent psychotherapy with young children exposed to violence and other trauma
- Malter Cohen M., Jing D., Yang R. R., Tottenham N., Lee F. S., Casey B. J. (2013). Early-life stress has persistent effects on amygdala function and development in mice and humans. Proceedings of the National Academy of Sciences, USA, 110(45), 18274–18278. https://doi.org/10.1073/pnas.1310163110 · DOI · Paper page
- Manzano Nieves G., Bravo M., Baskoylu S., Bath K. G. (2020). Early life adversity decreases pre-adolescent fear expression by accelerating amygdala PV cell development. ELife, 9, Article e55263. https://doi.org/10.7554/eLife.55263 · DOI
- Meyer H. C., Odriozola P., Cohodes E. M., Mandell J. D., Li A., Yang R., Hall B. S., Haberman J. T., Zacharek S. J., Liston C., Lee F. S., Gee D. G. (2019). Ventral hippocampus interacts with prelimbic cortex during inhibition of threat response via learned safety in both mice and humans. Proceedings of the National Academy of Sciences, USA, 116(52), 26970–26979. https://doi.org/10.1073/pnas.1910481116 · DOI
- Opendak M., Robinson-Drummer P., Blomkvist A., Zanca R. M., Wood K., Jacobs L., Chan S., Tan S., Woo J., Venkataraman G., Kirschner E., Lundström J. N., Wilson D. A., Serrano P. A., Sullivan R. M. (2019). Neurobiology of maternal regulation of infant fear: The role of mesolimbic dopamine and its disruption by maltreatment. Neuropsychopharmacology, 44, 1247–1257. https://doi.org/10.1038/s41386-019-0340-9 · DOI
- Opendak M., Theisen E., Blomkvist A., Hollis K., Lind T., Sarro E., Lundström J. N., Tottenham N., Dozier M., Wilson D. A., Sullivan R. M. (2020). Adverse caregiving in infancy blunts neural processing of the mother. Nature Communications, 11(1), 1119. https://doi.org/10.1038/s41467-020-14801-3 · DOI
- Perry R., Sullivan R. M. (2014). Neurobiology of attachment to an abusive caregiver: Short-term benefits and long-term costs. Developmental Psychobiology, 56(8), 1626–1634. https://doi.org/10.1002/dev.21219 · DOI
- Robinson-Drummer P. A., Opendak M., Blomkvist A., Chan S., Tan S., Delmer C., Wood K., Sloan A., Jacobs L., Fine E., Chopra D., Sandler C., Kamenetzky G., Sullivan R. M. (2019). Infant trauma alters social buffering of threat learning: Emerging role of prefrontal cortex in preadolescence. Frontiers in Behavioral Neuroscience, 13, Article 132. https://doi.org/10.3389/fnbeh.2019.00132 · DOI
- Sanchez M. M., McCormack K. M., Howell B. R. (2015). Social buffering of stress responses in nonhuman primates: Maternal regulation of the development of emotional regulatory brain circuits. Social Neuroscience, 10(5), 512–526. https://doi.org/10.1080/17470919.2015.1087426 · DOI
- Singh-Taylor A., Molet J., Jiang S., Korosi A., Bolton J. L., Noam Y., Simeone K., Cope J., Chen Y., Mortazavi A., Baram T. Z. (2018). NRSF-dependent epigenetic mechanisms contribute to programming of stress-sensitive neurons by neonatal experience, promoting resilience. Molecular Psychiatry, 23(3), 648–657. https://doi.org/10.1038/mp.2016.240 · DOI · Paper page
- Tottenham N., Shapiro M., Flannery J., Caldera C., Sullivan R. M. (2019). Parental presence switches avoidance to attraction learning in children. Nature Human Behaviour, 3(10), 1070–1077. https://doi.org/10.1038/s41562-019-0656-9 · DOI
- 10.1146/annurev-psych-010814-015104 · DOI · Paper page
Cited by
Early deprivation alters structural brain development from middle childhood to adolescence
Sheridan, M. A., Mukerji, C. E., Wade, M., Humphreys, K. L., Garrisi, K., Goel, S., Patel, K., Fox, N. A., Zeanah, C. H., Nelson, C. A., et al. (2022) · Science Advances · doi:10.1126/sciadv.abn4316 · Cited by 84
Herzberg, M. P., & Smyser, C. D. (2024) · Pediatric Research · doi:10.1038/s41390-024-03345-7 · Cited by 22
The epigenetic impacts of pubertal acceleration following early caregiver disruptions
Jopling, E., Drury, S. S., Fox, N. A., Zeanah, C. H., & Nelson, C. A. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2504216122 · Cited by 2
Abdul Hamid, H., Lenihan, R., Ahern, E., Terracciano, A., Stephan, Y., & O'Súilleabháin, P. S. (2026) · Social Science & Medicine · doi:10.1016/j.socscimed.2026.119373 · Cited by 1
Metadata
- Authors
- Gee, D. G., & Cohodes, E. M.
- Venue
- Current Directions in Psychological Science
- Publisher
- SAGE Publications
- Published
- 2021-08-06
- Volume
- 30
- Issue
- 5
- Pages
- 376-383
- ISSN
- 0963-7214
- 1467-8721
- Cited by
- 119
- References
- 8
- Language
- en
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
Data sources
Bibliographic data: Semantic Scholar, OpenAlex, Crossref.
Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).
Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.