Indiscriminate Amygdala Response to Mothers and Strangers After Early Maternal Deprivation
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Background In altricial species, maternal stimuli have powerful effects on amygdala development and attachment-related behaviors. In humans, maternal deprivation has been associated with both "indiscriminate friendliness" toward non-caregiving adults and altered amygdala development. We hypothesized that maternal deprivation would be associated with reduced amygdala discrimination between mothers and strangers and increased parent report of indiscriminate friendliness behaviors.Methods Sixty-seven youths (33 previously institutionalized; 34 comparison; age-at-scan 4-17 years) participated in a functional magnetic resonance imaging experiment designed to examine amygdala response to mother versus stranger faces. In-scanner behavior was measured. Indiscriminate friendliness was assessed with parental report.Results Comparison youth showed an amygdala response that clearly discriminated mother versus stranger stimuli. Previously institutionalized youths, by contrast, exhibited reduced amygdala discrimination between mothers and strangers. Reduced amygdala differentiation correlated with greater reports of indiscriminate friendliness. These effects correlated with age-at-adoption, with later adoptions being associated with reduced amygdala discrimination and more indiscriminate friendliness.Conclusions Our results suggest that early maternal deprivation is associated with reduced amygdala discrimination between mothers and strangers, and reduced amygdala discrimination was associated with greater reports of indiscriminate friendliness. Moreover, these effects increased with age-at-adoption. These data suggest that the amygdala, in part, is associated with indiscriminate friendliness and that there might be a dose-response relationship between institutional rearing and indiscriminate friendliness.
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Children adopted from institutions showed reduced amygdala discrimination between mothers and strangers compared with children with no history of institutional rearing or adoption.
“Olsavsky et al (2013) used fMRI to demonstrate that children adopted from institutions showed reduced amygdala discrimination between mothers and strangers compared with children with no history of institutional rearing or adoption.”
From Deviations from the expectable environment in early childhood and emerging psychopathology (2015) · cites this paper as Olsavsky et al, 2013
Reductions in mother-stranger discriminations were moderately associated with indiscriminate behavior.
“Reductions in mother-stranger discriminations were moderately associated with indiscriminate behavior.”
From Deviations from the expectable environment in early childhood and emerging psychopathology (2015) · cites this paper as Olsavsky et al, 2013
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Diagnostic and Statistical Manual of Mental Disorders
Williams, J. B. W., & First, M. B. (2013) · Oxford University Press eBooks · doi:10.1093/acrefore/9780199975839.013.104 · Cited by 109,841 · see citing works
AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages
Cox, R. W. (1996) · Computers and Biomedical Research · doi:10.1006/cbmr.1996.0014 · Cited by 10,913 · see citing works
Diagnostic and Statistical Manual of Mental Disorders (DSM-IV)
Hu, R. J. (2003) · Elsevier eBooks · doi:10.1016/b0-12-226870-9/01070-4 · Cited by 9,167 · see citing works
Ainsworth, M. D. S., & Bell, S. M. (1970) · Child Development · doi:10.2307/1127388 · Cited by 1,764 · see citing works
Achenbach, T. M., & EDELBROCK, C. S. (1981) · Monographs of the Society for Research in Child Development · doi:10.2307/1165983 · Cited by 1,705 · see citing works
Achenbach, T. M., & Ruffle, T. M. (2000) · Pediatrics in Review · doi:10.1542/pir.21-8-265 · Cited by 1,287 · see citing works
The neurobiology of attachment
Insel, T. R., & Young, L. J. (2001) · Nature Reviews Neuroscience · doi:10.1038/35053579 · Cited by 1,173 · see citing works
Hoyme, H. E., May, P. A., Kalberg, W. O., Kodituwakku, P. W., Gossage, J. P., Trujillo, P. M., Buckley, D. G., Miller, J. H., Aragón, A. S., Khaole, N., et al. (2005) · PEDIATRICS · doi:10.1542/peds.2004-0259 · Cited by 981 · see citing works
Developmental psychiatry comes of age
(1988) · American Journal of Psychiatry · doi:10.1176/ajp.145.1.1 · Cited by 978 · see citing works
The Human Amygdala: An Evolved System for Relevance Detection
Sander, D., Grafman, J., & Zalla, T. (2003) · Reviews in the Neurosciences · doi:10.1515/revneuro.2003.14.4.303 · Cited by 944 · cited 1× · see citing works
“(A) Whole-brain linear mixed effect analysis revealed a Group St amygdala region of interest (peak [ 27 3 19]; k 1⁄4 47).”
MethodThe primate amygdala represents the positive and negative value of visual stimuli during learning
Paton, J. J., Belova, M. A., Morrison, S. E., & Salzman, C. D. (2006) · Nature · doi:10.1038/nature04490 · Cited by 917 · see citing works
Tottenham, N., Hare, T. A., Quinn, B. T., McCarry, T. W., Nurse, M., Gilhooly, T., Millner, A., Galvan, A., Davidson, M. C., Eigsti, I., et al. (2010) · Developmental Science · doi:10.1111/j.1467-7687.2009.00852.x · Cited by 905 · see citing works
Self-citationWhat does the amygdala contribute to social cognition
Adolphs, R. (2010) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2010.05445.x · Cited by 836 · see citing works
The world report on violence against children
(2018) · Human Rights Documents online · doi:10.1163/2210-7975_hrd-0302-2016002 · Cited by 805 · see citing works
Peer relationships and preadolescents' perceptions of security in the child-mother relationship.
Kerns, K. A., Klepac, L., & Cole, A. (1996) · Developmental Psychology · doi:10.1037/0012-1649.32.3.457 · Cited by 630 · see citing works
Variations in maternal care in infancy regulate the development of stress reactivity
Caldji, C., Diorio, J. C., & Meaney, M. J. (2000) · Biological Psychiatry · doi:10.1016/s0006-3223(00)01084-2 · Cited by 574 · see citing works
Chisholm, K. (1998) · Child Development · doi:10.1111/j.1467-8624.1998.tb06162.x · Cited by 571 · see citing works
Phan, K. L., Fitzgerald, D. A., Nathan, P. J., & Tancer, M. E. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.08.012 · Cited by 539 · see citing works
Plotsky, P. M., Thrivikraman, K. V., Nemeroff, C. B., Caldji, C., Sharma, S., & Meaney, M. J. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300769 · Cited by 522 · see citing works
Swain, J. E., Lorberbaum, J. P., Kose, S., & Strathearn, L. (2007) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2007.01731.x · Cited by 499 · see citing works
Mothers' neural activation in response to pictures of their children and other children
Leibenluft, E., Gobbini, M. I., Harrison, T., & Haxby, J. V. (2004) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.05.017 · Cited by 493 · see citing works
Mehta, M. A., Golembo, N. I., Nosarti, C., Colvert, E., Mota, A., Williams, S. C. R., Rutter, M., & Sonuga‐Barke, E. J. S. (2009) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2009.02084.x · Cited by 488 · see citing works
O'CONNOR, T. G., & RUTTER, M. (2000) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/00004583-200006000-00008 · Cited by 482 · see citing works
Elevated amygdala response to faces following early deprivation
Tottenham, N., Hare, T. A., Millner, A., Gilhooly, T., Zevin, J. D., & Casey, B. J. (2011) · Developmental Science · doi:10.1111/j.1467-7687.2010.00971.x · Cited by 468 · see citing works
Self-citationRutter, M. L., English and Romanian Adoptees (ERA) Study Team, & O'Connor, T. G. (2003) · Developmental Psychology · doi:10.1037/0012-1649.40.1.81 · Cited by 407 · see citing works
THE EFFECT OF EARLY INSTITUTIONAL REARING ON THE DEVELOPMENT OF EIGHT YEAR OLD CHILDREN
Tizard, B., & Hodges, J. (1978) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.1978.tb00453.x · Cited by 390 · see citing works
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 · see citing works
Positive and negative emotional verbal stimuli elicit activity in the left amygdala
Hamann, S., & Mao, H. (2002) · Neuroreport · doi:10.1097/00001756-200201210-00008 · Cited by 385 · see citing works
Attachment disturbances in young children: I: the continuum of caretaking casualty
SMYKE, A. T., DUMITRESCU, A., & ZEANAH, C. H. (2002) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/00004583-200208000-00016 · Cited by 362 · see citing works
Rutter, M., Colvert, E., Kreppner, J., Beckett, C., Castle, J., Groothues, C., Hawkins, A., O'Connor, T. G., Stevens, S. E., & Sonuga‐Barke, E. J. S. (2007) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2006.01688.x · Cited by 358 · see citing works
I. CHILDREN IN INSTITUTIONAL CARE: DELAYED DEVELOPMENT AND RESILIENCE
van IJzendoorn, M. H., Palacios, J., Sonuga-Barke, E. J. S., Gunnar, M. R., Vorria, P., McCall, R. B., Mare, L. L., Bakermans‐Kranenburg, M. J., Dobrova‐Krol, N. A., & Juffer, F. (2011) · Monographs of the Society for Research in Child Development · doi:10.1111/j.1540-5834.2011.00626.x · Cited by 347 · see citing works
Social and Family Relationships of Ex‐Institutional Adolescents
Hodges, J., & Tizard, B. (1989) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.1989.tb00770.x · Cited by 343 · see citing works
Affect-biased attention as emotion regulation
Todd, R. M., Cunningham, W. A., Anderson, A. K., & Thompson, E. (2012) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2012.06.003 · Cited by 336 · see citing works
Child–parent attachment following early institutional deprivation
O'CONNOR, T. G., MARVIN, R. S., RUTTER, M., OLRICK, J. T., BRITNER, P. A., & THE ENGLISH AND ROMANIAN ADOPTEES STUDY TEAM (2003) · Development and Psychopathology · doi:10.1017/s0954579403000026 · Cited by 314 · see citing works
Parent-child attachment and monitoring in middle childhood.
Kerns, K. A., Aspelmeier, J. E., Gentzler, A. L., & Grabill, C. M. (2001) · Journal of Family Psychology · doi:10.1037//0893-3200.15.1.69 · Cited by 305 · see citing works
International adoption of institutionally reared children: research and policy
GUNNAR, M. R., BRUCE, J., & GROTEVANT, H. D. (2000) · Development and Psychopathology · doi:10.1017/s0954579400004077 · Cited by 261 · see citing works
THE EFFECTS OF MOTHER‐CHILD SEPARATION: A FOLLOW‐UP STUDY
Bowlby, J., Ainsworth, M. D. S., Boston, M., & Rosenbluth, D. (1956) · British Journal of Medical Psychology · doi:10.1111/j.2044-8341.1956.tb00915.x · Cited by 242 · see citing works
Parent–child attachment and monitoring in middle childhood.
Kerns, K. A., Aspelmeier, J. E., Gentzler, A. L., et al. (2001) · Journal of Family Psychology · doi:10.1037/0893-3200.15.1.69 · Cited by 224 · see citing works
Attachment Disturbances in Young Children. II: Indiscriminate Behavior and Institutional Care
ZEANAH, C. H., SMYKE, A. T., & DUMITRESCU, A. (2002) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/00004583-200208000-00017 · Cited by 219 · see citing works
Gleason, M. M., Fox, N. A., Drury, S., Smyke, A., Egger, H. L., Nelson, C. A., Gregas, M. C., & Zeanah, C. H. (2011) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2010.12.012 · Cited by 206 · see citing works
Rutter (2010) · doi:10.1111/j.1540-5834.2010.00548.x · Cited by 194 · see citing works
Independence in ROI analysis: where is the voodoo?
Poldrack, R. A., & Mumford, J. A. (2009) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsp011 · Cited by 192 · see citing works
Colvert, E., Rutter, M., Beckett, C., Castle, J., Groothues, C., Hawkins, A., Kreppner, J., O'connor, T. G., Stevens, S., & Sonuga-Barke, E. J. S. (2008) · Development and Psychopathology · doi:10.1017/s0954579408000278 · Cited by 182 · see citing works
Neurobiology of infant attachment
Moriceau, S., & Sullivan, R. M. (2005) · Developmental Psychobiology · doi:10.1002/dev.20093 · Cited by 180 · see citing works
III. ATTACHMENT AND EMOTIONAL DEVELOPMENT IN INSTITUTIONAL CARE: CHARACTERISTICS AND CATCH UP
Bakermans‐Kranenburg, M. J., Steele, H., Zeanah, C. H., Muhamedrahimov, R. J., Vorria, P., Dobrova‐Krol, N. A., Steele, M., van IJzendoorn, M. H., Juffer, F., & Gunnar, M. R. (2011) · Monographs of the Society for Research in Child Development · doi:10.1111/j.1540-5834.2011.00628.x · Cited by 175 · see citing works
Ono, M., Kikusui, T., Sasaki, N., Ichikawa, M., Mori, Y., & Murakami-Murofushi, K. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.07.078 · Cited by 149 · see citing works
The Development of Social Behavior Following Neonatal Amygdala Lesions in Rhesus Monkeys
Bauman, M., Lavenex, P., Mason, W., Capitanio, J., & Amaral, D. (2004) · Journal of Cognitive Neuroscience · doi:10.1162/0898929042304741 · Cited by 148 · see citing works
Unique neural circuitry for neonatal olfactory learning
Moriceau, S., & Sullivan, R. M. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.4578-03.2004 · Cited by 141 · see citing works
Roy, P., Rutter, M. L., & Pickles, A. R. (2004) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2004.00278.x · Cited by 141 · see citing works
Hoyme, H. E. (2005) · PEDIATRICS · doi:10.1542/peds.2005-0702 · Cited by 135 · see citing works
Amygdala Gene Expression Correlates of Social Behavior in Monkeys Experiencing Maternal Separation
Sabatini, M. J., Ebert, P., Lewis, D. A., Levitt, P., Cameron, J. L., & Mirnics, K. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.4765-06.2007 · Cited by 125 · see citing works
The Development of Mother-Infant Interactions after Neonatal Amygdala Lesions in Rhesus Monkeys
Bauman, M., Lavenex, P., Mason, W., Capitanio, J., & Amaral, D. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.3263-03.2004 · Cited by 122 · see citing works
Implications of Attachment Theory and Research for Developmental-Behavioral Pediatrics
Carlson, E. A., Sampson, M. C., & Sroufe, L. A. (2003) · Journal of Developmental & Behavioral Pediatrics · doi:10.1097/00004703-200310000-00010 · Cited by 118 · see citing works
A New Model of Foster Care for Young Children: The Bucharest Early Intervention Project
Smyke, A. T., Zeanah, C. H., Fox, N. A., & Nelson, C. A. (2009) · Child and Adolescent Psychiatric Clinics of North America · doi:10.1016/j.chc.2009.03.003 · Cited by 112 · see citing works
BECKETT, C., BREDENKAMP, D., CASTLE, J., GROOTHUES, C., O’CONNOR, T. G., & RUTTER, M. (2002) · Journal of Developmental & Behavioral Pediatrics · doi:10.1097/00004703-200210000-00001 · Cited by 111 · see citing works
Astley, S. J. (2006) · PEDIATRICS · doi:10.1542/peds.2006-0577 · Cited by 109 · see citing works
Ousdal, O. T., Jensen, J., Server, A., Hariri, A. R., Nakstad, P. H., & Andreassen, O. A. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.07.066 · Cited by 102 · see citing works
The changing face of emotion: age-related patterns of amygdala activation to salient faces
Todd, R. M., Evans, J. W., Morris, D. M., Lewis, M. D., & Taylor, M. J. (2010) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsq007 · Cited by 97 · see citing works
Tottenham, N., Shapiro, M., Telzer, E. H., & Humphreys, K. L. (2012) · Developmental Science · doi:10.1111/j.1467-7687.2011.01128.x · Cited by 91 · see citing works
Self-citationTranslating Research Findings on Early Experience to Prevention
O’Connor, T. G., & Cameron, J. L. (2006) · American Journal of Preventive Medicine · doi:10.1016/j.amepre.2006.07.005 · Cited by 43 · see citing works
Electrophysiological insights into the enduring effects of early life stress on the brain
Ali, I. Y., Salzberg, M. R., French, C. R., & Jones, N. C. (2010) · Psychopharmacology · doi:10.1007/s00213-010-2125-z · Cited by 25 · see citing works
The effect of separation from the mother in early life
Bowlby, J. (1954) · Irish Journal of Medical Science (1971 -) · doi:10.1007/bf02952876 · Cited by 22 · see citing works
An abbreviated form of the Wechsler Intelligence Scale for Children.
Clements, G. R. (1965) · Journal of Consulting Psychology · doi:10.1037/h0020970 · Cited by 20 · see citing works
Attachment disturbances and disorders in children exposed to early severe deprivation
O'Connor, T. G., Bredenkamp, D., Rutter, M., & The English and Romanian Adoptees (ERA) Study Team (1999) · Infant Mental Health Journal · doi:10.1002/(sici)1097-0355(199921)20:1
Flagged first, then by citations
Research works printed but not linked: 3
- [48]Tizard B Hodges J 1978 The effect of early institutional rearing on the development of eight year old children J Child Psychol Psychiatry 19 99 118 670339
- [49]Hodges J Tizard B 1989 Social and Family Relationships of Ex-Institutional Adolescents J Child Psychol Psyc 30 77 97 2925822
- [54]Talairach J Tournoux P 1988 Co-planar stereotaxic atlas of the human brain: an approach to medical cerebral imaging Stuttgart New York New York G. Thieme; Thieme Medical Publishers
Cited by
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Childhood Adversity and Neural Development: A Systematic Review
McLaughlin, K. A., Weissman, D., & Bitrán, D. (2019) · Annual Review of Developmental Psychology · doi:10.1146/annurev-devpsych-121318-084950 · Cited by 892 · see citing works
Early Adverse Experiences and the Developing Brain
Bick, J., & Nelson, C. A. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2015.252 · Cited by 559 · see citing works
Social re-orientation and brain development: An expanded and updated view
Nelson, E. E., Jarcho, J. M., & Guyer, A. E. (2016) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2015.12.008 · Cited by 447 · see citing works
Zeanah, C. H., & Gleason, M. M. (2015) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.12347 · Cited by 265 · see citing works
Hidden talents in harsh environments
Ellis, B. J., Abrams, L. S., Masten, A. S., Sternberg, R. J., Tottenham, N., & Frankenhuis, W. E. (2020) · Development and Psychopathology · doi:10.1017/s0954579420000887 · Cited by 267 · see citing works
Self-citationDeviations from the expectable environment in early childhood and emerging psychopathology
Humphreys, K. L., & Zeanah, C. H. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2014.165 · Cited by 231 · see citing works
Self-citationLomanowska, A. M., Boivin, M., Hertzman, C., & Fleming, A. S. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2015.09.029 · Cited by 224 · see citing works
Bick, J., Zhu, T., Stamoulis, C., Fox, N. A., Zeanah, C., & Nelson, C. A. (2015) · JAMA Pediatrics · doi:10.1001/jamapediatrics.2014.3212 · Cited by 199 · see citing works
Early life adversity shapes neural circuit function during sensitive postnatal developmental periods
Malave, L., van Dijk, M. T., & Anacker, C. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-02092-9 · Cited by 177 · see citing works
Effects of early life stress on amygdala and striatal development
Fareri, D. S., & Tottenham, N. (2016) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2016.04.005 · Cited by 166 · see citing works
Self-citationMarques, A. H., Bjørke-Monsen, A.-L., Teixeira, A. L., & Silverman, M. N. (2015) · Brain Research · doi:10.1016/j.brainres.2014.10.051 · Cited by 166 · see citing works
The complex neurobiology of resilient functioning after childhood maltreatment
Ioannidis, K., Askelund, A. D., Kievit, R., & van Harmelen, A. (2020) · BMC Medicine · doi:10.1186/s12916-020-1490-7 · Cited by 163 · see citing works
Oxytocin׳s role in anxiety: A critical appraisal
MacDonald, K., & Feifel, D. (2014) · Brain Research · doi:10.1016/j.brainres.2014.01.025 · Cited by 139 · see citing works
Zeanah, C. H., Chesher, T. L., Boris, N. W., Walter, H. J., Bukstein, O. G., Bellonci, C., Benson, R. S., Bussing, R., Chrisman, A. K., Hamilton, J. D., et al. (2016) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2016.08.004 · Cited by 132 · see citing works
The Importance of Early Experiences for Neuro-Affective Development
Tottenham, N. (2013) · Current topics in behavioral neurosciences · doi:10.1007/7854_2013_254 · Cited by 133 · see citing works
Self-citationThe Importance of Early Experiences for Neuro-Affective Development
Tottenham, N. (2013) · Current topics in behavioral neurosciences · doi:10.1007/978-3-662-45758-0_254 · Cited by 128 · see citing works
Self-citationEliasova, I., Anderkova, L., Marecek, R., & Rektorova, I. (2014) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2014.08.036 · Cited by 115 · see citing works
Early experience and brain development
Bick, J. R., & Nelson, C. A. (2016) · Wiley Interdisciplinary Reviews Cognitive Science · doi:10.1002/wcs.1387 · Cited by 109 · see citing works
Thijssen, S., Muetzel, R. L., Bakermans‐Kranenburg, M. J., Jaddoe, V. W. V., Tiemeier, H. W., Verhulst, F. C., White, T. J. H., & van IJzendoorn, M. H. (2017) · Development and Psychopathology · doi:10.1017/s0954579417000141 · Cited by 97 · see citing works
Hostinar, C. E., Johnson, A. E., & Gunnar, M. R. (2015) · Developmental Psychology · doi:10.1037/dev0000029 · Cited by 91 · see citing works
Callaghan, B., Gee, D., Gabard-Durnam, L. J., Telzer, E., Humphreys, K., Goff, B., Shapiro, M., Flannery, J. E., Lumian, D. S., Fareri, D. S., et al. (2019) · Biological Psychiatry: Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2019.02.001 · Cited by 75 · see citing works
Self-citationFareri, D. S., Gabard-Durnam, L. J., Goff, B., Flannery, J., Gee, D. G., Lumian, D. S., Caldera, C., & Tottenham, N. (2017) · Development and Psychopathology · doi:10.1017/s0954579417001456 · Cited by 83 · see citing works
Self-citationHumphreys, K. L., Nelson, C. A., Fox, N. A., & Zeanah, C. H. (2017) · Development and Psychopathology · doi:10.1017/s0954579417000256 · Cited by 74 · see citing works
Self-citationAdverse Life Experiences and Brain Function
Hosseini‐Kamkar, N., Farahani, M. V., Nikolic, M., Stewart, K., Goldsmith, S. F., Soltaninejad, M., Rajabli, R., Lowe, C. J., Nicholson, A. A., Morton, J. B., et al. (2023) · JAMA Network Open · doi:10.1001/jamanetworkopen.2023.40018 · Cited by 72 · see citing works
Recent developments in the study of social relationships, stress responses, and physical health
Hostinar, C. E. (2015) · Current Opinion in Psychology · doi:10.1016/j.copsyc.2015.05.004 · Cited by 69 · see citing works
Vaidya, N., Marquand, A. F., Nees, F., Siehl, S., & Schumann, G. (2024) · Molecular Psychiatry · doi:10.1038/s41380-024-02556-y · Cited by 68 · see citing works
The evolving neurobiology of early-life stress
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The Neurobiology of Attachment: From Infancy to Clinical Outcomes
Chambers, J. E. (2017) · Psychodynamic Psychiatry · doi:10.1521/pdps.2017.45.4.542 · Cited by 60 · see citing works
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McCormick, E. M., Qu, Y., & Telzer, E. H. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2015.09.063 · Cited by 54 · see citing works
Self-citationKay, C., & Green, J. (2015) · Development and Psychopathology · doi:10.1017/s0954579415000292 · Cited by 47 · see citing works
The pubertal stress recalibration hypothesis: Potential neural and behavioral consequences
DePasquale, C. E., Herzberg, M. P., & Gunnar, M. R. (2021) · Child Development Perspectives · doi:10.1111/cdep.12429 · Cited by 44 · see citing works
Rogers, C. R., Chen, X., Kwon, S., McElwain, N. L., & Telzer, E. H. (2021) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2021.101046 · Cited by 46 · see citing works
Self-citationSaxbe, D., Piero, L. B. D., Immordino‐Yang, M. H., Kaplan, J., & Margolin, G. (2015) · Social Neuroscience · doi:10.1080/17470919.2015.1022216 · Cited by 39 · see citing works
Tottenham, N. (2020) · Development and Psychopathology · doi:10.1017/s0954579420001169 · Cited by 38 · see citing works
Self-citationKay, C., Green, J., & Sharma, K. (2016) · Research on Child and Adolescent Psychopathology · doi:10.1007/s10802-016-0131-2 · Cited by 37 · see citing works
Long term effects of early life stress on HPA circuit in rodent models
Babicola, L., Ventura, R., D’Addario, S. L., Ielpo, D., Andolina, D., & Segni, M. D. (2020) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2020.111125 · Cited by 27 · see citing works
Ellis, B. J., Abrams, L. S., Masten, A. S., Sternberg, R. J., Tottenham, N., & Frankenhuis, W. E. (2023) · Cambridge University Press eBooks · doi:10.1017/9781009350051 · Cited by 28 · see citing works
Self-citationThe other side of the coin: Hypersociability
Tóth, M. (2018) · Genes Brain & Behavior · doi:10.1111/gbb.12512 · Cited by 24 · see citing works
Forbes, E. E., Eckstrand, K., Rofey, D. L., & Silk, J. S. (2020) · Biological Psychiatry Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2020.07.020 · Cited by 22 · see citing works
Lyons‐Ruth, K., Riley, C., Patrick, M. P. H., & Hobson, R. P. (2019) · Personality Disorders Theory Research and Treatment · doi:10.1037/per0000312 · Cited by 23 · see citing works
Green, S. A., Goff, B., Gee, D. G., Gabard-Durnam, L. J., Flannery, J., Telzer, E. H., Humphreys, K. L., Louie, J., & Tottenham, N. (2016) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.12578 · Cited by 23 · see citing works
Self-citationAmygdala growth from youth to adulthood in the macaque monkey
Schumann, C. M., Scott, J. A., Lee, A., Bauman, M. D., & Amaral, D. G. (2019) · The Journal of Comparative Neurology · doi:10.1002/cne.24728 · Cited by 18 · see citing works
Neural mediators of the intergenerational transmission of family aggression
Saxbe, D., Piero, L. B. D., Immordino‐Yang, M. H., Kaplan, J., & Margolin, G. (2015) · Development and Psychopathology · doi:10.1017/s0954579415000528 · Cited by 18 · see citing works
Halladay, L. R., & Herron, S. M. (2022) · Neuropharmacology · doi:10.1016/j.neuropharm.2022.109404 · Cited by 17 · see citing works
The biological bases of attachment
Oliveira, P., & Fearon, P. R. M. (2019) · Adoption & Fostering · doi:10.1177/0308575919867770 · Cited by 17 · see citing works
Meyer, H. C., Fields, A., Vannucci, A., Gerhard, D. M., Bloom, P. A., Heleniak, C. M., Opendak, M. M., Sullivan, R. M., Tottenham, N., Callaghan, B. L., et al. (2022) · Biological Psychiatry Global Open Science · doi:10.1016/j.bpsgos.2022.02.002 · Cited by 15 · see citing works
Self-citationFACTORS ASSOCIATED WITH INDISCRIMINATE FRIENDLINESS IN HIGH-RISK CHILDREN
Love, L., Minnis, H., & O’Connor, S. (2015) · Infant Mental Health Journal · doi:10.1002/imhj.21520 · Cited by 14 · see citing works
A Neuroscience Perspective on Emotional Development
Morales, S., & Fox, N. A. (2019) · Springer eBooks · doi:10.1007/978-3-030-17332-6_4 · Cited by 13 · see citing works
Programming social behavior by the maternal fragile X protein
Zupan, B., Sharma, A., Frazier, A., Klein, S. L., & Tóth, M. (2016) · Genes Brain & Behavior · doi:10.1111/gbb.12298 · Cited by 13 · see citing works
Unraveling the Longstanding Scars of Early Neurodevelopmental Stress
Cryan, J. F., & Dinan, T. G. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.10.004 · Cited by 13 · see citing works
Petranovich, C. L., Walz, N. C., Staat, M. A., Chiu, C.-Y. P., & Wade, S. L. (2016) · Applied Neuropsychology Child · doi:10.1080/21622965.2016.1182433 · Cited by 11 · see citing works
Mesquita, A. R., Belsky, J., Crego, A., Fachada, I., Oliveira, P., Sampaio, A., & Soares, I. (2015) · Child Development · doi:10.1111/cdev.12371 · Cited by 9 · see citing works
Perry, N. B., Johnson, A. E., Hostinar, C. E., & Gunnar, M. R. (2020) · Developmental Psychobiology · doi:10.1002/dev.22067 · Cited by 10 · see citing works
Lewis, L. R., Lopez, R. A., Hunt, R. H., Hodel, A. S., Gunnar, M. R., & Thomas, K. M. (2024) · Brain and Cognition · doi:10.1016/j.bandc.2024.106183 · Cited by 9 · see citing works
Bick, J. R., Lipschutz, R. S., Tabachnick, A. R., Biekman, B. D., Katz, D., Simons, R. F., & Dozier, M. (2022) · Developmental Psychobiology · doi:10.1002/dev.22249 · Cited by 7 · see citing works
Perego, G., Caputi, M., & Ogliari, A. L. (2015) · Child & Youth Care Forum · doi:10.1007/s10566-015-9340-z · Cited by 7 · see citing works
Weissmark, M. S. (2020) · doi:10.1093/oso/9780190686345.001.0001 · Cited by 4 · see citing works
Neural Representation of Parental Monitoring and Links to Adolescent Risk Taking
Lee, T., Qu, Y., & Telzer, E. H. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.01286 · Cited by 4 · see citing works
Self-citationNeural Responses to Caregivers After Early Life Threat Experiences
Murgueitio, N., Shipkova, M., Lurie, L. A., Rodriguez, M., Machlin, L., Tate, M., Boda, S., Priddy, Z., Propper, C. B., McLaughlin, K., et al. (2025) · Developmental Science · doi:10.1111/desc.70104 · Cited by 3 · see citing works
Winnette, P., & Abramson, L. (2025) · Attachment & Human Development · doi:10.1080/14616734.2024.2444722 · Cited by 3 · see citing works
One piece of the puzzle: Treatment of fostered and adopted children with RAD and DSED
Zilberstein, K. (2023) · Adoption & Fostering · doi:10.1177/03085759221150018 · Cited by 3 · see citing works
Zilberstein, K. (2016) · Springer eBooks · doi:10.1007/978-3-319-32132-5_112-2 · Cited by 3 · see citing works
Oliveira, P. (2024) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2024.1332898 · Cited by 2 · see citing works
Rosenberg, B. M., Moreira, J. F. G., Leal, A. S. M., Saragosa-Harris, N. M., Gaines, E., Meredith, W., McCann, C. F., Coury, S. M., Waizman, Y. H., Ninova, E., et al. (2025) · Biological Psychiatry · doi:10.1016/j.biopsych.2026.03.035 · Cited by 2 · see citing works
Tajabadi, A., Abbasnejad, M., Kooshki, R., Esmaeili‐Mahani, S., Raoof, M., & Lobbezoo, F. (2023) · Archives of Oral Biology · doi:10.1016/j.archoralbio.2023.105699 · Cited by 2 · see citing works
Cohen‐Gilbert, J. E., Stein, E., Gunnar, M. R., & Thomas, K. M. (2016) · The Journal of Early Adolescence · doi:10.1177/0272431616675975 · Cited by 2 · see citing works
Scott, E. P. (2017) · The Scholarship East Carolina University's Institutional Repository (East Carolina University) · Cited by 2 · see citing works
King, D. P., Khan, M., Majewska, A. K., Cameron, J. L., & Fudge, J. L. (2026) · Journal of Neuroscience · doi:10.1523/jneurosci.0017-26.2026 · Cited by 1 · see citing works
Selective neural sensitivity to familial threat in adolescents with weak family bonds
Sharp, P. B., Heller, W., & Telzer, E. H. (2017) · Social Neuroscience · doi:10.1080/17470919.2017.1397545 · Cited by 1 · see citing works
Self-citationDiversity and Ethnic Conflicts
Weissmark, M. S. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190686345.003.0008 · Cited by 1 · see citing works
Rodríguez, D. A. L., & Cárdenas, F. P. (2021) · Psykhe (Santiago) · doi:10.7764/psykhe.2019.21739 · Cited by 1 · see citing works
EARLY SOCIAL LEARNING AND CONSTANCY IN CLOSE RELATIONSHIP
Winnette, P. (2023) · Social Pathology and Prevention · doi:10.25142/spp.2023.004 · Cited by 1 · see citing works
The impact of reactive attachment disorder on adoptive family functioning
Vasquez, M. L. (2014) · doi:10.17077/etd.xdhcqe8m · Cited by 1 · see citing works
Zilberstein, K. (2018) · Springer eBooks · doi:10.1007/978-3-319-33228-4_112 · Cited by 1 · see citing works
Oliveira, P., Fearon, P. R. M., Belsky, J., Mesquita, A. R., Sampaio, A., Pinal, D., & Soares, I. (2022) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.13728 · Cited by 6 · see citing works
The Affect-Hungry Child: Friendliness and Amygdala Are Indiscriminate
Geller, B. (2013) · Journal watch · doi:10.1056/nejm-jw.na31603
Weissmark, M. S. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190686345.003.0007
Weissmark, M. S. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190686345.003.0006
Weissmark, M. S. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190686345.003.0001
Weissmark, M. S. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190686345.003.0005 · Cited by 1 · see citing works
Weissmark, M. S. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190686345.003.0009
Reactive Attachment Disorder and Disinhibited Social Engagement Disorder
Scott, E. L., Keary, C. J., King, J. M., Zeanah, C. H., & McDougle, C. J. (2018) · Oxford University Press eBooks · doi:10.1093/med/9780190457136.003.0002
Weissmark, M. S. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190686345.003.0002
Weissmark, M. S. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190686345.003.0004
Weissmark, M. S. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190686345.003.0003
Weissmark, M. S. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190686345.003.0010
Autocratic parenting of a humanoid robot: A QEEG-based case study
Ghalebin, S. S. A., Atadokht, A., & Mousavi, S. M. (2024) · Applied Psychology Research · doi:10.59400/apr.v3i1.504
Weissmark, M. S. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190686345.002.0007
Weissmark, M. S. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190686345.002.0004
Weissmark, M. S. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190686345.002.0015
Weissmark, M. S. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190686345.002.0008
Weissmark, M. S. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190686345.002.0003
Weissmark, M. S. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190686345.002.0005
Harris, J. C., & Coyle, J. T. (2024) · doi:10.1093/med/9780199928118.003.0012
King, D. P., Khan, M., Majewska, A. K., Cameron, J. L., & Fudge, J. L. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.01.06.697965
Childhood Attachment Patterns and Disorders
Fierro-Cobas, V. (2026) · Pediatrics in Review · doi:10.1542/pir.2025-006869
- Authors
- Olsavsky, A. K., Telzer, E. H., Shapiro, M., Humphreys, K. L., Flannery, J., Goff, B., & Tottenham, N.
- Affiliations
- University of California, Los Angeles (US)
- Corresponding author
- Olsavsky, Aviva K.
- ORCID
- Venue
- Biological Psychiatry
- Publisher
- Elsevier BV
- Published
- 2013-12
- Volume
- 74
- Issue
- 11
- Pages
- 853-860
- ISSN
- 0006-3223 (ISSN-L)
- PMC
- PMC3818506
- OpenAlex
- W2121807029
- Cited by
- 99
- References
- 63
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 5 · 2023: 6 · 2022: 6 · 2021: 3 · 2020: 24 · 2019: 7 · 2018: 3 · 2017: 6 · 2016: 9 · 2015: 13 · 2014: 6 · 2013: 4
- FWCI
- 15.96
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Biological Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (R01MH091864)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Face Recognition and Perception
- Social Sciences › Safety Research › Child Welfare and Adoption
- Keywords
- maternal deprivation, amygdala, face discrimination, institutionalized children, age at adoption, attachment, amygdala development, early rearing environment
- MeSH terms
- Adolescent, Affect, Amygdala, Brain Mapping, Child, Child, Preschool, Female, Humans, Interpersonal Relations, Magnetic Resonance Imaging, Male, Maternal Deprivation, Mothers
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