The international society for developmental psychobiology Sackler symposium: early adversity and the maturation of emotion circuits-a cross-species analysis
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Early-life caregiving shapes the architecture and function of the developing brain. The fact that the infant-caregiver relationship is critically important for infant functioning across all altricial species, and that the anatomical circuits supporting emotional functioning are highly preserved across different species, suggests that the results of studies examining the role of early adversity and emotional functioning should be translatable across species. Here we present findings from four different research laboratories, using three different species, which have converged on a similar finding: adversity accelerates the developmental trajectory of amygdala-prefrontal cortex (PFC) development and modifies emotional behaviors. First, a rodent model of attachment learning associated with adversity is presented showing precocial disruption of attachment learning and emergence of heightened fear learning and emotionality. Second, a model of infant-mother separation is presented in which early adversity is shown to accelerate the developmental emergence of adult-like fear retention and extinction. Third, a model of early life adversity in Rhesus monkeys is presented in which a naturally occurring variation in maternal-care (abuse) is shown to alter the functioning of emotion circuits. Finally, a human model of maternal deprivation is presented in which children born into orphanages and then adopted abroad exhibit aberrant development of emotion circuits. The convergence of these cross-species studies on early life adversity suggests that adversity targets the amygdala and PFC and has immediate impact on infant behavior with the caregiver, and emotional reactions to the world. These results provide insight into mechanisms responsible for caregiver induced mental health trajectory alterations.
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Trauma experienced from an attachment figure during a sensitive window in early life can produce life-long deficits in threat processing and social behavior across many species.
“In particular, trauma experienced from a caregiver during a sensitive window in early life can produce life-long deficits in threat processing and social behavior across many species (Amaral, 2003, Callaghan et al., 2014, McEwen, 2003, Moriceau et al., 2006, Tang et al., 2014, Tzanoulinou and Sandi, 2017, Zeanah et al., 2003).”
From Early life adversity during the infant sensitive period for attachment: Programming of behavioral neurobiology of threat processing and social behavior (2017) · cites this paper as Callaghan et al., 2014
Many effects of early life trauma on children's mental health appear delayed until transition into adolescence.
“In parallel with observations of latent abuse-related deficits in rodents and non-human primates, many of the effects of early life trauma on children’s mental health appear to be delayed until they begin to transition into adolescence (Bachevalier and Loveland, 2006, Bachevalier et al., 2001, Callaghan et al., 2014, Goursaud and Bachevalier, 2007, Goursaud et al., 2014, Machado and Bachevalier, 2”
From Early life adversity during the infant sensitive period for attachment: Programming of behavioral neurobiology of threat processing and social behavior (2017) · cites this paper as Callaghan et al., 2014
Early life adversity may accelerate brain development.
“Interestingly, early life adversity may accelerate brain development (Callaghan et al., 2014; Hostinar and Gunnar, 2013)”
From Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex? (2017) · cites this paper as Callaghan et al., 2014
Accelerated brain development following early life stress may be an adaptive mechanism that coordinates the development of neural circuits to meet the demands of an adverse environment.
“This accelerated brain development following early life stress may be an adaptive mechanism that coordinates the development of neural circuits to meet the demands of an adverse environment (Callaghan et al., 2014; Hostinar and Gunnar, 2013).”
From Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex? (2017) · cites this paper as Callaghan et al., 2014
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Cites
Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene
Caspi, A., Sugden, K., Moffitt, T. E., Taylor, A., Craig, I. W., Harrington, H., McClay, J., Mill, J., Martin, J., Braithwaite, A., et al. (2003) · Science · doi:10.1126/science.1083968 · Cited by 8,120 · see citing works
Epigenetic programming by maternal behavior
Weaver, I. C. G., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., Dymov, S., Szyf, M., & Meaney, M. J. (2004) · Nature Neuroscience · doi:10.1038/nn1276 · Cited by 6,177 · see citing works
Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse
McGowan, P. O., Sasaki, A., D'Alessio, A. C., Dymov, S., Labonté, B., Szyf, M., Turecki, G., & Meaney, M. J. (2009) · Nature Neuroscience · doi:10.1038/nn.2270 · Cited by 3,531 · see citing works
Neural regulation of endocrine and autonomic stress responses
Ulrich-Lai, Y. M., & Herman, J. P. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2647 · Cited by 3,318 · see citing works
Attachment and loss: Retrospect and prospect.
Bowlby, J. (1982) · American Journal of Orthopsychiatry · doi:10.1111/j.1939-0025.1982.tb01456.x · Cited by 2,930 · see citing works
Ongur, D. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.3.206 · Cited by 2,627 · see citing works
Neurocircuitry of stress: central control of the hypothalamo–pituitary–adrenocortical axis
Herman, J. P., & Cullinan, W. E. (1997) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)10069-2 · Cited by 2,270 · see citing works
Neurons in medial prefrontal cortex signal memory for fear extinction
Milad, M. R., & Quirk, G. J. (2002) · Nature · doi:10.1038/nature01138 · Cited by 1,836 · cited 1× · see citing works
“While extinction in adult rats is dependent upon the infralimbic (IL) region of the PFC (Milad & Quirk, 2002), infant extinction is IL independent (Kim, Hamlin, & Richardson, 2009).”
Endocrinology of the stress response
Charmandari, E., Tsigos, C., & Chrousos, G. (2005) · Annual Review of Physiology · doi:10.1146/annurev.physiol.67.040403.120816 · Cited by 1,799 · see citing works
Context, ambiguity, and unlearning: sources of relapse after behavioral extinction
Bouton, M. E. (2002) · Biological Psychiatry · doi:10.1016/s0006-3223(02)01546-9 · Cited by 1,662 · see citing works
Plotsky, P. M., & Meaney, M. J. (1993) · Molecular Brain Research · doi:10.1016/0169-328x(93)90189-v · Cited by 1,638 · see citing works
Object relations, dependency, and attachment: a theoretical review of the infant-mother relationship
Ainsworth, M. D. S. (1969) · Child Development · doi:10.2307/1127008 · Cited by 1,461 · cited 1× · see citing works
“Therefore, the infant, regardless of rodent, non-human primate, or human, has the same goal, which is to ensure proximity to the caregiver (Ainsworth, 1969; Bowlby, 1982; Moriceau & Roth, 2010).”
Evolutionary and biomedical insights from the rhesus macaque genome.
Gibbs, R. A., Rogers, J., Katze, M. G., Bumgarner, R., Weinstock, G. M., Mardis, E. R., Remington, K. A., Strausberg, R. L., Venter, J. C., Wilson, R. K., et al. (2007) · Science · doi:10.1126/science.1139247 · Cited by 1,403 · see citing works
Neurobiological Basis of Failure to Recall Extinction Memory in Posttraumatic Stress Disorder
Milad, M. R., Pitman, R. K., Ellis, C. B., Gold, A. L., Shin, L. M., Lasko, N. B., Zeidan, M. A., Handwerger, K., Orr, S. P., & Rauch, S. L. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.06.026 · Cited by 1,339 · see citing works
Sierra-Mercado, D., Padilla-Coreano, N., & Quirk, G. J. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.184 · Cited by 1,190 · see citing works
Schizophrenia as a Disorder of Neurodevelopment
Lewis, D. A., & Levitt, P. (2002) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.25.112701.142754 · Cited by 1,163 · see citing works
Classical fear-conditioning in the anxiety disorders: a meta-analysis
Lissek, S., Powers, A. S., McClure, E. B., Phelps, E. A., Woldehawariat, G., Grillon, C., & Pine, D. S. (2005) · Behaviour Research and Therapy · doi:10.1016/j.brat.2004.10.007 · Cited by 1,034 · see citing works
SÁNCHEZ, M. M., LADD, C. O., & PLOTSKY, P. M. (2001) · Development and Psychopathology · doi:10.1017/s0954579401003029 · Cited by 1,003 · see citing works
Quirk, G. J., Likhtik, E., Pelletier, J. G., & Paré, D. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-25-08800.2003 · Cited by 927 · 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
Early developmental emergence of human amygdala–prefrontal connectivity after maternal deprivation
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) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1307893110 · Cited by 871 · see citing works
Contextual control of the extinction of conditioned fear
Bouton, M. E., & Bolles, R. C. (1979) · Learning and Motivation · doi:10.1016/0023-9690(79)90057-2 · Cited by 796 · see citing works
Rutter, M. (1998) · Journal of Child Psychology and Psychiatry and Allied Disciplines · doi:10.1111/1469-7610.00343 · Cited by 796 · see citing works
Hostinar, C. E., Sullivan, R. M., & Gunnar, M. R. (2014) · Psychological Bulletin · doi:10.1037/a0032671 · Cited by 739 · see citing works
A Developmental Shift from Positive to Negative Connectivity in Human Amygdala–Prefrontal Circuitry
Gee, D. G., Humphreys, K. L., Flannery, J., Goff, B., Telzer, E. H., Shapiro, M., Hare, T. A., Bookheimer, S. Y., & Tottenham, N. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.3446-12.2013 · Cited by 731 · see citing works
Vidal-Gonzalez, I., Vidal-Gonzalez, B., Rauch, S. L., & Quirk, G. J. (2006) · Learning & Memory · doi:10.1101/lm.306106 · Cited by 705 · see citing works
Newman, D. L., Moffitt, T. E., Caspi, A., Magdol, L., Silva, P. A., & Stanton, W. R. (1996) · Journal of Consulting and Clinical Psychology · doi:10.1037/0022-006x.64.3.552 · Cited by 682 · see citing works
Monk, C. S., Telzer, E. H., Mogg, K., Bradley, B. P., Mai, X., Louro, H. M. C., Chen, G., McClure-Tone, E. B., Ernst, M., & Pine, D. S. (2008) · Archives of General Psychiatry · doi:10.1001/archpsyc.65.5.568 · Cited by 682 · cited 2× · see citing works
“Specifically, neural circuits that are affected by early stress, and those which support fear learning and attachment, are highly preserved across different species (e.g., rodents and primates; Lissek et al., 2005; Milad et al., 2008, 2009; Monk et al., 2008).”
Do Rats Have Prefrontal Cortex? The Rose-Woolsey-Akert Program Reconsidered
Preuss, T. M. (1995) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.1995.7.1.1 · Cited by 666 · see citing works
Barbas, H. (2000) · Brain Research Bulletin · doi:10.1016/s0361-9230(99)00245-2 · Cited by 664 · see citing works
Rutter, M. L. (1998) · PubMed · Cited by 653 · see citing works
A review of adversity, the amygdala and the hippocampus: a consideration of developmental timing
Tottenham, N. (2009) · Frontiers in Human Neuroscience · doi:10.3389/neuro.09.068.2009 · Cited by 651 · see citing works
Bradley, R. G., Binder, E. B., Epstein, M. P., Tang, Y., Nair, H. P., Liu, W., Gillespie, C. F., Berg, T., Evces, M., Newport, D. J., et al. (2008) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2007.26 · Cited by 643 · see citing works
Developmental catch-up, and deficit, following adoption after severe global early privation
Rutter, M. (1998) · Journal of Child Psychology and Psychiatry · doi:10.1017/s0021963098002236 · Cited by 640 · see citing works
Monkey to human comparative anatomy of the frontal lobe association tracts
Thiebaut de Schotten, M., Dell’Acqua, F., Valabregue, R., & Catani, M. (2012) · Cortex · doi:10.1016/j.cortex.2011.10.001 · Cited by 632 · see citing works
Fear extinction in rats: Implications for human brain imaging and anxiety disorders
Milad, M. R., Rauch, S. L., Pitman, R. K., & Quirk, G. J. (2006) · Biological Psychology · doi:10.1016/j.biopsycho.2006.01.008 · Cited by 597 · cited 2× · see citing works
“Further, the cognitive and behavioral treatments for anxiety disorders (i.e., exposure therapy) are modeled on the process of extinction (Milad et al., 2006).”
Activity in Prelimbic Cortex Is Necessary for the Expression of Learned, But Not Innate, Fears
Corcoran, K., & Quirk, G. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.5327-06.2007 · Cited by 580 · see citing works
Anxiety in a neglected population: Prevalence of anxiety disorders in pre-adolescent children
Cartwright-Hatton, S., McNicol, K., & Doubleday, E. (2006) · Clinical Psychology Review · doi:10.1016/j.cpr.2005.12.002 · Cited by 543 · see citing works
Impact of child sexual abuse on mental health
Spataro, J., Mullen, P. E., Burgess, P. M., Wells, D. L., & Moss, S. A. (2004) · The British Journal of Psychiatry · doi:10.1192/bjp.184.5.416 · Cited by 538 · see citing works
Burgos-Robles, A., Vidal-Gonzalez, I., & Quirk, G. J. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0378-09.2009 · Cited by 530 · 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
Presence and acquired origin of reduced recall for fear extinction in PTSD: Results of a twin study
Milad, M. R., Orr, S. P., Lasko, N. B., Chang, Y., Rauch, S. L., & Pitman, R. K. (2008) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2008.01.017 · Cited by 512 · 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
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
Variation in neural development as a result of exposure to institutionalization early in childhood
Sheridan, M. A., Fox, N. A., Zeanah, C. H., McLaughlin, K. A., & Nelson, C. A. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1200041109 · Cited by 432 · see citing works
Levine, S. (2001) · Physiology & Behavior · doi:10.1016/s0031-9384(01)00496-6 · Cited by 428 · see citing works
Role of the Basolateral Amygdala in the Storage of Fear Memories across the Adult Lifetime of Rats
Gale, G. D., Anagnostaras, S., Godsil, B. P., Mitchell, S., Nozawa, T., Sage, J. R., Wiltgen, B. J., & Fanselow, M. S. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.4100-03.2004 · Cited by 427 · see citing works
Sánchez, M. M., Young, L. J., Plotsky, P. M., & Insel, T. R. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-12-04657.2000 · Cited by 420 · see citing works
Specificity and heterogeneity in children's responses to profound institutional privation
Rutter, M., Kreppner, J., & O'Connor, T. G. (2001) · British Journal of Psychiatry · doi:10.1192/bjp.179.2.97 · Cited by 418 · see citing works
Croxson, P. L., Johansen-Berg, H., Behrens, T. E. J., Robson, M. D., Pinsk, M. A., Gross, C. G., Richter, W., Richter, M. C., Kastner, S., & Rushworth, M. F. S. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.1311-05.2005 · Cited by 410 · see citing works
Barr, C. S., Newman, T. K., Shannon, C., Parker, C., Dvoskin, R. L., Becker, M. L., Schwandt, M., Champoux, M., Lesch, K. P., Goldman, D., et al. (2004) · Biological Psychiatry · doi:10.1016/j.biopsych.2003.12.008 · Cited by 385 · see citing works
Neonatal maternal separation reduces hippocampal mossy fiber density in adult Long Evans rats
Huot, R. L., Plotsky, P. M., Lenox, R. H., & McNamara, R. K. (2002) · Brain Research · doi:10.1016/s0006-8993(02)02985-2 · Cited by 383 · see citing works
Lupien, S. J., Parent, S., Evans, A. C., Tremblay, R. E., Zelazo, P. D., Corbo, V., Pruessner, J. C., & Séguin, J. R. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1105371108 · Cited by 379 · see citing works
Ladd, C. O., Huot, R. L., Thrivikraman, K. V., Nemeroff, C. B., & Plotsky, P. M. (2004) · Biological Psychiatry · doi:10.1016/j.biopsych.2003.10.007 · Cited by 368 · see citing works
Institutional rearing and psychiatric disorders in Romanian preschool children
Zeanah, C. H., Egger, H. L., Smyke, A. T., Nelson, C. A., Fox, N. A., Marshall, P. J., & Guthrie, D. (2009) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2009.08091438 · Cited by 365 · see citing works
Preuss, T. M., & Goldman‐Rakic, P. S. (1991) · The Journal of Comparative Neurology · doi:10.1002/cne.903100402 · Cited by 359 · see citing works
Campbell, B. A., & Spear, N. E. (1972) · Psychological Review · doi:10.1037/h0032690 · Cited by 351 · see citing works
Casey, B. J., Cohen, J. D., Jezzard, P., Turner, R., Noll, D. C., Trainor, R. J., Giedd, J. N., Kaysen, D. L., Hertz‐Pannier, L., & Rapoport, J. L. (1995) · NeuroImage · doi:10.1006/nimg.1995.1029 · Cited by 349 · 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
Ahnert, L., Gunnar, M. R., Lamb, M. E., & Barthel, M. (2004) · Child Development · doi:10.1111/j.1467-8624.2004.00698.x · Cited by 334 · see citing works
The behaviour of socially living rhesus monkeys in their first two and a half years
Hinde, R. A., & Spencer‐Booth, Y. (1967) · Animal Behaviour · doi:10.1016/s0003-3472(67)80029-0 · Cited by 331 · see citing works
Kiess, W., Meidert, A. S., Dressendörfer, R. A., Schriever, K., Kessler, U., Köunig, A., Hp, S., & Strasburger, C. J. (1995) · Pediatric Research · doi:10.1203/00006450-199504000-00020 · Cited by 319 · see citing works
Memory biases in the anxiety disorders
Coles, M. E., & Heimberg, R. G. (2002) · Clinical Psychology Review · doi:10.1016/s0272-7358(01)00113-1 · Cited by 318 · see citing works
Good memories of bad events in infancy
Sullivan, R. M., Landers, M., Yeaman, B., & Wilson, D. A. (2000) · Nature · doi:10.1038/35024156 · Cited by 315 · 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
The signature of maternal rearing in the methylome in rhesus macaque prefrontal cortex and T cells
Provençal, N., Suderman, M. J., Guillemin, C., Massart, R., Ruggiero, A., Wang, D., Bennett, A. J., Pierre, P. J., Friedman, D. P., Côté, S. M., et al. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.1470-12.2012 · Cited by 312 · see citing works
The smell of danger: A behavioral and neural analysis of predator odor-induced fear
Takahashi, L. K., Nakashima, B. R., Hong, H., & Watanabe, K. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.04.008 · Cited by 298 · see citing works
Social vocalizations can release oxytocin in humans
Seltzer, L. J., Ziegler, T. E., & Pollak, S. D. (2010) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2010.0567 · Cited by 298 · see citing works
Responses to maternal separation : mechanisms and mediators
Kuhn, C. M., & Schanberg, S. M. (1998) · International Journal of Developmental Neuroscience · doi:10.1016/s0736-5748(98)00034-3 · Cited by 287 · see citing works
Polanczyk, G., Caspi, A., Williams, B., Price, T. S., Danese, A., Sugden, K., Uher, R., Poulton, R., & Moffitt, T. E. (2009) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2009.114 · Cited by 285 · see citing works
van Oers, H. J. J., de Kloet, E. R., Whelan, T., & Levine, S. D. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-23-10171.1998 · Cited by 284 · see citing works
Simple Method of Harvesting <i>Limnoria</i> from Nature
Johnson, F. H., & Ray, D. L. (1962) · Science · doi:10.1126/science.135.3506.795-a · Cited by 276 · see citing works
Odor aversion learning by the rat fetus
Smotherman, W. P. (1982) · Physiology & Behavior · doi:10.1016/0031-9384(82)90322-5 · Cited by 270 · see citing works
Juster, R.-P., Bizik, G., Picard, M., Arsenault-Lapierre, G., Sindi, S., Trepanier, L., Marin, M.-F., Wan, N., Sekerovic, Z., Lord, C., et al. (2011) · Development and Psychopathology · doi:10.1017/s0954579411000289 · Cited by 268 · see citing works
The impact of early adverse care on HPA axis development: Nonhuman primate models
Sánchez, M. M. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.06.012 · Cited by 247 · see citing works
Moriceau, S., Wilson, D. A., Levine, S. D., & Sullivan, R. M. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0499-06.2006 · Cited by 240 · see citing works
Early adversity and adult health outcomes
Taylor, S. E., Way, B. M., & Seeman, T. E. (2011) · Development and Psychopathology · doi:10.1017/s0954579411000411 · Cited by 235 · see citing works
Reduced nucleus accumbens reactivity and adolescent depression following early-life stress
Goff, B., Gee, D. G., Telzer, E. H., Humphreys, K. L., Gabard-Durnam, L., Flannery, J., & Tottenham, N. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2012.12.010 · Cited by 234 · see citing works
Self-citationRetention and extinction of learned fear in infant and adult rats
Campbell, B. A., & Campbell, E. H. (1962) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0049182 · Cited by 233 · see citing works
Kreppner, J., Rutter, M. L., Beckett, C., Castle, J., Colvert, E., Groothues, C., Hawkins, A., O’Connor, T. G., Stevens, S. E., & Sonuga-Barke, E. J. S. (2007) · Developmental Psychology · doi:10.1037/0012-1649.43.4.93 · Cited by 231 · see citing works
Kreppner, J. M., Rutter, M., Beckett, C., Castle, J., Colvert, E., Groothues, C., Hawkins, A., O'Connor, T. G., Stevens, S., & Sonuga-Barke, E. J. S. (2007) · Developmental Psychology · doi:10.1037/0012-1649.43.4.931 · Cited by 231 · see citing works
A 10-year perspective of motherless-mother monkey behavior.
Ruppenthal, G. C., & Al, E. (1976) · Journal of Abnormal Psychology · doi:10.1037//0021-843x.85.4.341 · Cited by 218 · see citing works
Raineki, C., Cortés, M. R., Belnoue, L., & Sullivan, R. M. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.5843-11.2012 · Cited by 217 · see citing works
Roth, T. L., & Sullivan, R. M. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.01.032 · Cited by 204 · see citing works
Self-citationAbnormal corticosterone regulation in an immature rat model of continuous chronic stress
Gilles, E. E., Schultz, L., & Baram, T. Z. (1996) · Pediatric Neurology · doi:10.1016/0887-8994(96)00153-1 · Cited by 199 · see citing works
From thought to therapy: lessons from a primate laboratory.
Harlow, H. F., Harlow, M. K., & Suomi, S. J. (1972) · PubMed · Cited by 198 · see citing works
Early-Life Stress Induces Long-term Morphologic Changes in Primate Brain
Spinelli, S., Chefer, S. I., Suomi, S. J., Higley, J. D., Barr, C. S., & Stein, E. A. (2009) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2009.52 · Cited by 193 · see citing works
A 10-year perspective of motherless-mother monkey behavior.
Ruppenthal, G. C., Arling, G. L., Harlow, H. F., et al. (1976) · Journal of Abnormal Psychology · doi:10.1037/0021-843x.85.4.341 · Cited by 193 · see citing works
Fast glucocorticoid actions on brain: Back to the future
Dallman, M. F. (2005) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2005.08.001 · Cited by 192 · see citing works
Developing a neurobehavioral animal model of infant attachment to an abusive caregiver
Raineki, C., Moriceau, S., & Sullivan, R. M. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.12.019 · Cited by 190 · see citing works
Self-citationKim, J. H., & Richardson, R. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.09.003 · Cited by 189 · see citing works
Sánchez, M. M., Noble, P. M., Lyon, C. K., Plotsky, P. M., Davis, M., Nemeroff, C. B., & Winslow, J. T. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.11.032 · Cited by 178 · see citing works
Early life stress impairs fear conditioning in adult male and female rats
Kosten, T. A., Lee, H. J., & Kim, J. J. (2006) · Brain Research · doi:10.1016/j.brainres.2006.03.009 · Cited by 170 · see citing works
Callaghan, B. L., & Richardson, R. (2011) · Behavioral Neuroscience · doi:10.1037/a0022008 · Cited by 169 · see citing works
A Neurobiological Perspective on Early Human Deprivation
Nelson, C. A. (2007) · Child Development Perspectives · doi:10.1111/j.1750-8606.2007.00004.x · Cited by 168 · see citing works
Evidence that GABA transmission mediates context-specific extinction of learned fear
Harris, J. A., & Westbrook, R. F. (1998) · Psychopharmacology · doi:10.1007/s002130050745 · Cited by 164 · see citing works
Behavioral and emotional symptoms of post-institutionalized children in middle childhood
Wiik, K. L., Loman, M. M., Van Ryzin, M. J., Armstrong, J. M., Essex, M. J., Pollak, S. D., & Gunnar, M. R. (2011) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2010.02294.x · Cited by 161 · see citing works
Effect of repetitive infant-infant separation of young monkeys.
Suomi, S. J., Harlow, H. F., & Domek, C. J. (1970) · Journal of Abnormal Psychology · doi:10.1037/h0029809 · Cited by 155 · see citing works
Kim, J. H., Hamlin, A. S., & Richardson, R. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.0596-09.2009 · Cited by 154 · see citing works
Human amygdala development in the absence of species‐expected caregiving
Tottenham, N. (2012) · Developmental Psychobiology · doi:10.1002/dev.20531 · Cited by 149 · 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
Camp, L. L., & Rudy, J. W. (1988) · Developmental Psychobiology · doi:10.1002/dev.420210103 · Cited by 147 · see citing works
Non‐human primate models of childhood psychopathology: the promise and the limitations
Machado, C. J., & Bachevalier, J. (2002) · Journal of Child Psychology and Psychiatry · doi:10.1111/1469-7610.00103 · Cited by 146 · see citing works
Ladd, C. O., Thrivikraman, K. V., Huot, R. L., & Plotsky, P. M. (2005) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2004.12.004 · Cited by 145 · see citing works
Relationship between Prefrontal and Limbic Cortex: A Comparative Anatomical Review; pp. 5–24
Reep, R. L. (2008) · Brain Behavior and Evolution · doi:10.1159/000118849 · Cited by 133 · see citing works
Immature integration and segregation of emotion-related brain circuitry in young children
Qin, S., Young, C. B., Supekar, K., Uddin, L. Q., & Menon, V. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1120408109 · Cited by 130 · see citing works
Payne, C., Machado, C. J., Bliwise, N. G., & Bachevalier, J. (2010) · Hippocampus · doi:10.1002/hipo.20688 · Cited by 129 · see citing works
A developmental dissociation of context and GABA effects on extinguished fear in rats.
Kim, J., & Richardson, R. (2007) · Behavioral Neuroscience · doi:10.1037/0735-7044.121.1.131 · Cited by 123 · see citing works
The role of frontal lobe functioning in the development of infant self-regulatory behavior
Dawson, G., Panagiotides, H., Klinger, L. G., & Hill, D. (1992) · Brain and Cognition · doi:10.1016/0278-2626(92)90066-u · Cited by 122 · see citing works
Rodent model of infant attachment learning and stress
Moriceau, S., Roth, T. L., & Sullivan, R. M. (2010) · Developmental Psychobiology · doi:10.1002/dev.20482 · Cited by 119 · see citing works
Transitions in sensitive period attachment learning in infancy: The role of corticosterone
Sullivan, R. M., & Holman, P. J. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.11.010 · Cited by 117 · see citing works
A developmental dissociation in reinstatement of an extinguished fear response in rats.
Kim, J., & Richardson, R. (2007) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2007.03.004 · Cited by 116 · see citing works
Bayart, F. E. S., Hayashi, K. T., Faull, K. F., Barchas, J. D., & Levine, S. D. (1990) · Behavioral Neuroscience · doi:10.1037/0735-7044.104.1.98 · Cited by 113 · see citing works
Knickmeyer, R. C., Styner, M. A., Short, S. J., Lubach, G. R., Kang, C., Hamer, R. M., Coe, C. L., & Gilmore, J. H. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp166 · Cited by 113 · see citing works
Neural correlates of maternal separation in rhesus monkeys
Rilling, J. K., Winslow, J., O’Brien, D., Gutman, D. A., Hoffman, J. M., & Kilts, C. D. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(00)00977-x · Cited by 108 · see citing works
Emergence of Interoceptive and Exteroceptive Control of Behavior in Rats
Haroutunian, V. H., & Campbell, B. A. (1979) · Science · doi:10.1126/science.472715 · Cited by 105 · see citing works
Behavioral Effects of Prolonged Partial Social Isolation in the Rhesus Monkey
Suomi, S. J., Harlow, H. F., & Kimball, S. D. (1971) · Psychological Reports · doi:10.2466/pr0.1971.29.3f.1171 · Cited by 105 · see citing works
Frontal Lobe Involvement in Cognitive Changes During the First Year of Life
Diamond, A. (2017) · Routledge eBooks · doi:10.4324/9781315082028-7 · Cited by 99 · see citing works
Callaghan, B. L., & Richardson, R. (2012) · Translational Psychiatry · doi:10.1038/tp.2012.65 · Cited by 97 · see citing works
Boyce, W. T., Champoux, M., Suomi, S. J., & Gunnar, M. R. (1995) · Developmental Psychobiology · doi:10.1002/dev.420280502 · Cited by 93 · see citing works
Sex-selective effects of neonatal isolation on fear conditioning and foot shock sensitivity
Kosten, T. A., Miserendino, M. J. D., Bombace, J. C., Lee, H. J., & Kim, J. J. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2004.07.001 · Cited by 93 · see citing works
Preuss, T. M., & Goldman, P. S. (1991) · The Journal of Comparative Neurology · doi:10.1002/cne.903100404 · Cited by 90 · see citing works
Extinction in the developing rat: an examination of renewal effects.
Yap, C., & Richardson, R. (2007) · Developmental Psychobiology · doi:10.1002/dev.20244 · Cited by 84 · see citing works
Environmental regulation of the neural epigenome
Caldji, C., Hellstrom, I. C., Zhang, T.-Y., Diorio, J., & Meaney, M. J. (2011) · FEBS Letters · doi:10.1016/j.febslet.2011.03.032 · Cited by 82 · see citing works
Risk Factors for Infant Abuse and Neglect in Group-Living Rhesus Monkeys
Maestripieri, D., & Carroll, K. A. (1998) · Psychological Science · doi:10.1111/1467-9280.00027 · Cited by 76 · see citing works
Beane, M. L., Cole, M. A., Spencer, R. L., & Rudy, J. W. (2002) · Hormones and Behavior · doi:10.1006/hbeh.2001.1725 · Cited by 75 · see citing works
Postnatal development of the amygdala: A stereological study in macaque monkeys
Chareyron, L. J., Lavenex, P. B., Amaral, D. G., & Lavenex, P. (2011) · The Journal of Comparative Neurology · doi:10.1002/cne.23023 · Cited by 72 · see citing works
Defining age limits of the sensitive period for attachment learning in rat pups
Upton, K. J., & Sullivan, R. M. (2010) · Developmental Psychobiology · doi:10.1002/dev.20448 · Cited by 71 · see citing works
Takahashi, L. K. (1994) · Developmental Brain Research · doi:10.1016/0165-3806(94)90074-4 · Cited by 70 · see citing works
Early experiences and the development of emotional learning systems in rats
Callaghan, B. L., & Richardson, R. (2013) · Biology of Mood & Anxiety Disorders · doi:10.1186/2045-5380-3-8 · Cited by 70 · see citing works
Self-citationWilber, A. A., Southwood, C. J., & Wellman, C. L. (2008) · Developmental Neurobiology · doi:10.1002/dneu.20691 · Cited by 64 · see citing works
Li, S., Kim, J. H., & Richardson, R. (2012) · Behavioral Neuroscience · doi:10.1037/a0027151 · Cited by 64 · see citing works
Olfactory-mediated fear-potentiated startle.
Paschall, G. Y., & Davis, M. E. (2002) · Behavioral Neuroscience · doi:10.1037//0735-7044.116.1.4 · Cited by 60 · see citing works
Editorial: Moments in Time—The Neonatal Rat Hypothalamo-Pituitary-Adrenal Axis
Dallman, M. F. (2000) · Endocrinology · doi:10.1210/endo.141.5.7527 · Cited by 48 · see citing works
Olfactory-mediated fear-potentiated startle.
Paschall, G. Y., & Davis, M. E. (2002) · Behavioral Neuroscience · doi:10.1037/0735-7044.116.1.4 · Cited by 47 · see citing works
Ontogeny of Nociception and Antinociception
Barr, G. A. (1995) · PsycEXTRA Dataset · doi:10.1037/e495712006-011 · Cited by 47 · see citing works
Kim, J. H., Li, S., Hamlin, A. S., McNally, G. P., & Richardson, R. (2012) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2011.09.005 · Cited by 46 · see citing works
Development switch in neural circuitry underlying odor-malaise learningPreprint
Shionoya, K., Moriceau, S., Lunday, L., Miner, C. A., Roth, T. L., & Sullivan, R. M. (2006) · Learning & Memory · doi:10.1101/lm.316006 · Cited by 43 · see citing works
Early life programming of innate fear and fear learning in adult female rats
Stevenson, C. W., Meredith, J. P., Spicer, C. H., Mason, R., & Marsden, C. A. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.10.021 · Cited by 35 · see citing works
The Clinical-Basic Interface in Defining Pathogenesis in Disorders of Neurodevelopmental Origin
Thompson, B. L., & Levitt, P. R. (2010) · Neuron · doi:10.1016/j.neuron.2010.08.037 · Cited by 33 · see citing works
Development of circadian periodicity in base and stress levels of corticosterone
Levin, R., & Levine, S. (1975) · American Journal of Physiology-Legacy Content · doi:10.1152/ajplegacy.1975.229.5.1397 · Cited by 30 · see citing works
Stress inoculation facilitates active avoidance learning of the semi-precocial rodent Octodon degus
Abraham, A., & Gruß, M. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.05.018 · Cited by 23 · see citing works
A Phylogenetic Perspective for Social Behavior in Primates
Seay, B. M., & Gottfried, N. W. (1975) · The Journal of General Psychology · doi:10.1080/00221309.1975.9711323 · Cited by 15 · see citing works
Huttenlocher (1997) · doi:10.1002/(sici)1096-9861(19971020)387:2
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Research works printed but not linked: 2
- Levine S 1962 Plasma-free corticosteroid response to electric shock in rats stimulated in infancy Science 135 795 796 14464660
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Cited by
Sorted by citations
Poverty, Stress, and Brain Development: New Directions for Prevention and Intervention
Blair, C., & Raver, C. C. (2016) · Academic Pediatrics · doi:10.1016/j.acap.2016.01.010 · Cited by 543 · see citing works
Sensitive periods of substance abuse: Early risk for the transition to dependence
Jordan, C. J., & Andersen, S. L. (2017) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2016.10.004 · Cited by 455 · see citing works
“…early deprivation show blunted ventral STR NAc) activity during a reward anticipation task (Mehta et al., 2010). n addition to PFC → STR changes, the amygdala shows increased ctivity in human fMRI studies and in animals exposed to early life tress (recently reviewed by Callaghan et al., 2014).”
Stress and the adolescent brain
Tottenham, N., & Galván, A. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.07.030 · Cited by 324 · see citing works
Self-citationCallaghan, B. L., & Tottenham, N. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2015.204 · Cited by 268 · 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
Herzberg, M. P., & Gunnar, M. R. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.116493 · Cited by 238 · see citing works
Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex?
Piekarski, D. J., Johnson, C. M., Boivin, J. R., Thomas, A. W., Lin, W. C., Delevich, K., M. Galarce, E., & Wilbrecht, L. (2017) · Brain Research · doi:10.1016/j.brainres.2016.08.042 · Cited by 175 · see citing works
VanTieghem, M., & Tottenham, N. (2017) · Current topics in behavioral neurosciences · doi:10.1007/7854_2016_42 · Cited by 170 · see citing works
Gunnar, M. R., Hostinar, C. E., Sanchez, M. M., Tottenham, N., & Sullivan, R. M. (2015) · Social Neuroscience · doi:10.1080/17470919.2015.1070198 · Cited by 158 · see citing works
Teissier, A., Magueresse, C. L., Olusakin, J., da Costa, B. L. S. A., Stasi, A. M. D., Bacci, A., Kawasawa, Y. I., Vaidya, V. A., & Gaspar, P. (2019) · Molecular Psychiatry · doi:10.1038/s41380-019-0493-2 · Cited by 154 · see citing works
Dennison, M., Rosen, M. L., Sambrook, K., Jenness, J. L., Sheridan, M. A., & McLaughlin, K. A. (2017) · Child Development · doi:10.1111/cdev.13011 · Cited by 149 · see citing works
Silvers, J. A., Lumian, D. S., Gabard-Durnam, L., Gee, D. G., Goff, B., Fareri, D. S., Caldera, C., Flannery, J., Telzer, E. H., Humphreys, K. L., et al. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.0038-16.2016 · Cited by 140 · see citing works
Implications of newborn amygdala connectivity for fear and cognitive development at 6-months-of-age
Graham, A. M., Buss, C., Rasmussen, J. M., Rudolph, M. D., Demeter, D. V., Gilmore, J. H., Styner, M., Entringer, S., Wadhwa, P. D., & Fair, D. A. (2016) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2015.09.006 · Cited by 122 · see citing works
Social scaffolding of human amygdala-mPFCcircuit development
Tottenham, N. (2015) · Social Neuroscience · doi:10.1080/17470919.2015.1087424 · Cited by 112 · see citing works
Self-citationGee, D. G. (2016) · New Directions for Child and Adolescent Development · doi:10.1002/cad.20166 · Cited by 104 · see citing works
A novel ecological account of prefrontal cortex functional development.
Werchan, D. M., & Amso, D. (2017) · Psychological Review · doi:10.1037/rev0000078 · Cited by 101 · see citing works
Yan, C., Rincón‐Cortés, M., Raineki, C., Sarro, E. C., Colcombe, S. J., Guilfoyle, D. N., Yang, Z., Gerum, S. V., Biswal, B. B., Milham, M. P., et al. (2017) · Translational Psychiatry · doi:10.1038/tp.2016.276 · Cited by 96 · see citing works
Opendak, M., Gould, E., & Sullivan, R. (2017) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2017.02.002 · Cited by 94 · see citing works
Self-citationGuadagno, A., Belliveau, C., Mechawar, N., & Walker, C. (2021) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2021.669120 · Cited by 92 · see citing works
Resilience and young people’s brain structure, function and connectivity: A systematic review
Eaton, S., Cornwell, H., Hamilton-Giachritsis, C. E., & Fairchild, G. F. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.11.001 · Cited by 88 · see citing works
Santiago, A. N., Lim, K. Y., Opendak, M., Sullivan, R. M., & Aoki, C. (2018) · Journal of Comparative Neurology · doi:10.1002/cne.24522 · Cited by 87 · see citing works
Early life stress is associated with default system integrity and emotionality during infancy
Graham, A. M., Pfeifer, J. H., Fisher, P. A., Carpenter, S., & Fair, D. A. (2015) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.12409 · Cited by 84 · see citing works
Using a Developmental Ecology Framework to Align Fear Neurobiology Across Species
Callaghan, B. L., Meyer, H. C., Opendak, M. M., Tieghem, M. V., Harmon, C., Li, A., Lee, F. S., Sullivan, R. M., & Tottenham, N. (2019) · Annual Review of Clinical Psychology · doi:10.1146/annurev-clinpsy-050718-095727 · Cited by 81 · see citing works
Newborn amygdala connectivity and early emerging fear
Thomas, E., Buß, C., Rasmussen, J. M., Entringer, S., Ramirez, J. S. B., Marr, M. C., Rudolph, M. D., Gilmore, J. H., Styner, M. A., Wadhwa, P. D., et al. (2018) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2018.12.002 · Cited by 77 · see citing works
Perry, R. E., Finegood, E. D., Braren, S. H., DeJoseph, M. L., Putrino, D. F., Wilson, D. A., Sullivan, R. M., Raver, C. C., Blair, C., & Family Life Project Key Investigators (2018) · Development and Psychopathology · doi:10.1017/s095457941800007x · Cited by 74 · see citing works
Numan, M. (2020) · doi:10.1093/oso/9780190848675.001.0001 · Cited by 101 · see citing works
Plasticity‐related genes in brain development and amygdala‐dependent learning
Ehrlich, D., & Josselyn, S. A. (2015) · Genes Brain & Behavior · doi:10.1111/gbb.12255 · Cited by 68 · see citing works
Cowan, C. S. M., Stylianakis, A. A., & Richardson, R. (2019) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2019.100627 · Cited by 70 · see citing works
The Stress Acceleration Hypothesis of Nightmares
Nielsen, T. (2017) · Frontiers in Neurology · doi:10.3389/fneur.2017.00201 · Cited by 63 · see citing works
Hill, M. N., Eiland, L. R., Lee, T. T.-Y., Hillard, C. J., & McEwen, B. S. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.11.036 · Cited by 62 · see citing works
An Adolescent Sensitive Period for Threat Responding: Impacts of Stress and Sex
Gerhard, D. M., Meyer, H. C., & Lee, F. S. (2021) · Biological Psychiatry · doi:10.1016/j.biopsych.2020.10.003 · Cited by 54 · see citing works
Lean, R. E., Smyser, C. D., Brady, R. G., Triplett, R. L., Kaplan, S., Kenley, J. K., Shimony, J. S., Smyser, T. A., Miller, J. P., Barch, D. M., et al. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2204135119 · Cited by 54 · see citing works
Opendak, M. M., Robinson-Drummer, P. A., Blomkvist, A., Zanca, R. M., Wood, K., Jacobs, L., Chan, S., Tan, S., Woo, J., Venkataraman, G., et al. (2019) · Neuropsychopharmacology · doi:10.1038/s41386-019-0340-9 · Cited by 56 · see citing works
VanTieghem, M., Gabard-Durnam, L. J., Goff, B., Flannery, J., Humphreys, K. L., Telzer, E. H., Caldera, C., Louie, J., Shapiro, M., Bolger, N. P., et al. (2017) · Development and Psychopathology · doi:10.1017/s0954579417000153 · Cited by 53 · see citing works
Herzberg, M. P., Jedd, K., Hodel, A. S., Hunt, R. H., Mueller, B. A., Gunnar, M. R., & Thomas, K. M. (2021) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2021.100922 · Cited by 50 · see citing works
Vigilance, the Amygdala, and Anxiety in Youths With a History of Institutional Care
Silvers, J. A., Goff, B., Gabard-Durnam, L. J., Gee, D. G., Fareri, D. S., Caldera, C., & Tottenham, N. (2017) · Biological Psychiatry Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2017.03.016 · Cited by 46 · see citing works
Andre, Q. R., McMorris, C. A., Kar, P., Ritter, C., Gibbard, W. B., Tortorelli, C., & Lebel, C. A. (2020) · Human Brain Mapping · doi:10.1002/hbm.25130 · Cited by 41 · see citing works
Change of pace: How developmental tempo varies to accommodate failed provision of early needs
Roubinov, D. S., Meaney, M. J., & Boyce, W. T. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.09.031 · Cited by 40 · see citing works
Over-generalization in youth with anxiety disorders
El-Bar, N., Laufer, O., Yoran‐Hegesh, R., & Paz, R. (2016) · Social Neuroscience · doi:10.1080/17470919.2016.1167123 · Cited by 36 · see citing works
Implications of the Research Domain Criteria project for childhood anxiety and its disorders
Lebowitz, E. R., Gee, D. G., Pine, D. S., & Silverman, W. K. (2018) · Clinical Psychology Review · doi:10.1016/j.cpr.2018.01.005 · Cited by 33 · see citing works
Ferber, S. G., Trezza, V., & Weller, A. (2019) · Developmental Psychobiology · doi:10.1002/dev.21944 · Cited by 33 · see citing works
Adjimann, T. S., Argañaraz, C., & Soiza‐Reilly, M. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01388-6 · Cited by 32 · see citing works
The developmental consequences of early adverse care on infant macaques: A cross-fostering study
McCormack, K. M., Howell, B., Higgins, M. K., Bramlett, S. N., Guzman, D., Morin, E. L., Villongco, C., Liu, Y., Meyer, J. S., & Sánchez, M. M. (2022) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2022.105947 · Cited by 30 · see citing works
Opendak, M. M., & Sullivan, R. M. (2016) · European Journal of Psychotraumatology · doi:10.3402/ejpt.v7.31276 · Cited by 29 · 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
Sanders, A. F. P., Tirado, B. A., Seider, N. A., Triplett, R. L., Lean, R. E., Neil, J. J., Miller, J. P., Tillman, R., Smyser, T. A., Barch, D. M., et al. (2024) · Translational Psychiatry · doi:10.1038/s41398-024-02782-6 · Cited by 27 · see citing works
Gehrand, A. L., Hoeynck, B., Jablonski, M., Leonovicz, C., Ye, R., Scherer, P. E., & Raff, H. (2016) · Physiological Reports · doi:10.14814/phy2.12972 · Cited by 25 · see citing works
Knop, J., Joëls, M., & van der Veen, R. (2017) · Current Opinion in Psychology · doi:10.1016/j.copsyc.2017.02.030 · Cited by 26 · see citing works
Key Factors and Threats to Team Dynamics in Long-Duration Extreme Environments
Roma, P. G., & Bedwell, W. L. (2017) · Research on managing groups and teams · doi:10.1108/s1534-085620160000018007 · Cited by 25 · see citing works
Gee, D. G., & Cohodes, E. M. (2023) · Development and Psychopathology · doi:10.1017/s0954579423001128 · Cited by 25 · see citing works
New policies on skin-to-skin contact warrant an oxytocin-based perspective on perinatal health care
Bergman, N. (2024) · Frontiers in Psychology · doi:10.3389/fpsyg.2024.1385320 · Cited by 23 · see citing works
Silvers, J. A. (2020) · Child Development Perspectives · doi:10.1111/cdep.12372 · Cited by 23 · see citing works
Packard, K., & Opendak, M. M. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.918862 · Cited by 23 · see citing works
Kooiker, C. L., Chen, Y., Birnie, M. T., & Baram, T. Z. (2023) · Biological Psychiatry Global Open Science · doi:10.1016/j.bpsgos.2023.01.002 · Cited by 20 · see citing works
Gehrand, A. L., Hoeynck, B., Jablonski, M., Leonovicz, C., Cullinan, W. E., & Raff, H. (2018) · Endocrinology · doi:10.1210/en.2018-00370 · Cited by 19 · see citing works
Fischer, J. T., Bickart, K. C., Giza, C. C., & Babikian, T. (2021) · Biological Psychiatry · doi:10.1016/j.biopsych.2021.08.012 · Cited by 20 · see citing works
Jarrar, Q., Ayoub, R., Alhussine, K., Goh, K. W., Moshawih, S., Ardianto, C., Goh, B. H., & Ming, L. C. (2022) · Journal of Personalized Medicine · doi:10.3390/jpm12111921 · Cited by 22 · see citing works
Howland, M. A. (2023) · Development and Psychopathology · doi:10.1017/s0954579423000998 · Cited by 19 · see citing works
Toward an animal model of borderline personality disorder
Corniquel, M. B., Koenigsberg, H. W., & Likhtik, E. (2019) · Psychopharmacology · doi:10.1007/s00213-019-05289-x · Cited by 18 · see citing works
Perry, R. E., Braren, S. H., Opendak, M. M., Brandes-Aitken, A. N., Chopra, D., Woo, J., Sullivan, R. M., Blair, C., & Family Life Project Key Investigators (2020) · Development and Psychopathology · doi:10.1017/s0954579420001455 · Cited by 17 · see citing works
Early adversity and the regulation of gene expression: implications for prenatal health
Gillespie, S. L., Cole, S. W., & Christian, L. M. (2019) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2019.02.005 · Cited by 17 · see citing works
Juvenile confinement exacerbates adversity burden: A neurobiological impetus for decarceration
Orendain, N., Galván, A., Smith, E., Barnert, E. S., & Chung, P. J. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.1004335 · Cited by 18 · see citing works
Huskey, A., Taylor, D. J., & Friedman, B. H. (2022) · Developmental Psychobiology · doi:10.1002/dev.22242 · Cited by 18 · see citing works
Haikonen, J., Englund, J., Amarilla, S. P., Kharybina, Z., Shintyapina, A. B., Kegler, K., Garcia, M. S., Atanasova, T., Taira, T., Hartung, H., et al. (2022) · iScience · doi:10.1016/j.isci.2022.105724 · Cited by 15 · see citing works
Evidence for cultural differences in affect during mother–infant interactions
Salih, M. A., Abargil, M., Badarneh, S., Selle, N. K., Irani, M., & Atzil, S. (2023) · Scientific Reports · doi:10.1038/s41598-023-31907-y · Cited by 17 · see citing works
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Raper, J., & Chahroudi, A. (2021) · Tropical Medicine and Infectious Disease · doi:10.3390/tropicalmed6010010 · Cited by 15 · 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
Pagliaccio, D., Pine, D. S., Leibenluft, E., Monte, O. D., Averbeck, B. B., & Costa, V. D. (2019) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsz041 · Cited by 12 · see citing works
An Overview of Trauma-Informed Care
Sciolla, A. (2017) · Springer eBooks · doi:10.1007/978-3-319-54509-7_14 · Cited by 11 · see citing works
Effects of early-life stress on fear memory in the developing rat
Richardson, R., Cowan, C. S., Callaghan, B. L., & Kan, J. M. (2016) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2015.10.003 · Cited by 10 · see citing works
Self-citationLyons‐Ruth, K., Chasson, M., Khoury, J. E., & Ahtam, B. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105746 · Cited by 11 · see citing works
Family environment and development in children adopted from institutionalized care
Keil, M. F., Leahu, A., Rescigno, M., Myles, J. G., & Stratakis, C. A. (2021) · Pediatric Research · doi:10.1038/s41390-020-01325-1 · Cited by 12 · see citing works
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Boulanger-Bertolus, J., Mouly, A., & Sullivan, R. M. (2016) · Learning & Memory · doi:10.1101/lm.042218.116 · Cited by 9 · see citing works
Adebiyi, O. E., Adigun, K. O., Adebiyi, A. I., & Odenibi, B. S. (2022) · Neuroscience · doi:10.1016/j.neuroscience.2022.02.026 · Cited by 8 · see citing works
Kooiker, C. L., Hardy, M., Birnie, M. T., Chen, Y., de Carvalho, G., Floriou‐Servou, A., Ding, Q., Thiagarajan, N., Tetzlaff, M. R., Smith, A., et al. (2026) · Biological Psychiatry Global Open Science · doi:10.1016/j.bpsgos.2026.100840 · Cited by 10 · see citing works
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Zeng, H., Yu, Z., Huang, Q., & Xu, H. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.637678 · Cited by 8 · see citing works
A precision medicine approach to pharmacological adjuncts to extinction: A call to broaden research
King, G., Baker, K. D., Bisby, M. A., Chan, D., Cowan, C. S. M., Stylianakis, A. A., Zimmermann, K. S., & Richardson, R. (2019) · Psychopharmacology · doi:10.1007/s00213-018-4999-0 · Cited by 6 · see citing works
Repeated cross‐fostering affects maternal behavior and olfactory preferences in rat pups
Finkler, A. D., Pardo, G. V. E., & Lucion, A. B. (2019) · Developmental Psychobiology · doi:10.1002/dev.21907 · Cited by 6 · see citing works
Neurobiology and programming capacity of attachment learning to nurturing and abusive caregivers
Roth, T. L., Barr, G. A., Lewis, M. J., & Sullivan, R. M. (2016) · Wiley eBooks · doi:10.1002/9781118931684.ch6 · Cited by 6 · see citing works
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Lean, R. E., Constantino-Pettit, A. M., Gorham, L. S., Herzberg, M. P., Anaya, B., Rogers, C. E., & Luby, J. L. (2025) · Neuropsychopharmacology · doi:10.1038/s41386-025-02169-1 · Cited by 7 · see citing works
Early-Life Experiences: Enduring Behavioral, Neurological, and Endocrinological Consequences
Romeo, R. D., Tang, A. C., & Sullivan, R. M. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-803592-4.00099-7 · Cited by 5 · see citing works
Factors Affecting Emission of Infantile Vocalizations and Vocal Expression of Emotional States
Shair, H. N. (2018) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-809600-0.00015-9 · Cited by 5 · see citing works
Rebello, K., Moura, L. M., Bueno, A. P. A., Picon, F., Pan, P., Gadelha, A., Miguel, E., Bressan, R., Rohde, L., & Sato, J. (2022) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph19106055 · Cited by 3 · see citing works
Lean, R. E., Kenley, J. K., Latham, A. R., Smyser, T. A., Neil, J. J., Nielsen, A. N., Sylvester, C. M., Miller, J. P., Shimony, J. S., Luby, J. L., et al. (2025) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2025.04.016 · Cited by 2 · see citing works
Salivary Bioscience in Military, Space, and Operational Research
Roma, P. G., Beckner, M. E., Mehta, S. K., Nindl, B. C., & Crucian, B. E. (2020) · Springer eBooks · doi:10.1007/978-3-030-35784-9_24 · Cited by 2 · see citing works
张, 梦. (2022) · Advances in Psychology · doi:10.12677/ap.2022.1210407 · Cited by 2 · see citing works
Numan, M. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190848675.003.0008 · Cited by 2 · see citing works
Hormonal Control of Maternal Behavior in Nonhuman Mammals
Numan, M. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190848675.003.0003 · Cited by 2 · see citing works
Ranger, M., Behring, T. B., Kaidbey, J. H., Anwar, M., Lipshutz, A. B., Mollicone, I., Hassan, G., Fasano, K. M., Hinz, N. K., Ludwig, R. J., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.05.19.444831 · Cited by 2 · see citing works
Numan, M. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190848675.003.0002 · Cited by 1 · see citing works
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de Lemos, K. G., & Carvalho, A. L. N. (2023) · Ensaios USF · doi:10.24933/e-usf.v7i2.350 · Cited by 2 · see citing works
Posttraumatic Stress Disorder: From Neurobiology to Cycles of Violence
McCullough, K. M., & Ressler, K. J. (2018) · Springer eBooks · doi:10.1007/978-3-030-00503-0_3 · Cited by 1 · see citing works
Threat Sensitivity of Adolescents with Abuse Histories: The Impact of Residential Care
Blair, K. S., Bashford‐Largo, J., Bajaj, S., Zhang, R., Mathur, A., Elowsky, J., Dominguez, A. J., Emmert, A. D., Dobbertin, M. D., Tottenham, N., et al. (2025) · Residential Treatment for Children & Youth · doi:10.1080/0886571x.2025.2543392 · Cited by 1 · see citing works
Numan, M. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190848675.003.0001 · Cited by 1 · see citing works
Central Neural Circuits Regulating Maternal Behavior in Nonhuman Mammals
Numan, M. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190848675.003.0005 · Cited by 1 · see citing works
Alloparental Behavior and Paternal Behavior in Nonhuman Mammals
Numan, M. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190848675.003.0007 · Cited by 1 · see citing works
Катан, Е. А. (2020) · S S Korsakov Journal of Neurology and Psychiatry · doi:10.17116/jnevro2020120111141 · Cited by 2 · see citing works
Elison, J. T., & Sera, M. D. (2018) · Wiley eBooks · doi:10.1002/9781119461746.ch2 · Cited by 1 · see citing works
“When you talk about it, something in your heart becomes lighter”
Sarkadi, A., & Warner, G. (2020) · European Child & Adolescent Psychiatry · doi:10.1007/s00787-020-01538-z
Evolutionary Perspectives on the Parental Brain
Numan, M. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190848675.003.0011
- Authors
- Callaghan, B. L., Sullivan, R. M., Howell, B., & Tottenham, N.
- Affiliations
- Columbia University (US)
- New York University (US)
- Emory University (US)
- University of California, Los Angeles (US)
- Corresponding author
- Callaghan, Bridget L.
- Venue
- Developmental Psychobiology
- Publisher
- Wiley
- Published
- 2014-10-07
- Volume
- 56
- Issue
- 8
- Pages
- 1635-1650
- ISSN
- 0012-1630 (ISSN-L)
- 1098-2302
- PMC
- PMC4831705
- OpenAlex
- W1506262237
- Cited by
- 115
- References
- 140
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 3 · 2023: 7 · 2022: 11 · 2021: 10 · 2020: 25 · 2019: 13 · 2018: 10 · 2017: 11 · 2016: 13 · 2015: 7
- FWCI
- 0.84
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Developmental Psychobiology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (FMH086203A, R01MH091864, NIH-MH091451, NIH-DC009910)
- Dana Foundation
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Social Sciences › Psychology › Clinical Psychology › Child Abuse and Trauma
- Keywords
- childhood adversity, emotional development, amygdala, prefrontal cortex, caregiver-infant relationship, attachment disruption, fear learning, fear extinction, maternal deprivation, orphanage children, maternal abuse, rhesus monkeys, rodent models, cross-species comparison
- MeSH terms
- Amygdala, Animals, Animals, Newborn, Child Abuse, Disease Models, Animal, Fear, Humans, Infant, Macaca mulatta, Maternal Deprivation, Object Attachment, Prefrontal Cortex, Rats
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