1932

Abstract

Children's development is largely dependent on caregiving; when caregiving is disrupted, children are at increased risk for numerous poor outcomes, in particular psychopathology. Therefore, determining how caregivers regulate children's affective neurobiology is essential for understanding psychopathology etiology and prevention. Much of the research on affective functioning uses fear learning to map maturation trajectories, with both rodent and human studies contributing knowledge. Nonetheless, as no standard framework exists through which to interpret developmental effects across species, research often remains siloed, thus contributing to the current therapeutic impasse. Here, we propose a developmental ecology framework that attempts to understand fear in the ecological context of the child: their relationship with their parent. By referring to developmental goals that are shared across species (to attach to, then, ultimately, separate from the parent), this framework provides a common grounding from which fear systems and their dysfunction can be understood, thus advancing research on psychopathologies and their treatment.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-clinpsy-050718-095727
2019-05-07
2024-12-05
Loading full text...

Full text loading...

/deliver/fulltext/clinpsy/15/1/annurev-clinpsy-050718-095727.html?itemId=/content/journals/10.1146/annurev-clinpsy-050718-095727&mimeType=html&fmt=ahah

Literature Cited

  1. Adolph KE, Berger SE 2006. Motor development. Handbook of Child Psychology, Vol. 2: Cognition, Perception, and Language161–213 New York: Wiley. , 6th ed..
    [Google Scholar]
  2. Ahnert L, Gunnar MR, Lamb ME, Barthel M 2004. Transition to child care: associations with infant–mother attachment, infant negative emotion, and cortisol elevations. Child Dev 75:639–50
    [Google Scholar]
  3. Ainsworth MD, Bell SM 1970. Attachment, exploration, and separation: illustrated by the behavior of one-year-olds in a strange situation. Child Dev 41:49–67
    [Google Scholar]
  4. Al Aïn S, Perry RE, Kayser K, Hochman C, Brehman E et al. 2017. Neurobehavioral assessment of maternal odor in developing rat pups: implications for social buffering. Soc. Neurosci. 12:32–49
    [Google Scholar]
  5. Andrews K, Fitzgerald M 1997. Barriers to optimal pain management in infants, children, and adolescents: biological barriers to paediatric pain management. Clin. J. Pain 13:138–43
    [Google Scholar]
  6. Anisfeld E, Casper V, Nozyce M, Cunningham N 1990. Does infant carrying promote attachment? An experimental study of the effects of increased physical contact on the development of attachment. Child Dev 61:1617–27
    [Google Scholar]
  7. Arruda-Carvalho M, Wu W-C, Cummings KA, Clem RL 2017. Optogenetic examination of prefrontal—amygdala synaptic development. J. Neurosci. 37:2976–85
    [Google Scholar]
  8. Artioli F, Reese E 2014. Early memories in young adults from separated and non-separated families. Memory 22:1082–102
    [Google Scholar]
  9. Baker KD, Bisby MA, Richardson R 2016. Impaired fear extinction in adolescent rodents: behavioural and neural analyses. Neurosci. Biobehav. Rev. 70:59–73
    [Google Scholar]
  10. Barr GA 1995. Ontogeny of nociception and antinociception. NIDA Res. Monogr. 158:172–201
    [Google Scholar]
  11. Barr GA, Moriceau S, Shionoya K, Muzny K, Gao P et al. 2009. Transitions in infant learning are modulated by dopamine in the amygdala. Nat. Neurosci. 12:1367–69
    [Google Scholar]
  12. Bath KG, Manzano-Nieves G, Goodwill H 2016. Early life stress accelerates behavioral and neural maturation of the hippocampus in male mice. Horm. Behav. 82:64–71
    [Google Scholar]
  13. Bayer SA, Altman J, Russo R, Zhang X 1993. Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat. Neurotoxicology 14:83–144
    [Google Scholar]
  14. Block JD, Sersen EA, Wortis J 1970. Cardiac classical conditioning and reversal in the Mongoloid, encephalopathic, and normal child. Child Dev 41:771–85
    [Google Scholar]
  15. Bolles RC, Woods PJ 1964. The onotogeny of behavior in the albino rat. Anim. Behav. 12:425–41
    [Google Scholar]
  16. Bos K, Zeanah CH, Fox NA, Drury SS, McLaughlin KA, Nelson CA 2011. Psychiatric outcomes in young children with a history of institutionalization. Harv. Rev. Psychiatry 19:15–24
    [Google Scholar]
  17. Bowlby J 1969. Attachment and Loss 1 Attachment New York: Basic Books
    [Google Scholar]
  18. Bowlby J 1977. The making and breaking of affectional bonds. I. Aetiology and psychopathology in the light of attachment theory. An expanded version of the Fiftieth Maudsley Lecture, delivered before the Royal College of Psychiatrists, 19 November 1976. Br. J. Psychiatry 130:201–10
    [Google Scholar]
  19. Bronfenbrenner U 1977. Toward an experimental ecology of human development. Am. Psychol. 32:513–31
    [Google Scholar]
  20. Butler H, Juurlink B 1987. An Atlas for Staging Mammalian and Chick Embryos Boca Raton, FL: CRC Press
    [Google Scholar]
  21. Callaghan BL, Dandash O, Simmons J, Schwartz O, Byrne ML et al. 2017. Amygdala resting connectivity mediates association between maternal aggression and adolescent major depression: a 7-year longitudinal study. J. Am. Acad. Child Adolesc. Psychiatry 56:983–991
    [Google Scholar]
  22. Callaghan BL, Richardson R 2011. Maternal separation results in early emergence of adult-like fear and extinction learning in infant rats. Behav. Neurosci. 125:20–28
    [Google Scholar]
  23. Callaghan BL, Richardson R 2012a. Early-life stress affects extinction during critical periods of development: an analysis of the effects of maternal separation on extinction in adolescent rats. Stress 15:671–79
    [Google Scholar]
  24. Callaghan BL, Richardson R 2012b. The effect of adverse rearing environments on persistent memories in young rats: removing the brakes on infant fear memories. Transl. Psychiatry 2:e138
    [Google Scholar]
  25. Callaghan BL, Sullivan RM, Howell B, Tottenham N 2014. The International Society for Developmental Psychobiology Sackler Symposium: early adversity and the maturation of emotion circuits—a cross‐species analysis. Dev. Psychobiol. 56:1635–50
    [Google Scholar]
  26. Callaghan BL, Tottenham N 2016a. The neuro-environmental loop of plasticity: a cross-species analysis of parental effects on emotion circuitry development following typical and adverse caregiving. Neuropsychopharmacology 41:163–76
    [Google Scholar]
  27. Callaghan BL, Tottenham N 2016b. The stress acceleration hypothesis: effects of early-life adversity on emotion circuits and behavior. Curr. Opin. Behav. Sci. 7:76–81
    [Google Scholar]
  28. Camp LL, Rudy JW 1988. Changes in the categorization of appetitive and aversive events during postnatal development of the rat. Dev. Psychobiol. 21:25–42
    [Google Scholar]
  29. Campbell BA, Spear NE 1972. Ontogeny of memory. Psychol. Rev. 79:215–36
    [Google Scholar]
  30. Casey BJ, Glatt CE, Lee FS 2015. Treating the developing versus developed brain: translating preclinical mouse and human studies. Neuron 86:1358–68
    [Google Scholar]
  31. Casey BJ, Tottenham N, Liston C, Durston S 2005. Imaging the developing brain: What have we learned about cognitive development?. Trends Cogn. Sci. 9:104–10
    [Google Scholar]
  32. CDC (Cent. Dis. Control Prev.). 2018. Child abuse and neglect: risk and protective factors. Cent. Dis. Control Prev https://www.cdc.gov/violenceprevention/childabuseandneglect/riskprotectivefactors.html
    [Google Scholar]
  33. Champagne FA, Francis DD, Mar A, Meaney MJ 2003. Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol. Behav. 79:359–71
    [Google Scholar]
  34. Clancy B, Finlay BL, Darlington RB, Anand KJS 2007a. Extrapolating brain development from experimental species to humans. Neurotoxicology 28:931–37
    [Google Scholar]
  35. Clancy B, Kersh B, Hyde J, Darlington RB, Anand K, Finlay BL 2007b. Web-based method for translating neurodevelopment from laboratory species to humans. Neuroinformatics 5:79–94
    [Google Scholar]
  36. Collier AC, Bolles RC 1980. The ontogenesis of defensive reactions to shock in preweanling rats. Dev. Psychobiol. 13:141–50
    [Google Scholar]
  37. Cunningham MG, Bhattacharyya S, Benes FM 2002. Amygdalo–cortical sprouting continues into early adulthood: implications for the development of normal and abnormal function during adolescence. J. Comp. Neurol. 453:116–30
    [Google Scholar]
  38. Dallman MF 2000. Moments in time—the neonatal rat hypothalamo–pituitary–adrenal axis. Endocrinology 141:1590–92
    [Google Scholar]
  39. Danielewicz J, Hess G 2014. Early life stress alters synaptic modification range in the rat lateral amygdala. Behav. Brain Res. 265:32–37
    [Google Scholar]
  40. De Shetler NG, Rissman J 2017. Dissociable profiles of generalization/discrimination in the human hippocampus during associative retrieval. Hippocampus 27:115–21
    [Google Scholar]
  41. DiPietro JA 2012. Maternal stress in pregnancy: considerations for fetal development. J. Adolesc. Health 51:Suppl.S3–8
    [Google Scholar]
  42. Eisenberg N, Cumberland A, Spinrad TL 1998. Parental socialization of emotion. Psychol. Inq. 9:241–47
    [Google Scholar]
  43. Feldman R, Singer M, Zagoory O 2010. Touch attenuates infants’ physiological reactivity to stress. Dev. Sci. 13:271–78
    [Google Scholar]
  44. Gabard-Durnam LJ, Flannery J, Goff B, Gee DG, Humphreys KL et al. 2014. The development of human amygdala functional connectivity at rest from 4 to 23 years: a cross-sectional study. Neuroimage 95:193–207
    [Google Scholar]
  45. Gabard-Durnam LJ, Gee DG, Goff B, Flannery J, Telzer E et al. 2016. Stimulus-elicited connectivity influences resting-state connectivity years later in human development: a prospective study. J. Neurosci. 36:4771–84
    [Google Scholar]
  46. Gao Y, Raine A, Venables PH, Dawson ME, Mednick SA 2010. The development of skin conductance fear conditioning in children from ages 3 to 8 years. Dev. Sci. 13:201–12
    [Google Scholar]
  47. Gee DG, Gabard-Durnam LJ, Flannery J, Goff B, Humphreys KL et al. 2013a. Early developmental emergence of human amygdala–prefrontal connectivity after maternal deprivation. PNAS 110:15638–43
    [Google Scholar]
  48. Gee DG, Gabard-Durnam LJ, Telzer EH, Humphreys KL, Goff B et al. 2014. Maternal buffering of human amygdala–prefrontal circuitry during childhood but not during adolescence. Psychol. Sci. 25:2067–78
    [Google Scholar]
  49. Gee DG, Humphreys KL, Flannery J, Goff B, Telzer EH et al. 2013b. A developmental shift from positive to negative connectivity in human amygdala–prefrontal circuitry. J. Neurosci. 33:4584–93
    [Google Scholar]
  50. Giedd JN 2004. Structural magnetic resonance imaging of the adolescent brain. Ann. N. Y. Acad. Sci. 1021:77–85
    [Google Scholar]
  51. Giedd JN, Blumenthal J, Jeffries NO, Castellanos FX, Liu H et al. 1999. Brain development during childhood and adolescence: a longitudinal MRI study. Nat. Neurosci. 2:861–63
    [Google Scholar]
  52. Glenn CR, Klein DN, Lissek S, Britton JC, Pine DS, Hajcak G 2012. The development of fear learning and generalization in 8–13 year-olds. Dev. Psychobiol. 54:675–84
    [Google Scholar]
  53. Gogtay N, Giedd JN, Lusk L, Hayashi KM, Greenstein D et al. 2004. Dynamic mapping of human cortical development during childhood through early adulthood. PNAS 101:8174–79
    [Google Scholar]
  54. Graham AM, Buss C, Rasmussen JM, Rudolph MD, Demeter DV et al. 2016. Implications of newborn amygdala connectivity for fear and cognitive development at 6-months-of-age. Dev. Cogn. Neurosci. 18:12–25
    [Google Scholar]
  55. Graham AM, Fisher PA, Pfeifer JH 2013. What sleeping babies hear: a functional MRI study of interparental conflict and infants’ emotion processing. Psychol. Sci. 24:782–89
    [Google Scholar]
  56. Graham AM, Pfeifer JH, Fisher PA, Carpenter S, Fair DA 2015. Early life stress is associated with default system integrity and emotionality during infancy. J. Child Psychol. Psychiatry 56:1212–22
    [Google Scholar]
  57. Green JG, McLaughlin KA, Berglund PA, Gruber MJ, Sampson NA et al. 2010. Childhood adversities and adult psychiatric disorders in the National Comorbidity Survey Replication (NCS-R) I: associations with first onset of DSM-IV disorders. Arch. Gen. Psychiatry 67:113–23
    [Google Scholar]
  58. Gunnar MR, Hostinar CE, Sanchez MM, Tottenham N, Sullivan RM 2015. Parental buffering of fear and stress neurobiology: reviewing parallels across rodent, monkey, and human models. Soc. Neurosci. 10:474–78
    [Google Scholar]
  59. Haroutunian V, Campbell BA 1979. Emergence of interoceptive and exteroceptive control of behavior in rats. Science 205:927–29
    [Google Scholar]
  60. Havighurst RJ 1948. Developmental Tasks and Education Chicago: Chicago Univ. Press
    [Google Scholar]
  61. Hennessy MB, Hornschuh G, Kaiser S, Sachser N 2006. Cortisol responses and social buffering: a study throughout the life span. Horm. Behav. 49:383–90
    [Google Scholar]
  62. Hennessy MB, Schiml PA, Willen R, Watanasriyakul W, Johnson J, Garrett T 2015. Selective social buffering of behavioral and endocrine responses and Fos induction in the prelimbic cortex of infants exposed to a novel environment. Dev. Psychobiol. 57:50–62
    [Google Scholar]
  63. Hostinar CE, Johnson AE, Gunnar MR 2015a. Parent support is less effective in buffering cortisol stress reactivity for adolescents compared to children. Dev. Sci. 18:281–97
    [Google Scholar]
  64. Hostinar CE, Johnson AE, Gunnar MR 2015b. Early social deprivation and the social buffering of cortisol stress responses in late childhood: an experimental study. Dev. Psychol. 51:1597–1609
    [Google Scholar]
  65. Hunt PS, Richardson R, Campbell BA 1994. Delayed development of fear-potentiated startle in rats. Behav. Neurosci. 108:69–80
    [Google Scholar]
  66. Huot RL, Thrivikraman K, Meaney MJ, Plotsky PM 2001. Development of adult ethanol preference and anxiety as a consequence of neonatal maternal separation in Long Evans rats and reversal with antidepressant treatment. Psychopharmacology 158:366–73
    [Google Scholar]
  67. Johnson DC, Casey BJ 2015a. Easy to remember, difficult to forget: the development of fear regulation. Dev. Cogn. Neurosci. 11:42–55
    [Google Scholar]
  68. Johnson DC, Casey BJ 2015b. Extinction during memory reconsolidation blocks recovery of fear in adolescents. Sci. Rep. 5:8863
    [Google Scholar]
  69. Jovanovic T, Nylocks KM, Gamwell KL, Smith A, Davis TA et al. 2014. Development of fear acquisition and extinction in children: effects of age and anxiety. Neurobiol. Learn. Mem. 113:135–42
    [Google Scholar]
  70. Karmiloff-Smith A 2009. Nativism versus neuroconstructivism: rethinking the study of developmental disorders. Dev. Psychol. 45:56–63
    [Google Scholar]
  71. Kessler RC, Berglund P, Demler O, Jin R, Merikangas KR, Walters EE 2005. Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Arch. Gen. Psychiatry 62:593–602
    [Google Scholar]
  72. Kessler RC, Greenberg PE 2002. The economic burden of anxiety and stress disorders. Neuropsychopharmacology 67:982–92
    [Google Scholar]
  73. Kikusui T, Winslow JT, Mori Y 2006. Social buffering: relief from stress and anxiety. Philos. Trans. R. Soc. B 361:2215–28
    [Google Scholar]
  74. Kim JH, Hamlin AS, Richardson R 2009. Fear extinction across development: the involvement of the medial prefrontal cortex as assessed by temporary inactivation and immunohistochemistry. J. Neurosci. 29:10802–8
    [Google Scholar]
  75. Kim JH, Li S, Richardson R 2011. Immunohistochemical analyses of long-term extinction of conditioned fear in adolescent rats. Cereb. Cortex 21:530–38
    [Google Scholar]
  76. Koppensteiner P, Aizawa S, Yamada D, Kabuta T, Boehm S et al. 2014. Age-dependent sensitivity to glucocorticoids in the developing mouse basolateral nucleus of the amygdala. Psychoneuroendocrinology 46:64–77
    [Google Scholar]
  77. Lambert HK, Sheridan MA, Sambrook KA, Rosen ML, Askren MK, McLaughlin KA 2017. Hippocampal contribution to context encoding across development is disrupted following early-life adversity. J. Neurosci. 37:1925–34
    [Google Scholar]
  78. Landers MS, Sullivan RM 2012. The development and neurobiology of infant attachment and fear. Dev. Neurosci. 34:101–14
    [Google Scholar]
  79. LeDoux JE 2000. Emotion circuits in the brain. Annu. Rev. Neurosci. 23:155–84
    [Google Scholar]
  80. Leonardo ED, Hen R 2008. Anxiety as a developmental disorder. Neuropsychopharmacology 33:134–40
    [Google Scholar]
  81. Li S, Kim J, Richardson R 2012. Updating memories: changing the involvement of the prelimbic cortex in the expression of an infant fear memory. Neuroscience 222:316–25
    [Google Scholar]
  82. Lupien SJ, Parent S, Evans AC, Tremblay RE, Zelazo PD et al. 2011. Larger amygdala but no change in hippocampal volume in 10-year-old children exposed to maternal depressive symptomatology since birth. PNAS 108:14324–29
    [Google Scholar]
  83. Marco EM, Valero M, de la Serna O, Aisa B, Borcel E et al. 2012. Maternal deprivation effects on brain plasticity and recognition memory in adolescent male and female rats. Neuropharmacology 68:223–31
    [Google Scholar]
  84. Matthews K, Robbins TW 2003. Early experience as a determinant of adult behavioural responses to reward: the effects of repeated maternal separation in the rat. Neurosci. Biobehav. Rev. 27:45–55
    [Google Scholar]
  85. McCallum J, Kim JH, Richardson R 2010. Impaired extinction retention in adolescent rats: effects of d-cycloserine. Neuropsychopharmacology 35:2134–42
    [Google Scholar]
  86. McLaughlin KA, Green JG, Gruber MJ, Sampson NA, Zaslavsky AM, Kessler RC 2012. Childhood adversities and first onset of psychiatric disorders in a national sample of US adolescents. Arch. Gen. Psychiatry 69:1151–60
    [Google Scholar]
  87. McLaughlin KA, Sheridan MA, Gold AL, Duys A, Lambert HK et al. 2016. Maltreatment exposure, brain structure, and fear conditioning in children and adolescents. Neuropsychopharmacology 41:1956–64
    [Google Scholar]
  88. McNally RJ 2007. Mechanisms of exposure therapy: how neuroscience can improve psychological treatments for anxiety disorders. Clin. Psychol. Rev. 27:750–59
    [Google Scholar]
  89. Michalska KJ, Shechner T, Hong M, Britton JC, Leibenluft E et al. 2016. A developmental analysis of threat/safety learning and extinction recall during middle childhood. J. Exp. Child Psychol. 146:95–105
    [Google Scholar]
  90. Mineka S, Zinbarg R 2006. A contemporary learning theory perspective on the etiology of anxiety disorders: It's not what you thought it was. Am. Psychol. 61:10–26
    [Google Scholar]
  91. Monk CS, Grillon C, Baas JMP, McClure EB, Nelson EE et al. 2003. A neuroimaging method for the study of threat in adolescents. Dev. Psychobiol. 43:359–66
    [Google Scholar]
  92. Moriceau S, Shionoya K, Jakubs K, Sullivan RM 2009. Early-life stress disrupts attachment learning: the role of amygdala corticosterone, locus ceruleus corticotropin releasing hormone, and olfactory bulb norepinephrine. J. Neurosci. 29:15745–55
    [Google Scholar]
  93. Moriceau S, Sullivan RM 2006. Maternal presence serves as a switch between learning fear and attraction in infancy. Nat. Neurosci. 9:1004–6
    [Google Scholar]
  94. Moriceau S, Wilson DA, Levine S, Sullivan RM 2006. Dual circuitry for odor–shock conditioning during infancy: corticosterone switches between fear and attraction via amygdala. J. Neurosci. 26:6737–48
    [Google Scholar]
  95. Myers KM, Davis M 2007. Mechanisms of fear extinction. Mol. Psychiatry 12:120–50
    [Google Scholar]
  96. Nachmias M, Gunnar M, Mangelsdorf S, Parritz RH, Buss K 1996. Behavioral inhibition and stress reactivity: the moderating role of attachment security. Child Dev 67:508–22
    [Google Scholar]
  97. Opendak M, Sullivan RM 2016. Unique neurobiology during the sensitive period for attachment produces distinctive infant trauma processing. Eur. J. Psychotraumatology 7:31276
    [Google Scholar]
  98. Papousek M, Papousek H 1990. Excessive infant crying and intuitive parental care: buffering support and its failures in parent–infant interaction. Early Child Dev. Care 65:117–26
    [Google Scholar]
  99. Pattwell SS, Bath KG, Casey BJ, Ninan I, Lee FS 2011. Selective early-acquired fear memories undergo temporary suppression during adolescence. PNAS 108:1182–87
    [Google Scholar]
  100. Pattwell SS, Duhoux S, Hartley CA, Johnson DC, Jing D et al. 2012. Altered fear learning across development in both mouse and human. PNAS 109:16318–23
    [Google Scholar]
  101. Pattwell SS, Liston C, Jing D, Ninan I, Yang RR et al. 2016. Dynamic changes in neural circuitry during adolescence are associated with persistent attenuation of fear memories. Nat. Commun. 7:11475
    [Google Scholar]
  102. Perlman SB, Pelphrey KA 2011. Developing connections for affective regulation: age-related changes in emotional brain connectivity. J. Exp. Child Psychol. 108:607–20
    [Google Scholar]
  103. Perry RE, Al Aïn S, Raineki C, Sullivan RM, Wilson DA 2016. Development of odor hedonics: experience-dependent ontogeny of circuits supporting maternal and predator odor responses in rats. J. Neurosci. 36:6634–50
    [Google Scholar]
  104. Perry RE, Finegood ED, Braren SH, Dejoseph ML, Putrino DF et al. 2018. Developing a neurobehavioral animal model of poverty: Drawing cross-species connections between environments of scarcity-adversity, parenting quality, and infant outcome. Dev. Psychopathol. In press. https://doi.org/10.1017/S095457941800007X
    [Crossref] [Google Scholar]
  105. Perry RE, Sullivan RM 2014. Neurobiology of attachment to an abusive caregiver: short-term benefits and long-term costs. Dev. Psychobiol. 56:1626–34
    [Google Scholar]
  106. Phelps EA, Delgado MR, Nearing KI, LeDoux JE 2004. Extinction learning in humans: role of the amygdala and vmPFC. Neuron 43:897–905
    [Google Scholar]
  107. Pugh CR, Tremblay D, Fleshner M, Rudy JW 1997. A selective role for corticosterone in contextual-fear conditioning. Behav. Neurosci. 111:503–11
    [Google Scholar]
  108. Qiu A, Anh TT, Li Y, Chen H, Rifkin-Graboi A et al. 2015. Prenatal maternal depression alters amygdala functional connectivity in 6-month-old infants. Transl. Psychiatry 5:e508
    [Google Scholar]
  109. Quirk GJ, Mueller D 2008. Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 33:56–72
    [Google Scholar]
  110. Raineki C, Cortés MR, Belnoue L, Sullivan RM 2012. Effects of early-life abuse differ across development: Infant social behavior deficits are followed by adolescent depressive-like behaviors mediated by the amygdala. J. Neurosci. 32:7758–65
    [Google Scholar]
  111. Raineki C, Holman PJ, Debiec J, Bugg M, Beasley A, Sullivan RM 2010a. Functional emergence of the hippocampus in context fear learning in infant rats. Hippocampus 20:1037–46
    [Google Scholar]
  112. Raineki C, Moriceau S, Sullivan RM 2010b. Developing a neurobehavioral animal model of infant attachment to an abusive caregiver. Biol. Psychiatry 67:1137–45
    [Google Scholar]
  113. Raineki C, Shinoya K, Sander K, Sullivan RM 2009. Ontogeny of odor-LiCl vs. odor-shock learning: similar behaviors but divergent ages of functional amygdala emergency. Learn. Mem. 16:114–21
    [Google Scholar]
  114. Repacholi BM, Meltzoff AN 2007. Emotional eavesdropping: Infants selectively respond to indirect emotional signals. Child Dev 78:503–21
    [Google Scholar]
  115. Robinson-Drummer PA, Stanton ME 2015. Using the context preexposure facilitation effect to study long-term context memory in preweanling, juvenile, adolescent, and adult rats. Physiol. Behav. 148:22–28
    [Google Scholar]
  116. Roth TL, Sullivan RM 2005. Memory of early maltreatment: neonatal behavioral and neural correlates of maternal maltreatment within the context of classical conditioning. Biol. Psychiatry 57:823–31
    [Google Scholar]
  117. Rudy JW, Morledge P 1994. Ontogeny of contextual fear conditioning in rats: implications for consolidation, infantile amnesia, and hippocampal system function. Behav. Neurosci. 108:227–34
    [Google Scholar]
  118. Schaffer HR, Greenwood A, Parry MH 1972. The onset of wariness. Child Dev 43:165–75
    [Google Scholar]
  119. Schlund MW, Siegle GJ, Ladouceur CD, Silk JS, Cataldo MF et al. 2010. Nothing to fear? Neural systems supporting avoidance behavior in healthy youths. Neuroimage 52:710–19
    [Google Scholar]
  120. Seltzer LJ, Prososki AR, Ziegler TE, Pollak SD 2012. Instant messages versus speech: hormones and why we still need to hear each other. Evol. Hum. Behav. 33:42–45
    [Google Scholar]
  121. Silvers JA, Insel C, Powers A, Franz P, Helion C et al. 2016a. vlPFC–vmPFC–amygdala interactions underlie age-related differences in cognitive regulation of emotion. Cereb. Cortex 27:3502–14
    [Google Scholar]
  122. Silvers JA, Lumian DS, Gabard-Durnam L, Gee DG, Goff B et al. 2016b. Previous institutionalization is followed by broader amygdala–hippocampal–PFC network connectivity during aversive learning in human development. J. Neurosci. 36:6420–30
    [Google Scholar]
  123. Smotherman WP 1982. Odor aversion learning by the rat fetus. Physiol. Behav. 29:769–71
    [Google Scholar]
  124. Spangler G, Schieche M 1998. Emotional and adrenocortical responses of infants to the strange situation: the differential function of emotional expression. Int. J. Behav. Dev. 22:681–706
    [Google Scholar]
  125. Spear LP 2000. The adolescent brain and age-related behavioral manifestations. Neurosci. Biobehav. Rev. 24:417–63
    [Google Scholar]
  126. Stanton ME, Levine S 1990. Inhibition of infant glucocorticoid stress response: specific role of maternal cues. Dev. Psychobiol. 23:411–26
    [Google Scholar]
  127. Stanton ME, Wallstrom J, Levine S 1987. Maternal contact inhibits pituitary–adrenal stress responses in preweanling rats. Dev. Psychobiol. 20:131–45
    [Google Scholar]
  128. Suchecki D, Rosenfeld P, Levine S 1993. Maternal regulation of the hypothalamic–pituitary–adrenal axis in the infant rat: the roles of feeding and stroking. Brain Res. Dev. Brain Res. 75:185–92
    [Google Scholar]
  129. Sullivan RM, Holman PJ 2010. Transitions in sensitive period attachment learning in infancy: the role of corticosterone. Neurosci. Biobehav. Rev. 34:835–44
    [Google Scholar]
  130. Sullivan RM, Landers M, Yeaman B, Wilson DA 2000. Good memories of bad events in infancy. Nature 407:38–39
    [Google Scholar]
  131. Sullivan RM, Wilson DA, Wong R, Correa A, Leon M 1990. Modified behavioral and olfactory bulb responses to maternal odors in preweanling rats. Brain Res. Dev. Brain Res. 53:243–47
    [Google Scholar]
  132. Swartz JR, Carrasco M, Wiggins JL, Thomason ME, Monk CS 2014. Age-related changes in the structure and function of prefrontal cortex–amygdala circuitry in children and adolescents: a multi-modal imaging approach. Neuroimage 86:212–20
    [Google Scholar]
  133. Thijssen S, Muetzel RL, Bakermans-Kranenburg MJ, Jaddoe VW, Tiemeier H et al. 2017. Insensitive parenting may accelerate the development of the amygdala–medial prefrontal cortex circuit. Dev. Psychopathol. 29:505–18
    [Google Scholar]
  134. Thompson BL, Levitt P 2010. The clinical–basic interface in defining pathogenesis in disorders of neurodevelopmental origin. Neuron 67:702–12
    [Google Scholar]
  135. Tottenham N 2012. Human amygdala development in the absence of species-expected caregiving. Dev. Psychobiol. 54:598–611
    [Google Scholar]
  136. Tottenham N, Hare TA, Quinn BT, McCarry TW, Nurse M et al. 2010. Prolonged institutional rearing is associated with atypically large amygdala volume and difficulties in emotion regulation. Dev. Sci. 13:46–61
    [Google Scholar]
  137. Uematsu A, Matsui M, Tanaka C, Takahashi T, Noguchi K et al. 2012. Developmental trajectories of amygdala and hippocampus from infancy to early adulthood in healthy individuals. PLOS ONE 7:e46970
    [Google Scholar]
  138. Upton KJ, Sullivan RM 2010. Defining age limits of the sensitive period for attachment learning in rat pups. Dev. Psychobiol. 52:453–64
    [Google Scholar]
  139. van Oers HJ, de Kloet ER, Levine S 1998. Early versus late maternal deprivation differentially alters the endocrine and hypothalamic responses to stress. Dev. Brain Res. 111:245–52
    [Google Scholar]
  140. Walker CD, Bath KG, Joels M, Korosi A, Larauche M et al. 2017. Chronic early life stress induced by limited bedding and nesting (LBN) material in rodents: critical considerations of methodology, outcomes and translational potential. Stress 20:421–48
    [Google Scholar]
  141. Wickens DD, Wickens CL 1940. A study of conditioning in the neonate. J. Exp. Psychol. 26:94–102
    [Google Scholar]
  142. Wilson A, Brooks DC, Bouton ME 1995. The role of the rat hippocampal system in several effects of context in extinction. Behav. Neurosci. 109:828–36
    [Google Scholar]
  143. Winnicott DW 1960. The theory of the parent–infant relationship. Int. J. Psychoanal. 41:585–95
    [Google Scholar]
  144. Woodward LJ, Fergusson DM 2001. Life course outcomes of young people with anxiety disorders in adolescence. J. Am. Acad. Child Adolesc. Psychiatry 40:1086–93
    [Google Scholar]
  145. Yap CS, Richardson R 2007. Extinction in the developing rat: an examination of renewal effects. Dev. Psychobiol. 49:565–75
    [Google Scholar]
  146. Young ES, Griskevicius V, Simpson JA, Waters TEA, Mittal C 2018. Can an unpredictable childhood environment enhance working memory? Testing the sensitized-specialization hypothesis. J. Personal. Soc. Psychol. 114:891–908
    [Google Scholar]
  147. Yurgelun-Todd DA, Killgore WD 2006. Fear-related activity in the prefrontal cortex increases with age during adolescence: a preliminary fMRI study. Neurosci. Lett. 406:194–99
    [Google Scholar]
/content/journals/10.1146/annurev-clinpsy-050718-095727
Loading
/content/journals/10.1146/annurev-clinpsy-050718-095727
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error