Previous institutionalization is followed by broader amygdala–hippocampal–PFC network connectivity during aversive learning in human development

Journal of Neuroscience

Volumn 36, Issue 24, 2016, Pages 6420-6430

  Silvers, Jennifer A ^a   Lumian, Daniel S ^b   Gabard Durnam, Laurel ^c   Gee, Dylan G ^d   Goff, Bonnie ^a   Fareri, Dominic S ^e   Caldera, Christina ^a   Flannery, Jessica ^f   Telzer, Eva H ^g   Humphreys, Kathryn L ^h   Tottenham, Nim ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF DENVER   (United States)

^c Och Spine at New York Presbyterian Hospitals   (United States)

^d WEILL CORNELL MEDICAL COLLEGE   (United States)

^e UNIVERSITY OF OREGON   (United States)

^f ADELPHI UNIVERSITY   (United States)

^g UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^h STANFORD UNIVERSITY   (United States)

Author keywords

Early life stress; FMRI; Learning; Neurodevelopment; Threat

Indexed keywords

ADOLESCENT; AMYGDALA; ANXIETY; ARTICLE; AVERSIVE BEHAVIOR; BEHAVIORAL SCIENCE; CHILD; CONNECTOME; DISCRIMINATION LEARNING; EARLY LIFE STRESS; ELECTRODERMAL RESPONSE; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HEAD MOVEMENT; HIPPOCAMPUS; HUMAN; HUMAN DEVELOPMENT; INSTITUTIONALIZATION; LEARNING; MAJOR CLINICAL STUDY; MALE; MIDDLE FRONTAL GYRUS; NERVE CELL DIFFERENTIATION; NUCLEAR MAGNETIC RESONANCE IMAGING; PREFRONTAL CORTEX; PRIORITY JOURNAL; QUESTIONNAIRE; REACTION TIME; SCHOOL CHILD; AVOIDANCE BEHAVIOR; BLOOD; BRAIN MAPPING; DIAGNOSTIC IMAGING; IMAGE PROCESSING; LONGITUDINAL STUDY; MENTAL DISEASE; NERVE TRACT; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGICAL RATING SCALE;

OXYGEN;

ADOLESCENT; AMYGDALA; ANXIETY; AVOIDANCE LEARNING; BRAIN MAPPING; CHILD; FEMALE; GALVANIC SKIN RESPONSE; HIPPOCAMPUS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; LONGITUDINAL STUDIES; MAGNETIC RESONANCE IMAGING; MALE; NEURAL PATHWAYS; NEURODEVELOPMENTAL DISORDERS; OXYGEN; PREFRONTAL CORTEX; PSYCHIATRIC STATUS RATING SCALES; REACTION TIME;

EID: 84974839216     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0038-16.2016     Document Type: Article

References (84)

1. Amat J, Baratta MV, Paul E, Bland ST, Watkins LR, Maier SF (2005) Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus. Nat Neurosci 8:365–371.
2. Bagot RC, van Hasselt FN, Champagne DL, Meaney MJ, Krugers HJ, Joëls M (2009) Maternal care determines rapid effects of stress mediators on synaptic plasticity in adult rat hippocampal dentate gyrus. Neurobiol Learn Mem 92:292–300.
3. Besnard A, Sahay A (2016) Adult hippocampal neurogenesis, fear generalization, and stress. Neuropsychopharmacology 41:24–44.
4. Birmaher B, Brent DA, Chiappetta L, Bridge J, Monga S, Baugher M (1999) Psychometric properties of the Screen for Child Anxiety Related Emotional Disorders (SCARED): a replication study. JAmAcad Child Adolesc Psychiatry 38:1230–1236.
5. Blaise JH, Koranda JL, Chow U, Haines KE, Dorward EC (2008) Neonatal isolation stress alters bidirectional long-term synaptic plasticity in amygdalo-hippocampal synapses in freely behaving adult rats. Brain Res 1193:25–33.
6. Bremner JD, Vermetten E, Schmahl C, Vaccarino V, Vythilingam M, Afzal N, Grillon C, Charney DS (2005) Positron emission tomographic imaging of neural correlates of a fear acquisition and extinction paradigm in women with childhood sexual-abuse-related post-traumatic stress disorder. Psychol Med 35:791–806.
7. Britton JC, Grillon C, Lissek S, Norcross MA, Szuhany KL, Chen G, Ernst M, Nelson EE, Leibenluft E, Shechner T, Pine DS (2013) Response to learned threat: an FMRI study in adolescent and adult anxiety. Am J Psychiatry 170:1195–1204.
8. Cain CK, LeDoux JE (2007) Escape from fear: a detailed behavioral analysis of two atypical responses reinforced by CS termination. J Exp Psychol Anim Behav Process 33:451–463.
9. 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.
10. Callaghan BL, Richardson R (2012) Early-life stress affects extinction during critical periods of development: an analysis of the effects of maternal separation on extinction in adolescent rats. Stress 15:671–679.
11. 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 56:1635–1650.
12. Cohen Kadosh K, Haddad AD, Heathcote LC, Murphy RA, Pine DS, Lau JY (2015) High trait anxiety during adolescence interferes with discriminatory context learning. Neurobiol Learn Mem 123:50–57.
13. Collins KA, Mendelsohn A, Cain CK, Schiller D (2014) Taking action in the face of threat: neural synchronization predicts adaptive coping. J Neurosci 34:14733–14738.
14. Corcoran KA, Quirk GJ (2007) Activity in prelimbic cortex is necessary for the expression of learned, but not innate, fears. J Neurosci 27:840–844.
15. Cox RW (1996) AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 29:162–173.
16. Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, Zilles K (2005) A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 25:1325–1335.
17. Etkin A, Wager TD (2007) Functional neuroimaging of anxiety: a metaanalysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. Am J Psychiatry 164:1476–1488.
18. Etkin A, Egner T, Kalisch R (2011) Emotional processing in anterior cingulate and medial prefrontal cortex. Trends Cogn Sci 15:85–93.
19. Friston KJ, Buechel C, Fink GR, Morris J, Rolls E, Dolan RJ (1997) Psychophysiological and modulatory interactions in neuroimaging. Neuroimage 6:218–229.
20. Frodl T, O’Keane V (2013) How does the brain deal with cumulative stress? A review with focus on developmental stress, HPA axis function and hippocampal structure in humans. Neurobiol Dis 52:24–37.
21. Fullana MA, Harrison BJ, Soriano-Mas C, Vervliet B, Cardoner N, Àvila Parcet A, Radua J (2016) Neural signatures of human fear conditioning: an updated and extended meta-analysis of fMRI studies. Mol Psychiatry 21:500–508.
22. Gee DG, Gabard-Durnam LJ, Flannery J, Goff B, Humphreys KL, Telzer EH, Hare TA, Bookheimer SY, Tottenham N (2013) Early developmental emergence of human amygdala-prefrontal connectivity after maternal deprivation. Proc Natl Acad Sci U S A 110:15638–15643.
23. Goosens KA (2011) Hippocampal regulation of aversive memories. Curr Opin Neurobiol 21:460–466.
24. Gorka AX, Hanson JL, Radtke SR, Hariri AR (2014) Reduced hippocampal and medial prefrontal gray matter mediate the association between reported childhood maltreatment and trait anxiety in adulthood and predict sensitivity to future life stress. Biol Mood Anxiety Disord 4:12.
25. Greco JA, Liberzon I (2016) Neuroimaging of fear-associated learning. Neuropsychopharmacology 41:320–334.
26. Huang CC, Chou PH, Yang CH, Hsu KS (2005) Neonatal isolation accelerates the developmental switch in the signalling cascades for long-term potentiation induction. J Physiol 569:789–799.
27. Hulshof HJ, Novati A, Sgoifo A, Luiten PG, den Boer JA, Meerlo P (2011) Maternal separation decreases adult hippocampal cell proliferation and impairs cognitive performance but has little effect on stress sensitivity and anxiety in adult Wistar rats. Behav Brain Res 216:552–560.
28. Humphreys KL, Gleason MM, Drury SS, Miron D, Nelson CA 3rd, Fox NA, Zeanah CH (2015) Effects of institutional rearing and foster care on psychopathology at age 12 years in Romania: follow-up of an open, randomised controlled trial. Lancet Psychiatry 2:625–634.
29. Indovina I, Robbins TW, Núñez-Elizalde AO, Dunn BD, Bishop SJ (2011) Fear-conditioning mechanisms associated with trait vulnerability to anxiety in humans. Neuron 69:563–571.
30. Jackowski A, Perera TD, Abdallah CG, Garrido G, Tang CY, Martinez J, Mathew SJ, Gorman JM, Rosenblum LA, Smith EL, Dwork AJ, Shungu DC, Kaffman A, Gelernter J, Coplan JD, Kaufman J (2011) Early-life stress, corpus callosum development, hippocampal volumetrics, and anxious behavior in male nonhuman primates. Psychiatry Res 192:37–44.
31. Jacobson L, Sapolsky R (1991) The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis. Endocr Rev 12:118–134.
32. Jovanovic T, Nylocks KM, Gamwell KL, Smith A, Davis TA, Norrholm SD, Bradley B (2014) Development of fear acquisition and extinction in children: effects of age and anxiety. Neurobiol Learn Mem 113:135–142.
33. Kerr DL, McLaren DG, Mathy RM, Nitschke JB (2012) Controllability modulates the anticipatory response in the human ventromedial prefrontal cortex. Front Psychol 3:557.
34. Kessler RC, McLaughlin KA, Green JG, Gruber MJ, Sampson NA, Zaslavsky AM, Aguilar-Gaxiola S, Alhamzawi AO, Alonso J, Angermeyer M, Benjet C, Bromet E, Chatterji S, de Girolamo G, Demyttenaere K, Fayyad J, Florescu S, Gal G, Gureje O, Haro JM, et al. (2010) Childhood adversities and adult psychopathology in the WHO World Mental Health Surveys. Br J Psychiatry 197:378–385.
35. Kheirbek MA, Klemenhagen KC, Sahay A, Hen R (2012) Neurogenesis and generalization: a new approach to stratify and treat anxiety disorders. Nat Neurosci 15:1613–1620.
36. Kim JH, Li S, Hamlin AS, McNally GP, Richardson R (2012) Phosphorylation of mitogen-activated protein kinase in the medial prefrontal cortex and the amygdala following memory retrieval or forgetting in developing rats. Neurobiol Learn Mem 97:59–68.
37. Knight DC, Wood KH (2011) Investigating the neural mechanisms of aware and unaware fear memory with fMRI. J Vis Exp (56):e3083.
38. Knight DC, Waters NS, Bandettini PA (2009) Neural substrates of explicit and implicit fear memory. Neuroimage 45:208–214.
39. Korzus E (2015) Prefrontal cortex in learning to overcome generalized fear. J Exp Neurosci 9:53–56.
40. LeDoux JE, Cicchetti P, Xagoraris A, Romanski LM (1990) The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning. J Neurosci 10:1062–1069.
41. Li S, Kim JH, Richardson R (2012) Differential involvement of the medial prefrontal cortex in the expression of learned fear across development. Behav Neurosci 126:217–225.
42. Lissek S, Powers AS, McClure EB, Phelps EA, Woldehawariat G, Grillon C, Pine DS (2005) Classical fear conditioning in the anxiety disorders: a meta-analysis. Behav Res Ther 43:1391–1424.
43. Luby J, Belden A, Botteron K, Marrus N, Harms MP, Babb C, Nishino T, Barch D (2013) The effects of poverty on childhood brain development: the mediating effect of caregiving and stressful life events. JAMA Pediatr 167:1135–1142.
44. Malter Cohen M, Jing D, Yang RR, Tottenham N, Lee FS, Casey BJ (2013) Early-life stress has persistent effects on amygdala function and development in mice and humans. Proc Natl Acad Sci U S A 110:18274–18278.
45. Maren S, Phan KL, Liberzon I (2013) The contextual brain: implications for fear conditioning, extinction and psychopathology. Nat Rev Neurosci 14:417–428.
46. McAllister WR, McAllister DE (1962) Postconditioning delay and intensity of shock as factors in the measurement of acquired fear. J Exp Psychol 64:110–116.
47. McEwen BS, Nasca C, Gray JD (2016) Stress effects on neuronal structure: hippocampus, amygdala, and prefrontal cortex. Neuropsychopharmacology 41:3–23.
48. Mehta MA, Golembo NI, Nosarti C, Colvert E, Mota A, Williams SC, Rutter M, Sonuga-Barke EJ (2009) Amygdala, hippocampal and corpus callosum size following severe early institutional deprivation: the English and Romanian Adoptees study pilot. J Child Psychol Psychiatry 50:943–951.
49. Milad MR, Wright CI, Orr SP, Pitman RK, Quirk GJ, Rauch SL (2007) Recall of fear extinction in humans activates the ventromedial prefrontal cortex and hippocampus in concert. Biol Psychiatry 62:446–454.
50. Mineka S, Oehlberg K (2008) The relevance of recent developments in classical conditioning to understanding the etiology and maintenance of anxiety disorders. Acta Psychol 127:567–580.
51. Mirescu C, Peters JD, Gould E (2004) Early life experience alters response of adult neurogenesis to stress. Nat Neurosci 7:841–846.
52. Mobbs D, Hagan CC, Dalgleish T, Silston B, Prévost C (2015) The ecology of human fear: survival optimization and the nervous system. Front Neurosci 9:55.
53. Morgan MA, Romanski LM, LeDoux JE (1993) Extinction of emotional learning: contribution of medial prefrontal cortex. Neurosci Lett 163: 109–113.
54. Moriceau S, Sullivan RM (2006) Maternal presence serves as a switch between learning fear and attraction in infancy. Nat Neurosci 9:1004–1006.
55. Mowrer OH, Lamoreaux RR (1946) Fear as an intervening variable in avoidance conditioning. J Comp Psychol 39:29–50.
56. Muhammad A, Carroll C, Kolb B (2012) Stress during development alters dendritic morphology in the nucleus accumbens and prefrontal cortex. Neuroscience 216:103–109.
57. Neumann DL, Waters AM, Westbury HR, Henry J (2008) The use of an unpleasant sound unconditional stimulus in an aversive conditioning procedure with 8- to 11-year-old children. Biol Psychol 79:337–342.
58. Ono M, Kikusui T, Sasaki N, Ichikawa M, Mori Y, Murakami-Murofushi K (2008) Early weaning induces anxiety and precocious myelination in the anterior part of the basolateral amygdala of male BALB/c mice. Neuroscience 156:1103–1110.
59. Oomen CA, Soeters H, Audureau N, Vermunt L, van Hasselt FN, Manders EM, Joëls M, Lucassen PJ, Krugers H (2010) Severe early life stress hampers spatial learning and neurogenesis, but improves hippocampal synaptic plasticity and emotional learning under high-stress conditions in adulthood. J Neurosci 30:6635–6645.
60. Pagliaccio D, Luby JL, Bogdan R, Agrawal A, Gaffrey MS, Belden AC, Botteron KN, Harms MP, Barch DM (2014) Stress-system genes and life stress predict cortisol levels and amygdala and hippocampal volumes in children. Neuropsychopharmacology 39:1245–1253.
61. Pattwell SS, Bath KG, Casey BJ, Ninan I, Lee FS (2011) Selective earlyacquired fear memories undergo temporary suppression during adolescence. Proc Natl Acad Sci U S A 108:1182–1187.
62. Pattwell SS, Duhoux S, Hartley CA, Johnson DC, Jing D, Elliott MD, Ruberry EJ, Powers A, Mehta N, Yang RR, Soliman F, Glatt CE, Casey BJ, Ninan I, Lee FS (2012) Altered fear learning across development in both mouse and human. Proc Natl Acad Sci U S A 109:16318–16323.
63. Penney RK, Kirwin PM (1965) Differential adaptation of anxious and nonanxious children in instrumental escape conditioning. J Exp Psychol 70: 539–541.
64. Preston AR, Eichenbaum H (2013) Interplay of hippocampus and prefrontal cortex in memory. Curr Biol 23:R764–R773.
65. Reichenberg A, Caspi A, Harrington H, Houts R, Keefe RS, Murray RM, Poulton R, Moffitt TE (2010) Static and dynamic cognitive deficits in childhood preceding adult schizophrenia: a 30-year study. Am J Psychiatry 167:160–169.
66. Roceri M, Cirulli F, Pessina C, Peretto P, Racagni G, Riva MA (2004) Postnatal repeated maternal deprivation produces age-dependent changes of brain-derived neurotrophic factor expression in selected rat brain regions. Biol Psychiatry 55:708–714.
67. 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 57:823–831.
68. Schiller D, Levy I, Niv Y, LeDoux JE, Phelps EA (2008) From fear to safety and back: reversal of fear in the human brain. J Neurosci 28:11517–11525.
69. Sehlmeyer C, Schöning S, Zwitserlood P, Pfleiderer B, Kircher T, Arolt V, Konrad C (2009) Human fear conditioning and extinction in neuroimaging: a systematic review. PLoS One 4:e5865.
70. Shors TJ, Seib TB, Levine S, Thompson RF (1989) Inescapable versus escapable shock modulates long-term potentiation in the rat hippocampus. Science 244:224–226.
71. Sierra-Mercado D, Padilla-Coreano N, Quirk GJ (2011) Dissociable roles of prelimbic and infralimbic cortices, ventral hippocampus, and basolateral amygdala in the expression and extinction of conditioned fear. Neuropsychopharmacology 36:529–538.
72. Simon E, Bögels SM (2009) Screening for anxiety disorders in children. Eur Child Adolesc Psychiatry 18:625–634.
73. Somerville LH, Wagner DD, Wig GS, Moran JM, Whalen PJ, Kelley WM (2013) Interactions between transient and sustained neural signals support the generation and regulation of anxious emotion. Cereb Cortex 23:49–60.
74. Sotres-Bayon F, Quirk GJ (2010) Prefrontal control of fear: more than just extinction. Curr Opin Neurobiol 20:231–235.
75. Sotres-Bayon F, Sierra-Mercado D, Pardilla-Delgado E, Quirk GJ (2012) Gating of fear in prelimbic cortex by hippocampal and amygdala inputs. Neuron 76:804–812.
76. Spinelli S, Chefer S, Suomi SJ, Higley JD, Barr CS, Stein E (2009) Early-life stress induces long-term morphologic changes in primate brain. Arch Gen Psychiatry 66:658–665.
77. Squire LR, Stark CE, Clark RE (2004) The medial temporal lobe. Annu Rev Neurosci 27:279–306.
78. Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain. Stuttgart, Germany: Thieme.
79. Torrents-Rodas D, Fullana MA, Bonillo A, Caseras X, Andión O, Torrubia R (2013) No effect of trait anxiety on differential fear conditioning or fear generalization. Biol Psychol 92:185–190.
80. Tottenham N, Hare TA, Quinn BT, McCarry TW, Nurse M, Gilhooly T, Millner A, Galvan A, Davidson MC, Eigsti IM, Thomas KM, Freed PJ, Booma ES, Gunnar MR, Altemus M, Aronson J, Casey BJ (2010) Prolonged institutional rearing is associated with atypically large amygdala volume and difficulties in emotion regulation. Dev Sci 13:46–61.
81. Tottenham N, Hare TA, Millner A, Gilhooly T, Zevin JD, Casey BJ (2011) Elevated amygdala response to faces following early deprivation. Dev Sci 14:190–204.
82. Uchida S, Hara K, Kobayashi A, Funato H, Hobara T, Otsuki K, Yamagata H, McEwen BS, Watanabe Y (2010) Early life stress enhances behavioral vulnerability to stress through the activation of REST4-mediated gene transcription in the medial prefrontal cortex of rodents. J Neurosci 30: 15007–15018.
83. Wager TD, van Ast VA, Hughes BL, Davidson ML, Lindquist MA, Ochsner KN (2009) Brain mediators of cardiovascular responses to social threat, part II: prefrontal-subcortical pathways and relationship with anxiety. Neuroimage 47:836–851.
84. Zeanah CH, Egger HL, Smyke AT, Nelson CA, Fox NA, Marshall PJ, Guthrie D (2009) Institutional rearing and psychiatric disorders in Romanian preschool children. Am J Psychiatry 166:777–785.