Early-life stress has persistent effects on amygdala function and development in mice and humans

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 45, 2013, Pages 18274-18278

  Cohen, Matthew Malter ^a   Jing, Deqiang ^a   Yang, Rui R ^a   Tottenham, Nim ^a,b   Lee, Francis S ^a   Casey, B J ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Anxiety; C fos; Cross species; Emotion regulation; Infralimbic cortex

Indexed keywords

ANTIDEPRESSANT AGENT; BENZODIAZEPINE; PROTEIN C FOS;

ADOPTION; AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY DISORDER; ARTICLE; ATTENTION; BASOLATERAL AMYGDALA; BOLD SIGNAL; BRAIN DEPTH STIMULATION; BRAIN DEVELOPMENT; BRAIN FUNCTION; CAGE; CAREGIVER; CHILD; CHILD BEHAVIOR; CLINICAL ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EARLY INTERVENTION; EARLY LIFE STRESS; EMOTIONALITY; FACIAL EXPRESSION; FEAR; FEMALE; HIPPOCAMPAL CA1 REGION; HUMAN; INFRALIMBIC CORTEX; LIMBIC CORTEX; MALE; MATERNAL CARE; MOUSE; NERVE CELL; NONHUMAN; ORPHANAGE; PARAVENTRICULAR THALAMIC NUCLEUS; PERINATAL PERIOD; PERSONAL EXPERIENCE; PRESCHOOL CHILD; PRIORITY JOURNAL; REARING; RISK; THREAT; VENTROMEDIAL PREFRONTAL CORTEX;

ANXIETY; C-FOS; CROSS-SPECIES; EMOTION REGULATION; INFRALIMBIC CORTEX;

AGE FACTORS; AMYGDALA; ANIMALS; CHILD; EMOTIONS; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C57BL; PARENT-CHILD RELATIONS; STRESS, PSYCHOLOGICAL;

EID: 84887312427     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1310163110     Document Type: Article

References (51)

1. Merikangas KR, et al. (2010) Prevalence and treatment of mental disorders among US children in the 2001-2004 NHANES. Pediatrics 125(1):75-81.
2. Green JG, et al. (2010) Childhood adversities and adult psychiatric disorders in the national comorbidity survey replication I: Associations with first onset of DSM-IV disorders. Arch Gen Psychiatry 67(2):113-123.
3. Juffer F, van Ijzendoorn MH (2005) Behavior problems and mental health referrals of international adoptees: A meta-analysis. JAMA 293(20):2501-2515.
4. Pechtel P, Pizzagalli DA (2011) Effects of early life stress on cognitive and affective function: An integrated review of human literature. Psychopharmacology (Berl) 214(1):55-70.
5. Shonkoff JP, Garner AS; Committee on Psychosocial Aspects of Child and Family Health; Committee on Early Childhood, Adoption, and Dependent Care; Section on Developmental and Behavioral Pediatrics (2012) The lifelong effects of early childhood adversity and toxic stress. Pediatrics 129(1):e232-e246.
6. Shonkoff JP, Boyce WT, McEwen BS (2009) Neuroscience, molecular biology, and the childhood roots of health disparities: Building a new framework for health promotion and disease prevention. JAMA 301(21):2252-2259.
7. Tottenham N, et al. (2010) Prolonged institutional rearing is associated with atypically large amygdala volume and difficulties in emotion regulation. Dev Sci 13(1):46-61.
8. Tottenham N, et al. (2011) Elevated amygdala response to faces following early deprivation. Dev Sci 14(2):190-204.
9. Mehta MA, et al. (2009) Amygdala, hippocampal and corpus callosum size following severe early institutional deprivation: The English and Romanian Adoptees study pilot. J Child Psychol Psychiatry 50(8):943-951.
10. Kumsta R, et al. (2010) Deprivation-specific psychological patterns. Monogr Soc Res Child Dev 75(1):48-78.
11. Kreppner J, et al. (2010) IV. Developmental course of deprivation-specific psychological patterns: Early manifestations, persistence to age 15, and clinical features. Monogr Soc Res Child Dev 75(1):79-101.
12. Tottenham N (2012) Risk and developmental heterogeneity in previously institutionalized children. J Adolesc Health 51(2 Suppl):S29-S33.
13. Rutter M, O'Connor TG; English and Romanian Adoptees (ERA) Study Team (2004) Are there biological programming effects for psychological development? Findings from a study of Romanian adoptees. Dev Psychol 40(1):81-94.
14. Gilles EE, Schultz L, Baram TZ (1996) Abnormal corticosterone regulation in an immature rat model of continuous chronic stress. Pediatr Neurol 15(2):114-119.
15. Rice CJ, Sandman CA, Lenjavi MR, Baram TZ (2008) A novel mouse model for acute and long-lasting consequences of early life stress. Endocrinology 149(10):4892-4900.
16. Liston C, McEwen BS, Casey BJ (2009) Psychosocial stress reversibly disrupts prefrontal processing and attentional control. Proc Natl Acad Sci USA 106(3):912-917.
17. Vyas A, Mitra R, Shankaranarayana Rao BS, Chattarji S (2002) Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J Neurosci 22(15):6810-6818.
18. McEwen BS (2012) Brain on stress: How the social environment gets under the skin. Proc Natl Acad Sci USA 109(Suppl 2):17180-17185.
19. Vyas A, Pillai AG, Chattarji S (2004) Recovery after chronic stress fails to reverse amygdaloid neuronal hypertrophy and enhanced anxiety-like behavior. Neuroscience 128(4):667-673.
20. Millstein RA, Holmes A (2007) Effects of repeated maternal separation on anxiety- and depression-related phenotypes in differentmouse strains. Neurosci Biobehav Rev 31(1):3-17.
21. Stevens HE, Leckman JF, Coplan JD, Suomi SJ (2009) Risk and resilience: Early manipulation of macaque social experience and persistent behavioral and neurophysiological outcomes. J Am Acad Child Adolesc Psychiatry 48(2):114-127.
22. Cui M, et al. (2006) Enriched environment experience overcomes thememory deficits and depressive-like behavior induced by early life stress. Neurosci Lett 404(1-2):208-212.
23. Dalle Molle R, et al. (2012) Associations between parenting behavior and anxiety in a rodent model and a clinical sample: Relationship to peripheral BDNF levels. Transcult Psychiatry 2:e195.
24. Jackowski A, et al. (2011) Early-life stress, corpus callosum development, hippocampal volumetrics, and anxious behavior inmale nonhuman primates. Psychiatry Res 192(1):37-44.
25. 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(22):7758-7765.
26. Gunnar MR, Bruce J, Grotevant HD (2000) International adoption of institutionally reared children: Research and policy. Dev Psychopathol 12(4):677-693.
27. Ivy AS, Brunson KL, Sandman C, Baram TZ (2008) Dysfunctional nurturing behavior in rat dams with limited access to nesting material: A clinically relevant model for earlylife stress. Neuroscience 154(3):1132-1142.
28. Adriani W, Laviola G (2004) Windows of vulnerability to psychopathology and therapeutic strategy in the adolescent rodent model. Behav Pharmacol 15(5-6):341-352.
29. Avishai-Eliner S, Brunson KL, Sandman CA, Baram TZ (2002) Stressed-out, or in (utero)? Trends Neurosci 25(10):518-524.
30. Spear LP (2000) The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24(4):417-463.
31. Brenhouse HC, Andersen SL (2011) Developmental trajectories during adolescence in males and females: A cross-species understanding of underlying brain changes. Neurosci Biobehav Rev 35(8):1687-1703.
32. Hare TA, et al. (2008) Biological substrates of emotional reactivity and regulation in adolescence during an emotional go-nogo task. Biol Psychiatry 63(10):927-934.
33. Dulawa SC, Holick KA, Gundersen B, Hen R (2004) Effects of chronic fluoxetine in animal models of anxiety and depression. Neuropsychopharmacology 29(7):1321-1330.
34. Kolb B, et al. (2012) Experience and the developing prefrontal cortex. Proc Natl Acad Sci USA 109(Suppl 2):17186-17193.
35. Lupien SJ, et al. (2011) Larger amygdala but no change in hippocampal volume in 10- year-old children exposed to maternal depressive symptomatology since birth. Proc Natl Acad Sci USA 108(34):14324-14329.
36. Milad MR, Quirk GJ (2012) Fear extinction as a model for translational neuroscience: Ten years of progress. Annu Rev Psychol 63:129-151.
37. Pattwell SS, et al. (2012) Altered fear learning across development in both mouse and human. Proc Natl Acad Sci USA 109(40):16318-16323.
38. Quirk GJ, Russo GK, Barron JL, Lebron K (2000) The role of ventromedial prefrontal cortex in the recovery of extinguished fear. J Neurosci 20(16):6225-6231.
39. Hamani C, et al. (2010) Antidepressant-like effects of medial prefrontal cortex deep brain stimulation in rats. Biol Psychiatry 67(2):117-124.
40. Knapska E, Maren S (2009) Reciprocal patterns of c-Fos expression in the medial prefrontal cortex and amygdala after extinction and renewal of conditioned fear. Learn Mem 16(8):486-493.
41. Dragunow M, Faull R (1989) The use of c-fos as a metabolic marker in neuronal pathway tracing. J Neurosci Methods 29(3):261-265.
42. Bechtholt AJ, Valentino RJ, Lucki I (2008) Overlapping and distinct brain regions associated with the anxiolytic effects of chlordiazepoxide and chronic fluoxetine. Neuropsychopharmacology 33(9):2117-2130.
43. Morgan JI, Cohen DR, Hempstead JL, Curran T (1987) Mapping patterns of c-fos expression in the central nervous system after seizure. Science 237(4811):192-197.
44. Finlay BL, Darlington RB (1995) Linked regularities in the development and evolution of mammalian brains. Science 268(5217):1578-1584.
45. Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A (2001) Neurophysiological investigation of the basis of the fMRI signal. Nature 412(6843):150-157.
46. Lee JH, et al. (2010) Global and local fMRI signals driven by neurons defined optogenetically by type and wiring. Nature 465(7299):788-792.
47. Gee DG, et al. (2013) A developmental shift from positive to negative connectivity in human amygdala-prefrontal circuitry. J Neurosci 33(10):4584-4593.
48. McLaughlin KA, et al. (2010) Childhood adversities and adult psychiatric disorders in the national comorbidity survey replication II: Associations with persistence of DSM-IV disorders. Arch Gen Psychiatry 67(2):124-132.
49. Rutter M; English and Romanian Adoptees (ERA) Study Team (1998) Developmental catch-up, and deficit, following adoption after severe global early privation. J Child Psychol Psychiatry 39(4):465-476.
50. Sabatini MJ, et al. (2007) Amygdala gene expression correlates of social behavior in monkeys experiencing maternal separation. J Neurosci 27(12):3295-3304.
51. Tottenham N, et al. (2009) The NimStim set of facial expressions: Judgments from untrained research participants. Psychiatry Res 168(3):242-249.