Altered fear learning across development in both mouse and human

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

Volumn 109, Issue 40, 2012, Pages 16318-16323

  Pattwell, Siobhan S ^a   Duhoux, Stéphanie ^a   Hartley, Catherine A ^a   Johnson, David C ^a   Jing, Deqiang ^a   Elliott, Mark D ^a   Ruberry, Erika J ^a   Powers, Alisa ^a   Mehta, Natasha ^a   Yang, Rui R ^a   Soliman, Fatima ^a   Glatt, Charles E ^a   Casey, B J ^a   Ninan, Ipe ^b   Lee, Francis S ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN C FOS;

ADOLESCENCE; ADOLESCENT; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; FEAR; HUMAN; LEARNING; MALE; MEMORY CONSOLIDATION; MOLECULAR PROBE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; OUTCOME ASSESSMENT; PARALLEL DESIGN; PREFRONTAL CORTEX; PRIORITY JOURNAL; TREATMENT RESPONSE;

ADOLESCENT; ADULT; ANALYSIS OF VARIANCE; ANIMALS; ANXIETY DISORDERS; CHILD; CONDITIONING (PSYCHOLOGY); EXTINCTION, PSYCHOLOGICAL; FEAR; FEMALE; GALVANIC SKIN RESPONSE; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICROSCOPY, INTERFERENCE; NEURONAL PLASTICITY; PREFRONTAL CORTEX; PROTO-ONCOGENE PROTEINS C-FOS;

MUS;

EID: 84867071678     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1206834109     Document Type: Article

References (56)

1. Rothbaum BO, Davis M (2003) Applying learning principles to the treatment of posttrauma reactions. Ann N Y Acad Sci 1008:112-121. (Pubitemid 38265155)
2. Liberman LC, Lipp OV, Spence SH, March S (2006) Evidence for retarded extinction of aversive learning in anxious children. Behav Res Ther 44:1491-1502. (Pubitemid 44414767)
3. Monk CS, et al. (2003) Adolescent immaturity in attention-related brain engagement to emotional facial expressions. Neuroimage 20:420-428. (Pubitemid 37188530)
4. Kessler RC, et al. (2005) Prevalence and treatment of mental disorders, 1990 to 2003. N Engl J Med 352:2515-2523. (Pubitemid 41007867)
5. Merikangas KR, et al. (2011) Service utilization for lifetime mental disorders in U.S. adolescents: Results of the National Comorbidity Survey-Adolescent Supplement (NCS-A). J Am Acad Child Adolesc Psychiatry 50:32-45.
6. Newman DL, et al. (1996) Psychiatric disorder in a birth cohort of young adults: Prevalence, comorbidity, clinical significance, and new case incidence from ages 11 to 21. J Consult Clin Psychol 64:552-562. (Pubitemid 26230549)
7. Pollack MH, et al. (1996) Relationship of childhood anxiety to adult panic disorder: Correlates and influence on course. Am J Psychiatry 153:376-381. (Pubitemid 26074713)
8. Kim-Cohen J, et al. (2003) Prior juvenile diagnoses in adults with mental disorder: Developmental follow-back of a prospective-longitudinal cohort. Arch Gen Psychiatry 60:709-717. (Pubitemid 36818633)
9. Merikangas KR, et al. (2010) Lifetime prevalence of mental disorders in U.S. adolescents: Results from the National Comorbidity Survey Replication - Adolescent Supplement (NCS-A). J Am Acad Child Adolesc Psychiatry 49:980-989.
10. Keller MB, et al. (1992) Chronic course of anxiety disorders in children and adolescents. J Am Acad Child Adolesc Psychiatry 31:595-599.
11. Lévesque J, et al. (2004) Neural basis of emotional self-regulation in childhood. Neuroscience 129:361-369. (Pubitemid 39388855)
12. Galvan A, et al. (2006) Earlier development of the accumbens relative to orbitofrontal cortex might underlie risk-taking behavior in adolescents. J Neurosci 26:6885-6892. (Pubitemid 44315249)
13. Hare TA, et al. (2008) Biological substrates of emotional reactivity and regulation in adolescence during an emotional go-nogo task. Biol Psychiatry 63:927-934. (Pubitemid 351602274)
14. Casey BJ, et al. (2010) The storm and stress of adolescence: Insights from human imaging and mouse genetics. Dev Psychobiol 52:225-235.
15. Milad MR, Quirk GJ (2012) Fear extinction as a model for translational neuroscience: Ten years of progress. Annu Rev Psychol 63:129-151.
16. Hensch TK (2005) Critical period plasticity in local cortical circuits. Nat Rev Neurosci 6:877-888.
17. Pattwell SS, Bath KG, Casey BJ, Ninan I, Lee FS (2011) Selective early-acquired fear memories undergo temporary suppression during adolescence. Proc Natl Acad Sci USA 108:1182-1187.
18. Soliman F, et al. (2010) A genetic variant BDNF polymorphism alters extinction learning in both mouse and human. Science 327:863-866.
19. Laviola G, Adriani W, Terranova ML, Gerra G (1999) Psychobiological risk factors for vulnerability to psychostimulants in human adolescents and animal models. Neurosci Biobehav Rev 23:993-1010. (Pubitemid 29502404)
20. Adriani W, Chiarotti F, Laviola G (1998) Elevated novelty seeking and peculiar damphetamine sensitization in periadolescent mice compared with adult mice. Behav Neurosci 112:1152-1166. (Pubitemid 28518998)
21. LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23:155-184.
22. Spear LP (2000) The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24:417-463.
23. McCallum J, Kim JH, Richardson R (2010) Impaired extinction retention in adolescent rats: Effects of D-cycloserine. Neuropsychopharmacology 35:2134-2142.
24. Gogolla N, Caroni P, Lüthi A, Herry C (2009) Perineuronal nets protect fear memories from erasure. Science 325:1258-1261.
25. Kim JH, Li S, Richardson R (2011) Immunohistochemical analyses of long-term extinction of conditioned fear in adolescent rats. Cereb Cortex 21:530-538.
26. Lai CS, Franke TF, Gan WB (2012) Opposite effects of fear conditioning and extinction on dendritic spine remodelling. Nature 483:87-91.
27. Gottfried JA, Dolan RJ (2004) Human orbitofrontal cortex mediates extinction learning while accessing conditioned representations of value. Nat Neurosci 7:1144-1152. (Pubitemid 41184456)
28. 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. (Pubitemid 46174503)
29. Milad MR, Vidal-Gonzalez I, Quirk GJ (2004) Electrical stimulation of medial prefrontal cortex reduces conditioned fear in a temporally specific manner. Behav Neurosci 118:389-394. (Pubitemid 38445616)
30. Hefner K, et al. (2008) Impaired fear extinction learning and cortico-amygdala circuit abnormalities in a common genetic mouse strain. J Neurosci 28:8074-8085.
31. Burgos-Robles A, Vidal-Gonzalez I, Quirk GJ (2009) Sustained conditioned responses in prelimbic prefrontal neurons are correlated with fear expression and extinction failure. J Neurosci 29:8474-8482.
32. 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 16:486-493.
33. Santini E, Ge H, Ren K, Peña de Ortiz S, Quirk GJ (2004) Consolidation of fear extinction requires protein synthesis in the medial prefrontal cortex. J Neurosci 24:5704-5710. (Pubitemid 38857224)
34. Santini E, Quirk GJ, Porter JT (2008) Fear conditioning and extinction differentially modify the intrinsic excitability of infralimbic neurons. J Neurosci 28:4028-4036.
35. Spear LP (2004) Adolescent brain development and animal models. Ann N Y Acad Sci 1021:23-26.
36. Rudy JW (1993) Contextual conditioning and auditory cue conditioning dissociate during development. Behav Neurosci 107:887-891.
37. Moriceau S, Sullivan RM (2006) Maternal presence serves as a switch between learning fear and attraction in infancy. Nat Neurosci 9:1004-1006. (Pubitemid 44264911)
38. Kim JH, Richardson R (2008) The effect of temporary amygdala inactivation on extinction and reextinction of fear in the developing rat: Unlearning as a potential mechanism for extinction early in development. J Neurosci 28:1282-1290.
39. Rudy JW, Morledge P (1994) Ontogeny of contextual fear conditioning in rats: Implications for consolidation, infantile amnesia, and hippocampal system function. Behav Neurosci 108:227-234. (Pubitemid 24142684)
40. Hefner K, Holmes A (2007) Ontogeny of fear-, anxiety- and depression-related behavior across adolescence in C57BL/6J mice. Behav Brain Res 176:210-215. (Pubitemid 44880082)
41. Shen H, et al. (2010) A critical role for alpha4betadelta GABAA receptors in shaping learning deficits at puberty in mice. Science 327:1515-1518.
42. Langton JM, Kim JH, Nicholas J, Richardson R (2007) The effect of the NMDA receptor antagonist MK-801 on the acquisition and extinction of learned fear in the developing rat. Learn Mem 14:665-668. (Pubitemid 350036777)
43. 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 29:10802-10808.
44. Kim JH, Richardson R (2010) Extinction in preweanling rats does not involve NMDA receptors. Neurobiol Learn Mem 94:176-182.
45. Kim JH, Richardson R (2007) A developmental dissociation in reinstatement of an extinguished fear response in rats. Neurobiol Learn Mem 88:48-57. (Pubitemid 46809811)
46. Burgos-Robles A, Vidal-Gonzalez I, Santini E, Quirk GJ (2007) Consolidation of fear extinction requires NMDA receptor-dependent bursting in the ventromedial prefrontal cortex. Neuron 53:871-880. (Pubitemid 46367556)
47. Vertes RP (2004) Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 51:32-58.
48. Vertes RP (2006) Interactions among the medial prefrontal cortex, hippocampus and midline thalamus in emotional and cognitive processing in the rat. Neuroscience 142:1-20.
49. Paré D, Quirk GJ, Ledoux JE (2004) New vistas on amygdala networks in conditioned fear. J Neurophysiol 92:1-9. (Pubitemid 38802225)
50. Milad MR, Quirk GJ (2002) Neurons in medial prefrontal cortex signal memory for fear extinction. Nature 420:70-74. (Pubitemid 35291441)
51. Quirk GJ, Garcia R, González-Lima F (2006) Prefrontal mechanisms in extinction of conditioned fear. Biol Psychiatry 60:337-343. (Pubitemid 44215848)
52. Likhtik E, Pelletier JG, Paz R, Pare D (2005) Prefrontal control of the amygdala. J Neurosci 25:7429-7437. (Pubitemid 41129816)
53. Phelps EA, Delgado MR, Nearing KI, LeDoux JE (2004) Extinction learning in humans: Role of the amygdala and vmPFC. Neuron 43:897-905. (Pubitemid 39215019)
54. Chattopadhyaya B, et al. (2004) Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period. J Neurosci 24:9598-9611. (Pubitemid 39441514)
55. Kilb W (2011) Development of the GABAergic system from birth to adolescence. Neuroscientist, 10.1177/1073858411422114.
56. Fanselow MS (1980) Conditioned and unconditional components of post-shock freezing. Pavlov J Biol Sci 15:177-182.