Fear learning and memory across adolescent development. Hormones and behavior special issue: Puberty and adolescence

Hormones and Behavior

Volumn 64, Issue 2, 2013, Pages 380-389

  Pattwell, Siobhan S ^a   Lee, Francis S ^a   Casey, B J ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Adolescence; Amygdala; Anxiety; Development; Extinction; Fear; Hippocampus; Prefrontal cortex; Sensitive period

Indexed keywords

ADOLESCENCE; ADOLESCENT DEVELOPMENT; ANXIETY; ANXIETY DISORDER; BEHAVIOR THERAPY; CHILD BEHAVIOR; CONDITIONING; CONNECTOME; DEVELOPMENTAL MODEL; DEVELOPMENTAL STAGE; DRUG THERAPY; FEAR; HUMAN; LEARNING; MEMORY; MODEL; NONHUMAN; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; PUBERTY; REVIEW;

ADOLESCENCE; AMYGDALA; ANXIETY; DEVELOPMENT; EXTINCTION; FEAR; HIPPOCAMPUS; PREFRONTAL CORTEX; SENSITIVE PERIOD;

ADOLESCENT; ADOLESCENT DEVELOPMENT; ANIMALS; CONDITIONING (PSYCHOLOGY); FEAR; HUMANS; LEARNING; MEMORY; MICE; SEXUAL MATURATION; STRESS, PSYCHOLOGICAL;

EID: 84883349535     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2013.01.016     Document Type: Review

References (125)

1. Adriani W., Chiarotti F., Laviola G. Elevated novelty seeking and peculiar d-amphetamine sensitization in periadolescent mice compared with adult mice. Behav. Neurosci. 1998, 112:1152-1166.
2. Arnold S.E., Trojanowski J.Q. Human fetal hippocampal development: I. Cytoarchitecture, myeloarchitecture, and neuronal morphologic features. J. Comp. Neurol. 1996, 367:274-292.
3. Bannerman D.M., Rawlins J.N., McHugh S.B., Deacon R.M., Yee B.K., Bast T., Zhang W.N., Pothuizen H.H., Feldon J. Regional dissociations within the hippocampus - memory and anxiety. Neurosci. Biobehav. Rev. 2004, 28:273-283.
4. Bechara A., Tranel D., Damasio H., Adolphs R., Rockland C., Damasio A.R. Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans. Science 1995, 269:1115-1118.
5. Benes F.M., Turtle M., Khan Y., Farol P. Myelination of a key relay zone in the hippocampal formation occurs in the human brain during childhood, adolescence, and adulthood. Arch. Gen. Psychiatry 1994, 51:477-484.
6. Bourtchouladze R., Abel T., Berman N., Gordon R., Lapidus K., Kandel E.R. Different training procedures recruit either one or two critical periods for contextual memory consolidation, each of which requires protein synthesis and PKA. Learn. Mem. 1998, 5:365-374.
7. Bouton M.E., Westbrook R.F., Corcoran K.A., Maren S. Contextual and temporal modulation of extinction: behavioral and biological mechanisms. Biol. Psychiatry 2006, 60:352-360.
8. Bremner J.D. Alterations in brain structure and function associated with post-traumatic stress disorder. Semin. Clin. Neuropsychiatry 1999, 4:249-255.
9. Brown S., Schafer E.A. An investigation into the functions of the occipital and temporal lobes of the monkey's brain. Philos. Trans. R. Soc. Lond. B 1888, 179:303-327.
10. Burgos-Robles A., Vidal-Gonzalez I., Quirk G.J. Sustained conditioned responses in prelimbic prefrontal neurons are correlated with fear expression and extinction failure. J. Neurosci. 2009, 29:8474-8482.
11. Callaghan B.L., Richardson R. Early-life stress affects extinction during critical periods of development: an analysis of the effects of maternal separation on extinction in adolescent rats. Stress 2012, 15(6):671-679. (Nov).
12. Casey B.J., Tottenham N., Liston C., Durston S. Imaging the developing brain: what have we learned about cognitive development?. Trends Cogn. Sci. 2005, 9:104-110.
13. Casey B.J., Getz S., Galvan A. The adolescent brain. Dev. Rev. 2008, 28:62-77.
14. Casey B.J., Pattwell S.S., Glatt C.E., Lee F.S. Treating the developing brain: implications from human imaging and mouse genetics. Annu. Rev. Med. 2013, 64.
15. Cavada C., Company T., Tejedor J., Cruz-Rizzolo R.J., Reinoso-Suarez F. The anatomical connections of the macaque monkey orbitofrontal cortex. A review. Cereb. Cortex 2000, 10:220-242.
16. Chan T., Kyere K., Davis B.R., Shemyakin A., Kabitzke P.A., Shair H.N., Barr G.A., Wiedenmayer C.P. The role of the medial prefrontal cortex in innate fear regulation in infants, juveniles, and adolescents. J. Neurosci. 2011, 31:4991-4999.
17. Chen X., Garelick M.G., Wang H., Lil V., Athos J., Storm D.R. PI3 kinase signaling is required for retrieval and extinction of contextual memory. Nat. Neurosci. 2005, 8:925-931.
18. Collins D.R., Pare D. Differential fear conditioning induces reciprocal changes in the sensory responses of lateral amygdala neurons to the CS(+) and CS(-). Learn. Mem. 2000, 7:97-103.
19. Corcoran K.A., Quirk G.J. Activity in prelimbic cortex is necessary for the expression of learned, but not innate, fears. J. Neurosci. 2007, 27:840-844.
20. Corcoran K.A., Desmond T.J., Frey K.A., Maren S. Hippocampal inactivation disrupts the acquisition and contextual encoding of fear extinction. J. Neurosci. 2005, 25:8978-8987.
21. Costello E.J., Egger H., Angold A. 10-year research update review: the epidemiology of child and adolescent psychiatric disorders: I. Methods and public health burden. J. Am. Acad. Child Adolesc. Psychiatry 2005, 44:972-986.
22. Craske M.G., Waters A.M., Lindsey Bergman R., Naliboff B., Lipp O.V., Negoro H., Ornitz E.M. Is aversive learning a marker of risk for anxiety disorders in children?. Behav. Res. Ther. 2008, 46:954-967.
23. Cunningham M.G., Bhattacharyya S., Benes F.M. Amygdalo-cortical sprouting continues into early adulthood: implications for the development of normal and abnormal function during adolescence. J. Comp. Neurol. 2002, 453:116-130.
24. Doremus-Fitzwater T.L., Barreto M., Spear L.P. Age-related differences in impulsivity among adolescent and adult Sprague-Dawley rats. Behav. Neurosci. 2012, 126(5):735-741. (Oct).
25. Eshel N., Nelson E.E., Blair R.J., Pine D.S., Ernst M. Neural substrates of choice selection in adults and adolescents: development of the ventrolateral prefrontal and anterior cingulate cortices. Neuropsychologia 2007, 45:1270-1279.
26. Fanselow M.S., Dong H.W. Are the dorsal and ventral hippocampus functionally distinct structures?. Neuron 2010, 65:7-19.
27. Fanselow M.S., Kim J.J. Acquisition of contextual Pavlovian fear conditioning is blocked by application of an NMDA receptor antagonist d, l-2-amino-5-phosphonovaleric acid to the basolateral amygdala. Behav. Neurosci. 1994, 108:210-212.
28. Foy M.R. Ovarian hormones, aging and stress on hippocampal synaptic plasticity. Neurobiol. Learn. Mem. 2011, 95:134-144.
29. Giedd J.N., Snell J.W., Lange N., Rajapakse J.C., Casey B.J., Kozuch P.L., Vaituzis A.C., Vauss Y.C., Hamburger S.D., Kaysen D., Rapoport J.L. Quantitative magnetic resonance imaging of human brain development: ages 4-18. Cereb. Cortex 1996, 6:551-560.
30. Giedd J.N., Blumenthal J., Jeffries N.O., Castellanos F.X., Liu H., Zijdenbos A., Paus T., Evans A.C., Rapoport J.L. Brain development during childhood and adolescence: a longitudinal MRI study. Nat. Neurosci. 1999, 2:861-863.
31. Glenn C.R., Klein D.N., Lissek S., Britton J.C., Pine D.S., Hajcak G. The development of fear learning and generalization in 8-13year-olds. Dev. Psychobiol. 2011.
32. Gogtay N., Giedd J.N., Lusk L., Hayashi K.M., Greenstein D., Vaituzis A.C., Nugent T.F., Herman D.H., Clasen L.S., Toga A.W., Rapoport J.L., Thompson P.M. Dynamic mapping of human cortical development during childhood through early adulthood. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:8174-8179.
33. Gogtay N., Nugent T.F., Herman D.H., Ordonez A., Greenstein D., Hayashi K.M., Clasen L., Toga A.W., Giedd J.N., Rapoport J.L., Thompson P.M. Dynamic mapping of normal human hippocampal development. Hippocampus 2006, 16:664-672.
34. Gottfried J.A., Dolan R.J. Human orbitofrontal cortex mediates extinction learning while accessing conditioned representations of value. Nat. Neurosci. 2004, 7:1144-1152.
35. Graber J.A., Brooks-Gunn J. Expectations for and precursors to leaving home in young women. New Dir. Child Dev. 1996, 21-38.
36. Grillon C., Dierker L., Merikangas K.R. Fear-potentiated startle in adolescent offspring of parents with anxiety disorders. Biol. Psychiatry 1998, 44:990-997.
37. Guyer A.E., Lau J.Y., McClure-Tone E.B., Parrish J., Shiffrin N.D., Reynolds R.C., Chen G., Blair R.J., Leibenluft E., Fox N.A., Ernst M., Pine D.S., Nelson E.E. Amygdala and ventrolateral prefrontal cortex function during anticipated peer evaluation in pediatric social anxiety. Arch. Gen. Psychiatry 2008, 65:1303-1312.
38. Hare T.A., Tottenham N., Galvan A., Voss H.U., Glover G.H., Casey B.J. Biological substrates of emotional reactivity and regulation in adolescence during an emotional go-nogo task. Biol. Psychiatry 2008, 63:927-934.
39. Hefner K., Holmes A. Ontogeny of fear-, anxiety- and depression-related behavior across adolescence in C57BL/6J mice. Behav. Brain Res. 2007, 176:210-215.
40. Hefner K., Whittle N., Juhasz J., Norcross M., Karlsson R.M., Saksida L.M., Bussey T.J., Singewald N., Holmes A. Impaired fear extinction learning and cortico-amygdala circuit abnormalities in a common genetic mouse strain. J. Neurosci. 2008, 28:8074-8085.
41. Herry C., Ciocchi S., Senn V., Demmou L., Muller C., Luthi A. Switching on and off fear by distinct neuronal circuits. Nature 2008, 454:600-606.
42. Hobin J.A., Ji J., Maren S. Ventral hippocampal muscimol disrupts context-specific fear memory retrieval after extinction in rats. Hippocampus 2006, 16:174-182.
43. Hugues S., Garcia R. Reorganization of learning-associated prefrontal synaptic plasticity between the recall of recent and remote fear extinction memory. Learn. Mem. 2007, 14:520-524.
44. Insel T.R., Fernald R.D. How the brain processes social information: searching for the social brain. Annu. Rev. Neurosci. 2004, 27:697-722.
45. Kalisch R., Korenfeld E., Stephan K.E., Weiskopf N., Seymour B., Dolan R.J. Context-dependent human extinction memory is mediated by a ventromedial prefrontal and hippocampal network. J. Neurosci. 2006, 26:9503-9511.
46. Keller M.B., Lavori P.W., Wunder J., Beardslee W.R., Schwartz C.E., Roth J. Chronic course of anxiety disorders in children and adolescents. J. Am. Acad. Child Adolesc. Psychiatry 1992, 31:595-599.
47. Kessler R.C., Demler O., Frank R.G., Olfson M., Pincus H.A., Walters E.E., Wang P., Wells K.B., Zaslavsky A.M. Prevalence and treatment of mental disorders, ss to 2003. N. Engl. J. Med. 2005, 352:2515-2523.
48. Kim J.J., Fanselow M.S. Modality-specific retrograde amnesia of fear. Science 1992, 256:675-677.
49. Kim H., Somerville L.H., Johnstone T., Alexander A.L., Whalen P.J. Inverse amygdala and medial prefrontal cortex responses to surprised faces. Neuroreport 2003, 14:2317-2322.
50. Kim J.H., Hamlin A.S., Richardson R. Fear extinction across development: the involvement of the medial prefrontal cortex as assessed by temporary inactivation and immunohistochemistry. J. Neurosci. 2009, 29:10802-10808.
51. Kim J.H., Li S., Richardson R. Immunohistochemical analyses of long-term extinction of conditioned fear in adolescent rats. Cereb. Cortex 2011, 21:530-538.
52. Kim-Cohen J., Caspi A., Moffitt T.E., Harrington H., Milne B.J., Poulton R. Prior juvenile diagnoses in adults with mental disorder: developmental follow-back of a prospective-longitudinal cohort. Arch. Gen. Psychiatry 2003, 60:709-717.
53. Kiyama Y., Manabe T., Sakimura K., Kawakami F., Mori H., Mishina M. Increased thresholds for long-term potentiation and contextual learning in mice lacking the NMDA-type glutamate receptor epsilon1 subunit. J. Neurosci. 1998, 18:6704-6712.
54. Kluver H., Bucy P.C. "Psychic blindness" and other symptoms following bilateral temporal lobectomy in Rhesus monkeys. Am. J. Physiol. 1937, 119:352-353.
55. Knapska E., Maren S. Reciprocal patterns of c-Fos expression in the medial prefrontal cortex and amygdala after extinction and renewal of conditioned fear. Learn. Mem. 2009, 16:486-493.
56. Kornack D.R., Rakic P. Continuation of neurogenesis in the hippocampus of the adult macaque monkey. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:5768-5773.
57. LaBar K.S., LeDoux J.E. Partial disruption of fear conditioning in rats with unilateral amygdala damage: correspondence with unilateral temporal lobectomy in humans. Behav. Neurosci. 1996, 110:991-997.
58. LaBar K.S., LeDoux J.E., Spencer D.D., Phelps E.A. Impaired fear conditioning following unilateral temporal lobectomy in humans. J. Neurosci. 1995, 15:6846-6855.
59. Lau J.Y., Lissek S., Nelson E.E., Lee Y., Roberson-Nay R., Poeth K., Jenness J., Ernst M., Grillon C., Pine D.S. Fear conditioning in adolescents with anxiety disorders: results from a novel experimental paradigm. J. Am. Acad. Child Adolesc. Psychiatry 2008, 47:94-102.
60. Lau J.Y., Britton J.C., Nelson E.E., Angold A., Ernst M., Goldwin M., Grillon C., Leibenluft E., Lissek S., Norcross M., Shiffrin N., Pine D.S. Distinct neural signatures of threat learning in adolescents and adults. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:4500-4505.
61. Laurent V., Westbrook R.F. Inactivation of the infralimbic but not the prelimbic cortex impairs consolidation and retrieval of fear extinction. Learn. Mem. 2009, 16:520-529.
62. Laviola G., Adriani W., Terranova M.L., Gerra G. Psychobiological risk factors for vulnerability to psychostimulants in human adolescents and animal models. Neurosci. Biobehav. Rev. 1999, 23:993-1010.
63. LeDoux J.E. Emotion circuits in the brain. Annu. Rev. Neurosci. 2000, 23:155-184.
64. Lee I., Kesner R.P. Differential contributions of dorsal hippocampal subregions to memory acquisition and retrieval in contextual fear-conditioning. Hippocampus 2004, 14:301-310.
65. Liberman L.C., Lipp O.V., Spence S.H., March S. Evidence for retarded extinction of aversive learning in anxious children. Behav. Res. Ther. 2006, 44:1491-1502.
66. Liberzon I., Sripada C.S. The functional neuroanatomy of PTSD: a critical review. Prog. Brain Res. 2008, 167:151-169.
67. Mahan A.L., Ressler K.J. Fear conditioning, synaptic plasticity and the amygdala: implications for posttraumatic stress disorder. Trends Neurosci. 2011, 35(1):24-35. (Jan).
68. Maren S. Neurobiology of Pavlovian fear conditioning. Annu. Rev. Neurosci. 2001, 24:897-931.
69. Maren S. Seeking a spotless mind: extinction, deconsolidation, and erasure of fear memory. Neuron 2011, 70:830-845.
70. Maren S., Hobin J.A. Hippocampal regulation of context-dependent neuronal activity in the lateral amygdala. Learn. Mem. 2007, 14:318-324.
71. Maren S., Quirk G.J. Neuronal signalling of fear memory. Nat. Rev. Neurosci. 2004, 5:844-852.
72. Maren S., Aharonov G., Stote D.L., Fanselow M.S. N-methyl-d-aspartate receptors in the basolateral amygdala are required for both acquisition and expression of conditional fear in rats. Behav. Neurosci. 1996, 110:1365-1374.
73. McCallum J., Kim J.H., Richardson R. Impaired extinction retention in adolescent rats: effects of d-cycloserine. Neuropsychopharmacology 2010, 35:2134-2142.
74. McKernan M.G., Shinnick-Gallagher P. Fear conditioning induces a lasting potentiation of synaptic currents in vitro. Nature 1997, 390:607-611.
75. Merikangas K.R., He J.P., Burstein M., Swanson S.A., Avenevoli S., Cui L., Benjet C., Georgiades K., Swendsen J. 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 2010, 49:980-989.
76. Milad M.R., Quirk G.J. Neurons in medial prefrontal cortex signal memory for fear extinction. Nature 2002, 420:70-74.
77. Milad M.R., Quirk G.J. Fear extinction as a model for translational neuroscience: ten years of progress. Annu. Rev. Psychol. 2012, 63:129-151.
78. Milad M.R., Vidal-Gonzalez I., Quirk G.J. Electrical stimulation of medial prefrontal cortex reduces conditioned fear in a temporally specific manner. Behav. Neurosci. 2004, 118:389-394.
79. Milad M.R., Quinn B.T., Pitman R.K., Orr S.P., Fischl B., Rauch S.L. Thickness of ventromedial prefrontal cortex in humans is correlated with extinction memory. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:10706-10711.
80. 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. Neurobiological basis of failure to recall extinction memory in posttraumatic stress disorder. Biol. Psychiatry 2009, 66:1075-1082.
81. Miserendino M.J., Sananes C.B., Melia K.R., Davis M. Blocking of acquisition but not expression of conditioned fear-potentiated startle by NMDA antagonists in the amygdala. Nature 1990, 345:716-718.
82. Monk C.S., McClure E.B., Nelson E.E., Zarahn E., Bilder R.M., Leibenluft E., Charney D.S., Ernst M., Pine D.S. Adolescent immaturity in attention-related brain engagement to emotional facial expressions. NeuroImage 2003, 20:420-428.
83. Monk C.S., Telzer E.H., Mogg K., Bradley B.P., Mai X., Louro H.M., Chen G., McClure-Tone E.B., Ernst M., Pine D.S. Amygdala and ventrolateral prefrontal cortex activation to masked angry faces in children and adolescents with generalized anxiety disorder. Arch. Gen. Psychiatry 2008, 65:568-576.
84. Morgan M.A., Romanski L.M., LeDoux J.E. Extinction of emotional learning: contribution of medial prefrontal cortex. Neurosci. Lett. 1993, 163:109-113.
85. Moriceau S., Sullivan R.M. Maternal presence serves as a switch between learning fear and attraction in infancy. Nat. Neurosci. 2006, 9:1004-1006.
86. Newman D.L., Moffitt T.E., Caspi A., Magdol L., Silva P.A., Stanton W.R. 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. 1996, 64:552-562.
87. Pare D., Quirk G.J., Ledoux J.E. New vistas on amygdala networks in conditioned fear. J. Neurophysiol. 2004, 92:1-9.
88. Pattwell S.S., Bath K.G., Casey B.J., Ninan I., Lee F.S. Selective early-acquired fear memories undergo temporary suppression during adolescence. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:1182-1187.
89. Pattwell S.S., Duhoux S., Hartley C.A., Johnson D.C., Jing D., Elliott M.D., Ruberry E.J., Powers A., Mehta N., Yang R.R., Soliman F., Glatt C.E., Casey B.J., Ninan I., Lee F.S. Altered fear learning across development in both mouse and human. Proc. Natl. Acad. Sci. U. S. A. 2012, 109(40):16318-16323. (Oct 2).
90. Petrovich G.D., Canteras N.S., Swanson L.W. Combinatorial amygdalar inputs to hippocampal domains and hypothalamic behavior systems. Brain Res. Brain Res. Rev. 2001, 38:247-289.
91. Pezawas L., Meyer-Lindenberg A., Drabant E.M., Verchinski B.A., Munoz K.E., Kolachana B.S., Egan M.F., Mattay V.S., Hariri A.R., Weinberger D.R. 5-HTTLPR polymorphism impacts human cingulate-amygdala interactions: a genetic susceptibility mechanism for depression. Nat. Neurosci. 2005, 8:828-834.
92. Phelps E.A., LeDoux J.E. Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 2005, 48:175-187.
93. Phillips R.G., LeDoux J.E. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav. Neurosci. 1992, 106:274-285.
94. Pine D.S., Cohen P., Gurley D., Brook J., Ma Y. The risk for early-adulthood anxiety and depressive disorders in adolescents with anxiety and depressive disorders. Arch. Gen. Psychiatry 1998, 55:56-64.
95. Pitkanen A., Pikkarainen M., Nurminen N., Ylinen A. Reciprocal connections between the amygdala and the hippocampal formation, perirhinal cortex, and postrhinal cortex in rat. A review. Ann. N. Y. Acad. Sci. 2000, 911:369-391.
96. Pollack M.H., Otto M.W., Sabatino S., Majcher D., Worthington J.J., McArdle E.T., Rosenbaum J.F. Relationship of childhood anxiety to adult panic disorder: correlates and influence on course. Am. J. Psychiatry 1996, 153:376-381.
97. Quirk G.J., Mueller D. Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 2008, 33:56-72.
98. Quirk G.J., Repa C., LeDoux J.E. Fear conditioning enhances short-latency auditory responses of lateral amygdala neurons: parallel recordings in the freely behaving rat. Neuron 1995, 15:1029-1039.
99. Quirk G.J., Armony J.L., LeDoux J.E. Fear conditioning enhances different temporal components of tone-evoked spike trains in auditory cortex and lateral amygdala. Neuron 1997, 19:613-624.
100. Rah J.H., Shamim A.A., Arju U.T., Labrique A.B., Rashid M., Christian P. Age of onset, nutritional determinants, and seasonal variations in menarche in rural Bangladesh. J. Health Popul. Nutr. 2009, 27:802-807.
101. Rauch S.L., Shin L.M., Phelps E.A. Neurocircuitry models of posttraumatic stress disorder and extinction: human neuroimaging research - past, present, and future. Biol. Psychiatry 2006, 60:376-382.
102. Rodriguez B.I., Craske M.G., Mineka S., Hladek D. Context-specificity of relapse: effects of therapist and environmental context on return of fear. Behav. Res. Ther. 1999, 37:845-862.
103. Rogan M.T., LeDoux J.E. LTP is accompanied by commensurate enhancement of auditory-evoked responses in a fear conditioning circuit. Neuron 1995, 15:127-136.
104. Rogan M.T., Staubli U.V., LeDoux J.E. Fear conditioning induces associative long-term potentiation in the amygdala. Nature 1997, 390:604-607.
105. Rudy J.W. Contextual conditioning and auditory cue conditioning dissociate during development. Behav. Neurosci. 1993, 107:887-891.
106. Rudy J.W., Morledge P. Ontogeny of contextual fear conditioning in rats: implications for consolidation, infantile amnesia, and hippocampal system function. Behav. Neurosci. 1994, 108:227-234.
107. Santini E., Ge H., Ren K., Pena de Ortiz S., Quirk G.J. Consolidation of fear extinction requires protein synthesis in the medial prefrontal cortex. J. Neurosci. 2004, 24:5704-5710.
108. Santini E., Quirk G.J., Porter J.T. Fear conditioning and extinction differentially modify the intrinsic excitability of infralimbic neurons. J. Neurosci. 2008, 28:4028-4036.
109. Schafe G.E., Nadel N.V., Sullivan G.M., Harris A., LeDoux J.E. Memory consolidation for contextual and auditory fear conditioning is dependent on protein synthesis, PKA, and MAP kinase. Learn. Mem. 1999, 6:97-110.
110. Schmitz A., Merikangas K., Swendsen H., Cui L., Heaton L., Grillon C. Measuring anxious responses to predictable and unpredictable threat in children and adolescents. J. Exp. Child Psychol. 2011, 110:159-170.
111. Schulz K.M., Molenda-Figueira H.A., Sisk C.L. Back to the future: the organizational-activational hypothesis adapted to puberty and adolescence. Horm. Behav. 2009, 55:597-604.
112. Selden N.R., Everitt B.J., Jarrard L.E., Robbins T.W. Complementary roles for the amygdala and hippocampus in aversive conditioning to explicit and contextual cues. Neuroscience 1991, 42:335-350.
113. Shin L.M., Orr S.P., Carson M.A., Rauch S.L., Macklin M.L., Lasko N.B., Peters P.M., Metzger L.J., Dougherty D.D., Cannistraro P.A., Alpert N.M., Fischman A.J., Pitman R.K. Regional cerebral blood flow in the amygdala and medial prefrontal cortex during traumatic imagery in male and female Vietnam veterans with PTSD. Arch. Gen. Psychiatry 2004, 61:168-176.
114. Sierra-Mercado D., Corcoran K.A., Lebron-Milad K., Quirk G.J. Inactivation of the ventromedial prefrontal cortex reduces expression of conditioned fear and impairs subsequent recall of extinction. Eur. J. Neurosci. 2006, 24:1751-1758.
115. Sierra-Mercado D., Padilla-Coreano N., Quirk G.J. Dissociable roles of prelimbic and infralimbic cortices, ventral hippocampus, and basolateral amygdala in the expression and extinction of conditioned fear. Neuropsychopharmacology 2011, 36:529-538.
116. Sigurdsson T., Doyere V., Cain C.K., LeDoux J.E. Long-term potentiation in the amygdala: a cellular mechanism of fear learning and memory. Neuropharmacology 2007, 52:215-227.
117. Silk J.S., Siegle G.J., Whalen D.J., Ostapenko L.J., Ladouceur C.D., Dahl R.E. Pubertal changes in emotional information processing: pupillary, behavioral, and subjective evidence during emotional word identification. Dev. Psychopathol. 2009, 21:7-26.
118. Sisk C.L., Zehr J.L. Pubertal hormones organize the adolescent brain and behavior. Front. Neuroendocrinol. 2005, 26:163-174.
119. Sotres-Bayon F., Quirk G.J. Prefrontal control of fear: more than just extinction. Curr. Opin. Neurobiol. 2010, 20:231-235.
120. Sotres-Bayon F., Cain C.K., LeDoux J.E. Brain mechanisms of fear extinction: historical perspectives on the contribution of prefrontal cortex. Biol. Psychiatry 2006, 60:329-336.
121. Spear L.P. The adolescent brain and age-related behavioral manifestations. Neurosci. Biobehav. Rev. 2000, 24:417-463.
122. Spear L.P. Heightened stress responsivity and emotional reactivity during pubertal maturation: implications for psychopathology. Dev. Psychopathol. 2009, 21:87-97.
123. Tsien J.Z., Huerta P.T., Tonegawa S. The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory. Cell 1996, 87:1327-1338.
124. Tsvetkov E., Carlezon W.A., Benes F.M., Kandel E.R., Bolshakov V.Y. Fear conditioning occludes LTP-induced presynaptic enhancement of synaptic transmission in the cortical pathway to the lateral amygdala. Neuron 2002, 34:289-300.
125. Weiskrantz L. Behavioral changes associated with ablation of the amygdaloid complex in monkeys. J. Comp. Physiol. Psychol. 1956, 49:381-391.