From resilience to vulnerability: Mechanistic insights into the effects of stress on transitions in critical period plasticity

Frontiers in Psychiatry

Volumn 4, Issue AUG, 2013, Pages

  Callaghan, Bridget L ^a   Graham, Bronwyn M ^a   Li, Stella ^a   Richardson, Rick ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR 2; MESSENGER RNA;

AMNESIA; AMYGDALOID NUCLEUS; AVERSIVE BEHAVIOR; COPING BEHAVIOR; EARLY LIFE STRESS; ELECTROENCEPHALOGRAM; FEAR; FGF2 GENE; GABAERGIC TRANSMISSION; GENE EXPRESSION; HIPPOCAMPUS; HUMAN; INTRACELLULAR SIGNALING; LONG TERM EXPOSURE; LONG TERM MEMORY; MEMORY CONSOLIDATION; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; REARING; REINFORCEMENT; REVIEW; UPREGULATION; VULNERABLE POPULATION;

EID: 84884397374     PISSN: None     EISSN: 16640640     Source Type: Journal    
DOI: 10.3389/fpsyt.2013.00090     Document Type: Review

References (170)

1. Repetti RL, Taylor SE, Seeman TE. Risky families: family social environments and the mental and physical health of offspring. Psychol Bull (2002) 128:330-66. doi:10.1037/0033-2909.128.2.330
2. McLaughlin KJ, Gomez JL, Baran SE, Conrad CD. The effects of chronic stress on hippocampal morphology and function: an evaluation of chronic restraint paradigms. Brain Res (2007) 1161:56-64. doi:10.1016/j.brainres.2007.05.042
3. Nelson CA, Zeanah CH, Fox NA, Marshall PJ, Smyke AT, Guthrie D. Cognitive recovery in socially deprived young children: the Bucharest Early Intervention Project. Science (2007) 318:1937-40. doi:10.1126/science.1143921
4. Zeanah C, Egger H, Smyke A, Nelson C, Fox N, Marshall P, et al. Institutional rearing and psychiatric disorders in Romanian preschool children. Am J Psychiatry (2009) 166:777-85. doi:10.1176/appi.ajp.2009.08091438
5. Taylor SE, Way BM, Seeman TE. Early adversity and adult health outcomes. Dev Psychopathol (2011) 23:939-54. doi:10.1017/S0954579411000411
6. Bock J, Gruss M, Becker S, Braun K. Experience-induced changes of dendritic spine densities in the prefrontal and sensory cortex: correlation with developmental time windows. Cereb Cortex (2005) 15:802-8. doi:10.1093/cercor/bhh181
7. Tottenham N, Hare TA, Quinn BT, McCarry TW, Nurse M, Gilhooly T, et al. Prolonged institutional rearing is associated with atypically large amygdala volume and difficulties in emotion regulation. Dev Sci (2010) 13:46-61. doi:10.1111/j.1467-7687.2009.00852.x
8. Xie L, Korkmaz KS, Braun K, Bock J. Early life stress-induced histone acetylations correlate with activation of the synaptic plasticity genes Arc and Egr1 in the mouse hippocampus. J Neurochem (2013) 125:457-64. doi:10.1111/jnc.12210
9. Coles ME, Heimberg RG. Memory biases in the anxiety disorders: current status. Clin Psychol Rev (2002) 22:587-627. doi:10.1016/S0272-7358(01)00113-1
10. Lissek S, Powers AS, McClure EB, Phelps EA, Woldehawariat G, Grillon C, et al. Classical fear conditioning in the anxiety disorders: a meta-analysis. Behav Res Ther (2005) 43:1391-424. doi:10.1016/j.brat.2004.10.007
11. Milad MR, Orr SP, Lasko NB, Chang Y, Rauch SL, Pitman RK. Presence and acquired origin of reduced recall for fear extinction in PTSD: results of a twin study. J Psychiatr Res (2008) 42:515-20. doi:10.1016/j.jpsychires.2008.01.017
12. Milad MR, Pitman RK, Ellis CB, Gold AL, Shin LM, Lasko NB, et al. Neurobiological basis of failure to recall extinction memory in posttraumatic stress disorder. Biol Psychiatry (2009) 66:1075-82. doi:10.1016/j.biopsych.2009.06.026
13. Campbell BA, Campbell EH. Retention and extinction of learned fear in infant and adult rats. J Comp Physiol Psychol (1962) 55:1-8. doi:10.1037/h0049182
14. Campbell BA, Spear NE. Ontogeny of memory. Psychol Rev (1972) 79:215-36. doi:10.1037/h0032690
15. Kim JH, McNally GP, Richardson R. Recovery of fear memories in rats: role of gamma-amino butyric acid (GABA) in infantile amnesia. Behav Neurosci (2006) 120:40-8. doi:10.1037/0735-7044.120.1.40
16. Yap CSL, Richardson R. Extinction in the developing rat: an examination of renewal effects. Dev Psychobiol (2007) 49:565-75. doi:10.1002/dev.20244
17. Kim JH, Richardson R. New findings on extinction of conditioned fear early in development: theoretical and clinical implications. Biol Psychiatry (2010) 67:297-303. doi:10.1016/j.biopsych.2009.09.003
18. Kim JH, Li S, Hamlin AS, McNally GP, Richardson R. 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 (2012) 97:59-68. doi:10.1016/j.nlm.2011.09.005
19. Blanchard RJ, Blanchard DC. Passive and active reactions to fear-eliciting stimuli. J Comp Physiol Psychol (1969) 68:129. doi:10.1037/h0027676
20. Gale GD, Anagnostaras SG, Godsil BP, Mitchell S, Nozawa T, Sage JR, et al. Role of the basolateral amygdala in the storage of fear memories across the adult lifetime of rats. J Neurosci (2004) 24:3810-5. doi:10.1523/JNEUROSCI.4100-03.2004
21. Campbell BA, Jaynes J, Misanin JR. Retention of a light-dark discrimination in rats of different ages. J Comp Physiol Psychol (1968) 66:467. doi:10.1037/h0026360
22. Feigley DA, Spear NE. Effect of age and punishment condition on long-term retention by the rat of active-and passive-avoidance learning. J Comp Physiol Psychol (1970) 73:515. doi:10.1037/h0030234
23. Spear NE, Rudy JW. Tests of the Ontogeny of Learning and Memory: Issues, Methods, and Results. New York, NY: Oxford University Press. (1991).
24. Hayne H. Infant memory development: implications for childhood amnesia. Dev Rev (2004) 24:33-73. doi:10.1016/j.dr.2003.09.007
25. Campbell BA, Jaynes J. Reinstatement. Psychol Rev (1966) 73:478-80. doi:10.1037/h0023679
26. Spear NE, Parsons PJ. Analysis of a reactivation treatment: ontogenetic determinants of alleviated forgetting. In: Medin DL, Roberts WA, Davis RT, editors. Processes of Animal Memory. Hillsdale, NJ: Erlbaum (1976). p. 135-65.
27. Rovee-Collier C. Dissociations in infant memory: rethinking the development of implicit and explicit memory. Psychol Rev (1997) 104:467. doi:10.1037/0033-295X.104.3.467
28. Tang HH, McNally GP, Richardson R. The effects of FG7142 on two types of forgetting in 18-day-old rats. Behav Neurosci (2007) 121:1421-4. doi:10.1037/0735-7044.121.6.1421
29. Harris JA, Westbrook RF. Benzodiazepine-induced amnesia in rats: reinstatement of conditioned performance by noxious stimulation on test. Behav Neurosci (1998) 112:183-92. doi:10.1037/0735-7044.112.1.183
30. Bouton ME, Bolles RC. Contextual control of the extinction of conditioned fear. Learn Motiv (1979) 10:445-66. doi:10.1016/0023-9690(79)90057-2
31. Milad MR, Orr SP, Pitman RK, Rauch SL. Context modulation of memory for fear extinction in humans. Psychophysiology (2005) 42:456-64. doi:10.1111/j.1469-8986.2005.00302.x
32. Bouton ME, Bolles RC. Role of conditioned contextual stimuli in reinstatement of extinguished fear. J Exp Psychol Anim Behav Process (1979) 5:368-78. doi:10.1037/0097-7403.5.4.368
33. Schiller D, Cain CK, Curley NG, Schwartz JS, Stern SA, LeDoux JE, et al. Evidence for recovery of fear following immediate extinction in rats and humans. Learn Mem (2008) 15:394-402. doi:10.1101/lm.909208
34. Quirk GJ. Memory for extinction of conditioned fear is long-lasting and persists following spontaneous recovery. Learn Mem (2002) 9:402-7. doi:10.1101/lm.49602
35. Miserendino MJD, Sananes CB, Melia KR, Davis M. Blocking of acquisition but not expression of conditioned fear-potentiated startle by NMDA antagonists in the amygdala. Nature (1990) 345:716-8. doi:10.1038/345716a0
36. Falls WA, Miserendino MJ, Davis M. Extinction of fear-potentiated startle: blockade by infusion of an NMDA antagonist into the amygdala. J Neurosci (1992) 12:854-63.
37. Laurent V, Westbrook RF. Infusion of the NMDA receptor antagonist, DL-APV, into the basolateral amygdala disrupts learning to fear a novel and a familiar context as well as relearning to fear an extinguished context. Learn Mem (2009) 16:96-105. doi:10.1101/lm.1218709
38. Walker DL, Ressler KJ, Lu K-T, Davis M. Facilitation of conditioned fear extinction by systemic administration or intra-amygdala infusions of D-cycloserine as assessed with fear-potentiated startle in rats. J Neurosci (2002) 22:2343-51.
39. Ledgerwood L, Richardson R, Cranney J. Effects of D-cycloserine on extinction of conditioned freezing. Behav Neurosci (2003) 117:341-9. doi:10.1037/0735-7044.117.2.341
40. Ledgerwood L, Richardson R, Cranney J. D-cycloserine and the facilitation of extinction of conditioned fear: consequences for reinstatement. Behav Neurosci (2004) 118:505-13. doi:10.1037/0735-7044.118.3.505
41. Harris JA, Westbrook RF. Evidence that GABA transmission mediates context-specific extinction of learned fear. Psychopharmacology (Berl) (1998) 140:105-15. doi:10.1007/s002130050745
42. Kim JH, Richardson R. A developmental dissociation of context and GABA effects on extinguished fear in rats. Behav Neurosci (2007) 121:131-9. doi:10.1037/0735-7044.121.1.131
43. McNally GP, Westbrook RF. Opioid receptors regulate the extinction of Pavlovian fear conditioning. Behav Neurosci (2003) 117:1292-301. doi:10.1037/0735-7044.117.6.1292
44. Kim JH, Richardson R. The effect of the μ-opioid receptor antagonist naloxone on extinction of conditioned fear in the developing rat. Learn Mem (2009) 16:161-6. doi:10.1101/lm.1282309
45. Kim JH, Richardson R. A developmental dissociation in reinstatement of an extinguished fear response in rats. Neurobiol Learn Mem (2007) 88:48-57. doi:10.1016/j.nlm.2007.03.004
46. Gogolla N, Caroni P, Lu¨thi A, Herry C. Perineuronal nets protect fear memories from erasure. Science (2009) 325:1258-61. doi:10.1126/science.1174146
47. Langton JM, Kim JH, Nicholas J, Richardson R. The effect of the NMDA receptor antagonist MK-801 on the acquisition and extinction of learned fear in the developing rat. Learn Mem (2007) 14:665-8. doi:10.1101/lm.692407
48. Ji J, Maren S. Hippocampal involvement in contextual modulation of fear extinction. Hippocampus (2007) 17:749-58. doi:10.1002/hipo.20331
49. Myers KM, Davis M. Mechanisms of fear extinction. Mol Psychiatry (2007) 12:120-50. doi:10.1038/sj.mp.4001939
50. Quirk GJ, Mueller D. Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology (2007) 33:56-72. doi:10.1038/sj.npp.1301555
51. Goosens KA, Maren S. NMDA receptors are essential for the acquisition, but not expression, of conditional fear and associative spike firing in the lateral amygdala. Eur J Neurosci (2004) 20:537-48. doi:10.1111/j.1460-9568.2004.03513.x
52. Corcoran KA, Maren S. Hippocampal inactivation disrupts contextual retrieval of fear memory after extinction. J Neurosci (2001) 21:1720-6.
53. Corcoran KA, Quirk GJ. Activity in prelimbic cortex is necessary for the expression of learned, but not innate, fears. J Neurosci (2007) 27:840-4. doi:10.1523/JNEUROSCI.5327-06.2007
54. Quirk GJ, Beer JS. Prefrontal involvement in the regulation of emotion: convergence of rat and human studies. Curr Opin Neurobiol (2006) 16:723-7. doi:10.1016/j.conb.2006.07.004
55. Phelps EA, Delgado MR, Nearing KI, LeDoux JE. Extinction learning in humans: role of the amygdala and vmPFC. Neuron (2004) 43:897-905. doi:10.1016/j.neuron.2004.08.042
56. Kalisch R, Korenfeld E, Stephan KE, Weiskopf N, Seymour B, Dolan RJ. Context-dependent human extinction memory is mediated by a ventromedial prefrontal and hippocampal network. J Neurosci (2006) 26:9503-11. doi:10.1523/JNEUROSCI.2021-06.2006
57. Bremner JD, Vermetten E, Schmahl C, Vaccarino V, Vythilingam M, Afzal N, et al. 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 (2005) 35:791-806. doi:10.1017/S0033291704003290
58. Kim JH, Richardson R. 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 (2008) 28:1282-90. doi:10.1523/JNEUROSCI.4736-07.2008
59. Kim JH, Hamlin AS, Richardson R. Fear extinction across development: the involvement of the medial prefrontal cortex as assessed by temporary inactivation and immunohistochemistry. J Neurosci (2009) 29:10802-8. doi:10.1523/JNEUROSCI.0596-09.2009
60. MacDonald S, Uesiliana K, Hayne H. Cross-cultural and gender differences in childhood amnesia. Memory (2000) 8:365-76. doi:10.1080/09658210050156822
61. Hayne H, MacDonald S, Barr R. Developmental changes in the specificity of memory over the second year of life. Infant Behav Dev (1997) 20:233-45. doi:10.1016/S0163-6383(97)90025-4
62. Hayne H, Boniface J, Barr R. The development of declarative memory in human infants: age-related changes in deferred imitation. Behav Neurosci (2000) 114:77-83. doi:10.1037/0735-7044.114.1.77
63. Rovee-Collier C, Cuevas K. The development of infant memory. In: Courage M, Cowan N, editors. The Development of Memory in Infancy and Childhood. Hoboken: Psychology Press (2009). p. 11-41.
64. Bronstein PM, Hirsch SM. Ontogeny of defensive reactions in Norway rats. J Comp Physiol Psychol (1976) 90:620-9. doi:10.1037/h0077224
65. Takahashi LK. Ontogeny of behavioral inhibition induced by unfamiliar adult male conspecifics in preweanling rats. Physiol Behav (1992) 52:493-8. doi:10.1016/0031-9384(92)90336-Z
66. Wiedenmayer CP, Barr GA. Developmental changes in c-fos expression to an age-specific social stressor in infant rats. Behav Brain Res (2001) 126:147-57. doi:10.1016/S0166-4328(01)00260-1
67. Takahashi LK, Rubin WW. Corticosteroid induction of threat-induced behavioral inhibition in preweanling rats. Behav Neurosci (1993) 107:860-6. doi:10.1037/0735-7044.107.5.860
68. Takahashi LK. Organizing action of corticosterone on the development of behavioral inhibition in the preweanling rat. Brain Res Dev Brain Res (1994) 81:121-7. doi:10.1016/0165-3806(94)90074-4
69. Moriceau S, Roth TL, Okotoghaide T, Sullivan RM. Corticosterone controls the developmental emergence of fear and amygdala function to predator odors in infant rat pups. Int J Dev Neurosci (2004) 22:415-22. doi:10.1016/j.ijdevneu.2004.05.011
70. Camp LL, Rudy JW. Changes in the categorization of appetitive and aversive events during postnatal development of the rat. Dev Psychobiol (1988) 21:25-42. doi:10.1002/dev.420210103
71. Upton KJ, Sullivan RM. Defining age limits of the sensitive period for attachment learning in rat pups. Dev Psychobiol (2010) 52:453-64. doi:10.1002/dev.20448
72. Raineki C, Moriceau S, Sullivan RM. Developing a neurobehavioral animal model of infant attachment to an abusive caregiver. Biol Psychiatry (2010) 67:1137-45. doi:10.1016/j.biopsych.2009.12.019
73. Moriceau S, Sullivan RM. Corticosterone influences on mammalian neonatal sensitive-period learning. Behav Neurosci (2004) 118:274-81. doi:10.1037/0735-7044.118.2.274
74. Moriceau S, Wilson DA, Levine S, Sullivan RM. Dual circuitry for odor-shock conditioning during infancy: corticosterone switches between fear and attraction via amygdala. J Neurosci (2006) 26:6737-48. doi:10.1523/JNEUROSCI.0499-06.2006
75. Moriceau S, Shionoya K, Jakubs K, Sullivan RM. Early-life stress disrupts attachment learning: the role of amygdala corticosterone, locus ceruleus corticotropin releasing hormone, and olfactory bulb norepinephrine. J Neurosci (2009) 29:15745-55. doi:10.1523/JNEUROSCI.4106-09.2009
76. Callaghan B, Richardson R. The effect of adverse rearing environments on persistent memories in young rats: removing the brakes on infant fear memories. Transl Psychiatry (2012) 2:e138. doi:10.1038/tp.2012.65
77. Callaghan BL, Richardson R. Maternal separation results in early emergence of adult-like fear and extinction learning in infant rats. Behav Neurosci (2011) 125:20-8. doi:10.1037/a0022008
78. Graham B, Richardson R. Memory of fearful events: the role of fibroblast growth factor-2 in fear acquisition and extinction. Neuroscience (2011) 189:156-69. doi:10.1016/j.neuroscience.2011.05.041
79. Turner CA, Watson SJ, Akil H. The fibroblast growth factor family: neuromodulation of affective behavior. Neuron (2012) 76:160-74. doi:10.1016/j.neuron.2012.08.037
80. Cheng Y, Tao Y, Black IB, DiCicco-Bloom E. A single peripheral injection of basic fibroblast growth factor (bFGF) stimulates granule cell production and increases cerebellar growth in newborn rats. J Neurobiol (2001) 46:220-9. doi:10.1002/1097-4695(20010215)46:3<220::AID-NEU1004>3.0.CO;2-P
81. Ohkubo Y, Uchida AO, Shin D, Partanen J, Vaccarino FM. Fibroblast growth factor receptor 1 is required for the proliferation of hippocampal progenitor cells and for hippocampal growth in mouse. J Neurosci (2004) 24:6057-69. doi:10.1523/JNEUROSCI.1140-04.2004
82. Graham BM, Richardson R. Early-life exposure to fibroblast growth factor-2 facilitates context-dependent long-term memory in developing rats. Behav Neurosci (2010) 124:337. doi:10.1037/a0019582
83. Rudy JW, Morledge P. Ontogeny of contextual fear conditioning in rats: implications for consolidation, infantile amnesia, and hippocampal system function. Behav Neurosci (1994) 108:227-34. doi:10.1037/0735-7044.108.2.227
84. Molteni R, Fumagalli F, Magnaghi V, Roceri M, Gennarelli M, Racagni G, et al. Modulation of fibroblast growth factor-2 by stress and corticosteroids: from developmental events to adult brain plasticity. Brain Res Rev (2001) 37:249-58. doi:10.1016/S0165-0173(01)00128-X
85. Anderson KJ, Dam D, Lee S, Cotman CW. Basic fibroblast growth factor prevents death of lesioned cholinergic neurons in vivo. Nature (1988) 332:360-1. doi:10.1038/332360a0
86. Gomez-Pinilla F, Vu L, Cotman CW. Regulation of astrocyte proliferation by FGF-2 and heparan sulfate in vivo. J Neurosci (1995) 15:2021-9.
87. Bland ST, Schmid MJ, Greenwood BN, Watkins LR, Maier SF. Behavioral control of the stressor modulates stress-induced changes in neurogenesis and fibroblast growth factor-2. Neuroreport (2006) 17:593-7. doi:10.1097/00001756-200604240-00008
88. Bland ST, Tamlyn JP, Barrientos RM, Greenwood BN, Watkins LR, Campeau S, et al. Expression of fibroblast growth factor-2 and brain-derived neurotrophic factor mRNA in the medial prefrontal cortex and hippocampus after uncontrollable or controllable stress. Neuroscience (2007) 144:1219-28. doi:10.1016/j.neuroscience.2006.11.026
89. Turner CA, Calvo N, Frost DO, Akil H, Watson SJ. The fibroblast growth factor system is downregulated following social defeat. Neurosci Lett (2008) 430:147-50. doi:10.1016/j.neulet.2007.10.041
90. Fagiolini M, Hensch TK. Inhibitory threshold for critical-period activation in primary visual cortex. Nature (2000) 404:183-6. doi:10.1038/35004582
91. Hensch TK. Critical period mechanisms in developing visual cortex. Curr Top Dev Biol (2005) 69:215-37. doi:10.1016/S0070-2153(05)69008-4
92. Levelt CN, Hu¨bener M. Critical-period plasticity in the visual cortex. Neuroscience (2012) 35:309-30.
93. Gogolla N, LeBlanc JJ, Quast KB, Su¨dhof TC, Fagiolini M, Hensch TK. Common circuit defect of excitatory-inhibitory balance in mouse models of autism. J Neurodev Disord (2009) 1:172-81. doi:10.1007/s11689-009-9023-x
94. LeBlanc JJ, Fagiolini M. Autism: a "critical period" disorder? Neural Plast (2011) 2011:921680. doi:10.1155/2011/921680
95. Lupien SJ, McEwen BS, Gunnar MR, Heim C. Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci (2009) 10:434-45. doi:10.1038/nrn2639
96. Banks MS, Aslin RN, Letson RD. Sensitive period for the development of human binocular vision. Science (1975) 190:675-7. doi:10.1126/science.1188363
97. Harrison RV, Gordon KA, Mount RJ. Is there a critical period for cochlear implantation in congenitally deaf children? Analyses of hearing and speech perception performance after implantation. Dev Psychobiol (2005) 46:252-61. doi:10.1002/dev.20052
98. Johnson JS, Newport EL. Critical period effects on universal properties of language: the status of subjacency in the acquisition of a second language. Cognition (1991) 39:215-58. doi:10.1016/0010-0277(91)90054-8
99. Birdsong D, Molis M. On the evidence for maturational constraints in second-language acquisition. J Mem Lang (2001) 44:235-49. doi:10.1006/jmla.2000.2750
100. Bos K, Zeanah CH, Fox NA, Drury SS, McLaughlin KA, Nelson CA. Psychiatric outcomes in young children with a history of institutionalization. Harv Rev Psychiatry (2011) 19:15-24. doi:10.3109/10673229.2011.549773
101. Fox K. A critical period for experience-dependent synaptic plasticity in rat barrel cortex. J Neurosci (1992) 12:1826-38.
102. Nelson DA, Marler P, Palleroni A. A comparative approach to vocal learning: intraspecific variation in the learning process. Anim Behav (1995) 50:83-97. doi:10.1006/anbe.1995.0223
103. Doupe AJ, Kuhl PK. Birdsong and human speech: common themes and mechanisms. Annu Rev Neurosci (1999) 22:567-631. doi:10.1146/annurev.neuro.22.1.567
104. Balmer TS, Carels VM, Frisch JL, Nick TA. Modulation of perineuronal nets and parvalbumin with developmental song learning. J Neurosci (2009) 29:12878-85. doi:10.1523/JNEUROSCI.2974-09.2009
105. Nowicka D, Soulsby S, Skangiel-Kramska J, Glazewski S. Parvalbumin-containing neurons, perineuronal nets and experience-dependent plasticity in murine barrel cortex. Eur J Neurosci (2009) 30:2053-63. doi:10.1111/j.1460-9568.2009.06996.x
106. Hubel DH, Wiesel TN. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J Physiol (1962) 160:106-54.
107. Wiesel TN, Hubel DH. Single-cell responses in striate cortex of kittens deprived of vision in one eye. J Neurophysiol (1963) 26:1013-7.
108. Hensch TK. Critical period plasticity in local cortical circuits. Nat Rev Neurosci (2005) 6:877-88. doi:10.1038/nrn1787
109. Hensch TK, Fagiolini M, Mataga N, Stryker MP, Baekkeskov S, Kash SF. Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science (1998) 282:1504-8. doi:10.1126/science.282.5393.1504
110. Hanover JL, Huang ZJ, Tonegawa S, Stryker MP. Brain-derived neurotrophic factor overexpression induces precocious critical period in mouse visual cortex. J Neurosci (1999) 19:RC40.
111. Huang ZJ, Kirkwood A, Pizzorusso T, Porciatti V, Morales B, Bear MF, et al. BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell (1999) 98:739-55. doi:10.1016/S0092-8674(00)81509-3
112. Pizzorusso T, Medini P, Berardi N, Chierzi S, Fawcett JW, Maffei L. Reactivation of ocular dominance plasticity in the adult visual cortex. Science (2002) 298:1248-51. doi:10.1126/science.1072699
113. McGee AW, Yang Y, Fischer QS, Daw NW, Strittmatter SM. Experience-driven plasticity of visual cortex limited by myelin and Nogo receptor. Science (2005) 309:2222-6. doi:10.1126/science.1114362
114. Chklovskii DB, Mel B, Svoboda K. Cortical rewiring and information storage. Nature (2004) 431:782-8. doi:10.1038/nature03012
115. GrandPré T, Li S, Strittmatter SM. Nogo-66 receptor antagonist peptide promotes axonal regeneration. Nature (2002) 417:547-51. doi:10.1038/417547a
116. Pham TA, Impey S, Storm DR, Stryker MP. CRE-mediated gene transcription in neocortical neuronal plasticity during the developmental critical period. Neuron (1999) 22:63-72. doi:10.1016/S0896-6273(00)80679-0
117. Pham TA, Graham SJ, Suzuki S, Barco A, Kandel ER, Gordon B, et al. A semi-persistent adult ocular dominance plasticity in visual cortex is stabilized by activated CREB. Learn Mem (2004) 11:738-47. doi:10.1101/lm.75304
118. Beaver CJ, Ji Q, Fischer QS, Daw NW. Cyclic AMP-dependent protein kinase mediates ocular dominance shifts in cat visual cortex. Nat Neurosci (2001) 4:159-63. doi:10.1038/83985
119. Vo N, Klein ME, Varlamova O, Keller DM, Yamamoto T, Goodman RH, et al. A cAMP-response element binding protein-induced microRNA regulates neuronal morphogenesis. Proc Natl Acad Sci U S A (2005) 102:16426-31. doi:10.1073/pnas.0508448102
120. Tognini P, Putignano E, Coatti A, Pizzorusso T. Experience-dependent expression of miR-132 regulates ocular dominance plasticity. Nat Neurosci (2011) 14:1237-9. doi:10.1038/nn.2920
121. Galanopoulou AS. Dissociated gender-specific effects of recurrent seizures on GABA signaling in CA1 pyramidal neurons: role of GABAA receptors. J Neurosci (2008) 28:1557-67. doi:10.1523/JNEUROSCI.5180-07.2008
122. Roceri M, Cirulli F, Pessina C, Peretto P, Racagni G, Riva MA. Postnatal repeated maternal deprivation produces age-dependent changes of brain-derived neurotrophic factor expression in selected rat brain regions. Biol Psychiatry (2004) 55:708-14. doi:10.1016/j.biopsych.2003.12.011
123. Kikusui T, Kiyokawa Y, Mori Y. Deprivation of mother-pup interaction by early weaning alters myelin formation in male, but not female, ICR mice. Brain Res (2007) 1133:115-22. doi:10.1016/j.brainres.2006.11.031
124. Ono M, Kikusui T, Sasaki N, Ichikawa M, Mori Y, Murakami-Murofushi K. Early weaning induces anxiety and precocious myelination in the anterior part of the basolateral amygdala of male Balb/c mice. Neuroscience (2008) 156:1103-10. doi:10.1016/j.neuroscience.2008.07.078
125. Chan JR, Phillips LJ, Glaser M. Glucocorticoids and progestins signal the initiation and enhance the rate of myelin formation. Proc Natl Acad Sci U S A (1998) 95:10459-64. doi:10.1073/pnas.95.18.10459
126. Bansal R, Miyake H, Nakamura I, Eto H, Gotoh A, Fujisawa M, et al. Fibroblast growth factors and their receptors in oligodendrocyte development: implications for demyelination and remyelination. Dev Neurosci (2002) 24:35-46. doi:10.1159/000064944
127. Furusho M, Dupree JL, Nave K-A, Bansal R. Fibroblast growth factor receptor signaling in oligodendrocytes regulates myelin sheath thickness. J Neurosci (2012) 32:6631-41. doi:10.1523/JNEUROSCI.6005-11.2012
128. Sung JY, Shin SW, Ahn YS, Chung KC. Basic fibroblast growth factor-induced activation of novel CREB kinase during the differentiation of immortalized hippocampal cells. J Biol Chem (2001) 276:13858-66.
129. Peltier J, O'Neill A, Schaffer DV. PI3K/Akt and CREB regulate adult neural hippocampal progenitor proliferation and differentiation. Dev Neurobiol (2007) 67:1348-61. doi:10.1002/dneu.20506
130. Uchida S, Hara K, Kobayashi A, Funato H, Hobara T, Otsuki K, et al. 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 (2010) 30:15007-18. doi:10.1523/JNEUROSCI.1436-10.2010
131. Numakawa T, Yamamoto N, Chiba S, Richards M, Ooshima Y, Kishi S, et al. Growth factors stimulate expression of neuronal and glial miR-132. Neurosci Lett (2011) 505:242-7. doi:10.1016/j.neulet.2011.10.025
132. Yehuda R, Engel SM, Brand SR, Seckl J, Marcus SM, Berkowitz GS. Transgenerational effects of posttraumatic stress disorder in babies of mothers exposed to the World Trade Center attacks during pregnancy. J Clin Endocrinol Metab (2005) 90:4115-8. doi:10.1210/jc.2005-0550
133. Stein MB, Chartier MJ, Lizak MV, Jang KL. Familial aggregation of anxiety-related quantitative traits in generalized social phobia: clues to understanding "disorder" heritability? Am J Med Genet (2001) 105:79-83. doi:10.1002/1096-8628(20010108)105:1<79:AID-AJMG1067>3.3.CO;2-6
134. Stein MB, Jang KL, Livesley W. Heritability of social anxiety-related concerns and personality characteristics: a twin study. J Nerv Ment Dis (2002) 190:219-24. doi:10.1097/00005053-200204000-00002
135. Distel MA, Vink JM, Willemsen G, Middeldorp CM, Merckelbach HLGJ, Boomsma DI. Heritability of self-reported phobic fear. Behav Genet (2008) 38:24-33. doi:10.1007/s10519-007-9182-z
136. Kim HK, Capaldi DM, Pears KC, Kerr DCR, Owen LD. Intergenerational transmission of internalising and externalising behaviours across three generations: gender-specific pathways. Crim Behav Ment Health (2009) 19:125-41. doi:10.1002/cbm.708
137. Roth TL, Lubin FD, Funk AJ, Sweatt JD. Lasting epigenetic influence of early-life adversity on the BDNF gene. Biol Psychiatry (2009) 65:760-9. doi:10.1016/j.biopsych.2008.11.028
138. Franklin TB, Russig H, Weiss IC, Gra¨ffJ, Linder N, Michalon A, et al. Epigenetic transmission of the impact of early stress across generations. Biol Psychiatry (2010) 68:408-15. doi:10.1016/j.biopsych.2010.05.036
139. Dietz DM, LaPlant Q, Watts EL, Hodes GE, Russo SJ, Feng J, et al. Paternal transmission of stress-induced pathologies. Biol Psychiatry (2011) 70:408-14. doi:10.1016/j.biopsych.2011.05.005
140. Weiss IC, Franklin TB, Vizi S, Mansuy IM. Inheritable effect of unpredictable maternal separation on behavioral responses in mice. Front Behav Neurosci (2011) 5:3. doi:10.3389/fnbeh.2011.00003
141. Champagne FA. Epigenetic mechanisms and the transgenerational effects of maternal care. Front Neuroendocrinol (2008) 29:386-97. doi:10.1016/j.yfrne.2008.03.003
142. Curley JP, Mashoodh R. Parent-of-origin and trans-generational germline influences on behavioral development: the interacting roles of mothers, fathers, and grandparents. Dev Psychobiol (2010) 52:312-30. doi:10.1002/dev.20430
143. Rajasethupathy P, Fiumara F, Sheridan R, Betel D, Puthanveettil SV, Russo JJ, et al. Characterization of small RNAs in aplysia reveals a role for miR-124 in constraining synaptic plasticity through CREB. Neuron (2009) 63:803-17. doi:10.1016/j.neuron.2009.05.029
144. Grandjean V, Gounon P, Wagner N, Martin L, Wagner KD, Bernex F, et al. The miR-124-Sox9 paramutation: RNA-mediated epigenetic control of embryonic and adult growth. Development (2009) 136:3647-55. doi:10.1242/dev.041061
145. Kessler RC, McLaughlin KA, Green JG, Gruber MJ, Sampson NA, Zaslavsky AM, et al. Childhood adversities and adult psychopathology in the WHO World Mental Health Surveys. Br J Psychiatry (2010) 197:378-85. doi:10.1192/bjp.bp.110.080499
146. Glaser J-P, van Os J, Portegijs P, Myin-Germeys I. Childhood trauma and emotional reactivity to daily life stress in adult frequent attenders of general practitioners. J Psychosom Res (2006) 61:229. doi:10.1016/j.jpsychores.2006.04.014
147. McLaughlin KA, Green JG, Gruber MJ, Sampson NA, Zaslavsky AM, Kessler RC. Childhood adversities and adult psychiatric disorders in the national comorbidity survey replication II: associations with persistence of DSM-IV disorders. Arch Gen Psychiatry (2010) 67:124-32. doi:10.1001/archgenpsychiatry.2009.187
148. Binder EB, Bradley RG, Liu W, Epstein MP, Deveau TC, Mercer KB, et al. Association of FKBP5 polymorphisms and childhood abuse with risk of posttraumatic stress disorder symptoms in adults. JAMA (2008) 299:1291-305. doi:10.1001/jama.299.11.1291
149. Bradley RG, Binder EB, Epstein MP, Tang Y, Nair HP, Liu W, et al. Influence of child abuse on adult depression: moderation by the corticotropin-releasing hormone receptor gene. Arch Gen Psychiatry (2008) 65:190. doi:10.1001/archgenpsychiatry.2007.26
150. Graham BM, Richardson R. Acute systemic fibroblast growth factor-2 enhances long-term extinction of fear and reduces reinstatement in rats. Neuropsychopharmacology (2009) 34:1875-82. doi:10.1038/npp.2009.14
151. Graham BM, Richardson R. Fibroblast growth factor-2 enhances extinction and reduces renewal of conditioned fear. Neuropsychopharmacology (2010) 35:1348-55. doi:10.1038/npp.2010.3
152. Graham BM, Richardson R. Fibroblast growth factor-2 alters the nature of extinction. Learn Mem (2011) 18:80-4. doi:10.1101/lm.2006511
153. Graham BM, Richardson R. Intraamygdala infusion of fibroblast growth factor 2 enhances extinction and reduces renewal and reinstatement in adult rats. J Neurosci (2011) 31:14151-7. doi:10.1523/JNEUROSCI.3014-11.2011
154. Langton JM, Richardson R. D-cycloserine facilitates extinction the first time but not the second time: an examination of the role of NMDA across the course of repeated extinction sessions. Neuropsychopharmacology (2008) 33:3096-102. doi:10.1038/npp
155. Laurent V, Marchand AR, Westbrook RF. The basolateral amygdala is necessary for learning but not relearning extinction of context conditioned fear. Learn Mem (2008) 15:304-14. doi:10.1101/lm.1080108
156. Chan WYM, McNally GP. Conditioned stimulus familiarity determines effects of MK-801 on fear extinction. Behav Neurosci (2009) 123:303. doi:10.1037/a0014988
157. Langton JM, Richardson R. The temporal specificity of the switch from NMDAr-dependent extinction to NMDAr-independent re-extinction. Behav Brain Res (2010) 208:646-9. doi:10.1016/j.bbr.2009.12.018
158. Kim JH, Richardson R. Extinction in preweanling rats does not involve NMDA receptors. Neurobiol Learn Mem (2010) 94:176-82. doi:10.1016/j.nlm.2010.05.004
159. Karpova NN, Pickenhagen A, Lindholm J, Tiraboschi E, Kulesskaya N, Ágústsdóttir A, et al. Fear erasure in mice
160. Pampallona S, Bollini P, Tibaldi G, Kupelnick B, Munizza C. Combined pharmacotherapy and psychological treatment for depression: a systematic review. Arch Gen Psychiatry (2004) 61:714. doi:10.1001/archpsyc.61.7.714
161. Fergusson DM, Horwood L, Lynskey MT. Childhood sexual abuse and psychiatric disorder in young adulthood: II. Psychiatric outcomes of childhood sexual abuse. J Am Acad Child Adolesc Psychiatry (1996) 35:1365-74. doi:10.1097/00004583-199610000-00023
162. Nikulina V, Widom CS, Czaja S. The role of childhood neglect and childhood poverty in predicting mental health, academic achievement and crime in adulthood. Am J Community Psychol (2011) 48:309-21. doi:10.1007/s10464-010-9385-y
163. Milad MR, Rauch SL, Pitman RK, Quirk GJ. Fear extinction in rats: implications for human brain imaging and anxiety disorders. Biol Psychol (2006) 73:61-71. doi:10.1016/j.biopsycho.2006.01.008
164. Milad MR, Quirk GJ. Fear extinction as a model for translational neuroscience: ten years of progress. Annu Rev Psychol (2012) 63:129-51. doi:10.1146/annurev.psych.121208.131631
165. Jacobs WJ, Nadel L. Stress-induced recovery of fears and phobias. Psychol Rev (1985) 92:512-31. doi:10.1037/0033-295X.92.4.512
166. Jacobs WJ, Nadel L. The first panic attack: a neurobiological theory. Can J Exp Psychol (1999) 53:92-107. doi:10.1037/h0087302
167. Mineka S, Zinbarg R. A contemporary learning theory perspective on the etiology of anxiety disorders: it's not what you thought it was. Am Psychol (2006) 61:10-26. doi:10.1037/0003-066X.61.1.10
168. Mineka S, Oehlberg K. The relevance of recent developments in classical conditioning to understanding the etiology and maintenance of anxiety disorders. Acta Psychol (Amst) (2008) 127:567-80. doi:10.1016/j.actpsy.2007.11.007
169. Zorawski M, Cook CA, Kuhn CM, LaBar KS. Sex, stress, and fear: individual differences in conditioned learning. Cogn Affect Behav Neurosci (2005) 5:191-201. doi:10.3758/CABN.5.2.191
170. Guthrie RM, Bryant RA. Extinction learning before trauma and subsequent posttraumatic stress. Psychosom Med (2006) 68:307-11. doi:10.1097/01.psy.0000208629.67653.cc