A window of vulnerability: Impaired fear extinction in adolescence

Neurobiology of Learning and Memory

Volumn 113, Issue , 2014, Pages 90-100

  Baker, Kathryn D ^a   Den, Miriam L ^a   Graham, Bronwyn M ^a   Richardson, Rick ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Adolescence; Extinction; Fear; Functional connectivity; Stress

Indexed keywords

ADOLESCENCE; ADOLESCENT BEHAVIOR; AGE DISTRIBUTION; AMYGDALOID NUCLEUS; ASSOCIATION; BRAIN FUNCTION; CHRONIC STRESS; DEVELOPMENTAL STAGE; EARLY LIFE STRESS; FEAR; HUMAN; MEMORY CONSOLIDATION; NEUROBIOLOGY; NONHUMAN; PREFRONTAL CORTEX; REINFORCEMENT; REVIEW; RODENT; ADOLESCENT; ADOLESCENT DEVELOPMENT; ANIMAL; GROWTH, DEVELOPMENT AND AGING; MENTAL STRESS; PATHOPHYSIOLOGY; PHYSIOLOGY;

ADOLESCENT; ADOLESCENT DEVELOPMENT; AMYGDALA; ANIMALS; EXTINCTION, PSYCHOLOGICAL; FEAR; HUMANS; PREFRONTAL CORTEX; STRESS, PSYCHOLOGICAL;

EID: 84902074694     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2013.10.009     Document Type: Review

References (105)

1. Baker K.D., McNally G.P., Richardson R. d-cycloserine does not facilitate fear extinction by reducing conditioned stimulus processing or promoting conditioned inhibition to contextual cues. Learning & Memory 2012, 19:461-469.
2. Baker K.D., McNally G.P., Richardson R. Memory retrieval before or after extinction reduces recovery of fear in adolescent rats. Learning & Memory 2013, 20:467-473.
3. Barha C.K., Brummelte S., Lieblich S.E., Galea L.A. Chronic restraint stress in adolescence differentially influences hypothalamic-pituitary-adrenal axis function and adult hippocampal neurogenesis in male and female rats. Hippocampus 2011, 21:1216-1227.
4. Bath K.G., Chuang J., Spencer-Segal J.L., Amso D., Altemus M., McEwen B.S., Lee F.S. Variant brain-derived neurotrophic factor (Valine66Methionine) polymorphism contributes to developmental and estrous stage-specific expression of anxiety-like behavior in female mice. Biological Psychiatry 2012, 72:499-504.
5. Brasser S.M., Spear N.E. Contextual conditioning in infants, but not older animals, is facilitated by CS conditioning. Neurobiology of Learning and Memory 2004, 81:46-59.
6. Broadwater M., Spear L.P. Age differences in fear retention and extinction in male Sprague-Dawley rats: Effects of ethanol challenge during conditioning. Behavioural Brain Research 2013, 252:377-387.
7. Brückner G., Brauer K., Härtig W., Wolff J.R., Rickmann M.J., Derouiche A., et al. Perineuronal nets provide a polyanionic, glia-associated form of microenvironment around certain neurons in many parts of the rat brain. Glia 1993, 8:183-200.
8. 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, 15:671-679.
9. Casey B.J., Duhoux S., Cohen M.M. Adolescence: What do transmission, transition, and translation have to do with it?. Neuron 2010, 67:749-760.
10. Casey B.J., Getz S., Galvan A. The adolescent brain. Developmental Review 2008, 28:62-77.
11. Casey B.J., Jones R.M., Levita L., Libby V., Pattwell S.S., Ruberry E.J., et al. The storm and stress of adolescence: Insights from human imaging and mouse genetics. Developmental Psychobiology 2010, 52:225-235.
12. Celio M.R., Blumcke I. Perineuronal nets - A specialized form of extracellular matrix in the adult nervous system. Brain Research Reviews 1994, 19:128-145.
13. Clem R.L., Huganir R.L. Calcium-permeable AMPA receptor dynamics mediate fear memory erasure. Science 2010, 330:1108-1112.
14. Cunningham M.G., Bhattacharyya S., Benes F.M. Increasing interaction of amygdalar afferents with GABAergic interneurons between birth and adulthood. Cerebral Cortex 2008, 18:1529-1535.
15. de Kleine R.A., Hendriks G.-J., Kusters W.J.C., Broekman T.G., van Minnen A. A randomized placebo-controlled trial of d-cycloserine to enhance exposure therapy for posttraumatic stress disorder. Biological Psychiatry 2012, 71:962-968.
16. Den M.L., Richardson R. Enhanced sensitivity to learning fearful associations during adolescence. Neurobiology of Learning and Memory 2013, 104:92-102.
17. Eiland L., Ramroop J., Hill M.N., Manley J., McEwen B.S. Chronic juvenile stress produces corticolimbic dendritic architectural remodeling and modulates emotional behavior in male and female rats. Psychoneuroendocrinology 2012, 37:39-47.
18. Etkin A., Wager T.D. Functional neuroimaging of anxiety: A meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. The American Journal of Psychiatry 2007, 164:1476-1488.
19. Fani N., Tone E.B., Phifer J., Norrholm S.D., Bradley B., Ressler K.J., et al. Attention bias toward threat is associated with exaggerated fear expression and impaired extinction in PTSD. Psychological Medicine 2012, 42:533-543.
20. Flavell C.R., Barber D.J., Lee J.L.C. Behavioural memory reconsolidation of food and fear memories. Nature Communications 2011, 2:504.
21. Foilb A.R., Lui P., Romeo R.D. The transformation of hormonal stress responses throughout puberty and adolescence. Journal of Endocrinology 2011, 210:391-398.
22. Foy M.R., Stanton M.E., Levine S., Thompson R.F. Behavioral stress impairs long-term potentiation in rodent hippocampus. Behavioral Neural Biology 1987, 48:138-149.
23. Gee D.G., Humphreys K.L., Flannery J., Goff B., Telzer E.H., Shapiro M., et al. A developmental shift from positive to negative connectivity in human amygdala-prefrontal circuitry. The Journal of Neuroscience 2013, 33:4584-4593.
24. Giamanco K.A., Matthews R.T. Deconstructing the perineuronal net: Cellular contributions and molecular composition of the neuronal extracellular matrix. Neuroscience 2012, 218:367-384.
25. Giedd J.N., Rapoport J.L. Structural MRI of pediatric brain development: What have we learned and where are we going?. Neuron 2010, 67:728-734.
26. Giedd J.N., Vaituzis A.C., Hamburger S.D., Lange N., Rajapakse J.C., Kaysen D., et al. Quantitative MRI of the temporal lobe, amygdala, and hippocampus in normal human development: Ages 4-18years. The Journal of Comparative Neurology 1996, 366:223-230.
27. Gogolla N., Caroni P., Lüthi A., Herry C. Perineuronal nets protect fear memories from erasure. Science 2009, 325:1258-1261.
28. Graham B.M., Langton J.M., Richardson R. Pharmacological enhancement of fear reduction: Preclinical models. British Journal of Pharmacology 2011, 164:1230-1247.
29. Graham B.M., Milad M.R. Blockade of estrogen by hormonal contraceptives impairs fear extinction in female rats and women. Biological Psychiatry 2013, 73:371-378.
30. Guastella A.J., Richardson R., Lovibond P.F., Rapee R.M., Gaston J.E., Mitchell P., et al. A randomized controlled trial of d-cycloserine enhancement of exposure therapy for social anxiety disorder. Biological Psychiatry 2008, 63:544-549.
31. Gunnar M.R., Wewerka S., Frenn K., Long J.D., Griggs C. Developmental changes in hypothalamus-pituitary-adrenal activity over the transition to adolescence: Normative changes and associations with puberty. Development and Psychopathology 2009, 21:69-85.
32. Gupta S.C., Hillman B.G., Prakash A., Ugale R.R., Stairs D.J., Dravid S.M. Effect of d-cycloserine in conjunction with fear extinction training on extracellular signal-regulated kinase activation in the medial prefrontal cortex and amygdala in rat. European Journal of Neuroscience 2013, 37:1811-1822.
33. Guyer A.E., Monk C.S., McClure-Tone E.B., Nelson E.E., Roberson-Nay R., Adler A.D., et al. A developmental examination of amygdala response to facial expressions. Journal of Cognitive Neuroscience 2008, 20:1565-1582.
34. Gyawali S., Subaran R., Weissman M.M., Hershkowitz D., McKenna M.C., Talati A., et al. Association of a polyadenylation polymorphism in the serotonin transporter and panic disorder. Biological Psychiatry 2010, 67:331-338.
35. Haddad A.D.M., Lissek S., Pine D.S., Lau J.Y.F. How do social fears in adolescence develop? Fear conditioning shapes attention orienting to social threat cues. Cognition & Emotion 2011, 25:1139-1147.
36. 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. Biological Psychiatry 2008, 63:927-934.
37. Hartley C.A., McKenna M.C., Salman R., Holmes A., Casey B.J., Phelps E.A., Glatt C.E. Serotonin transporter polyadenylation polymorphism modulates the retention of fear extinction memory. Proceedings of the National Academy of Sciences 2012, 3:5493-5498.
38. Hefner K., Holmes A. Ontogeny of fear-, anxiety- and depression-related behavior across adolescence in C57BL/6J mice. Behavioural Brain Research 2007, 176:210-215.
39. Hofmann S.G., Meuret A.E., Smits J.A.J., Simon N.M., Pollack M.H., Eisenmenger K., et al. Augmentation of exposure therapy with d-cycloserine for social anxiety disorder. Archives of General Psychiatry 2006, 63:298-304.
40. Hofmann S.G., Wu J.Q., Boettcher H. d-cycloserine as an augmentation strategy for cognitive behavioral therapy of anxiety disorders. Biology of Mood & Anxiety Disorders 2013, 3:11.
41. Holsboer F., Ising M. Stress hormone regulation: Biological role and translation into therapy. Annual Review of Psychology 2010, 61:81-109.
42. Holt D.J., Coombs G., Zeidan M.A., Goff D.C., Milad M.R. Failure of neural responses to safety cues in schizophrenia. Archives of General Psychiatry 2012, 69:893-903.
43. Hu S., Pruessner J.C., Coupé P., Collins D.L. Volumetric analysis of medial temporal lobe structures in brain development from childhood to adolescence. NeuroImage 2013, 74:276-287.
44. Jovanovic T., Ely T., Fani N., Glover E.M., Gutman D., Tone E.B., et al. Reduced neural activation during an inhibition task is associated with impaired fear inhibition in a traumatized civilian sample. Cortex 2013, 49:1884-1891.
45. Kessler R.C., Amminger G.P., Aguilar-Gaxiola S., Alonso J., Lee S., Ustun T.B. Age of onset of mental disorders: A review of recent literature. Current Opinion in Psychiatry 2007, 20:359-364.
46. Kessler R.C., Avenevoli S., Costello E.J., Georgiades K., Green J.G., Gruber M.J., et al. Prevalence, persistence, and sociodemographic correlates of DSM-IV disorders in the National Comorbidity Survey Replication Adolescent Supplement. Archives of General Psychiatry 2012, 69:372-380.
47. Kim J.H., Li S., Richardson R. Immunohistochemical analyses of long-term extinction of conditioned fear in adolescent rats. Cerebral Cortex 2011, 21:530-538.
48. Kim J.H., Richardson R. New findings on extinction of conditioned fear early in development: Theoretical and clinical implications. Biological Psychiatry 2010, 67:297-303.
49. 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. Archives of General Psychiatry 2003, 60:709-717.
50. Koenig J.I., Walker C.D., Romeo D., Lupien S.J. Effects of stress across the lifespan. Stress 2011, 14:475-480.
51. Langton J.M., 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, 33:3096-3102.
52. Lau J.Y., Britton J.C., Nelson E.E., Angold A., Ernst M., Goldwin M., et al. Distinct neural signatures of threat learning in adolescents and adults. Proceedings of the National Academy of Sciences 2011, 108:4500-4505.
53. Lau J.Y.F., Lissek S., Nelson E.E., Lee Y., Roberson-Nay R., Poeth K., et al. Fear conditioning in adolescents with anxiety disorders: Results from a novel experimental paradigm. Journal of the American Academy of Child & Adolescent Psychiatry 2008, 47:94-102.
54. Ledgerwood L., Richardson R., Cranney J. Effects of d-cycloserine on extinction of conditioned freezing. Behavioral Neuroscience 2003, 117:341-349.
55. Lissek S., Powers A.S., McClure E.B., Phelps E.A., Woldehawariat G., Grillon C., Pine D.S. Classical fear conditioning in the anxiety disorders: a meta-analysis. Behaviour Research and Therapy 2005, 43:1391-1424.
56. Lui P., Padow V.A., Franco D., Hall B.S., Park B., Klein Z.A., et al. Divergent stress-induced neuroendocrine and behavioral responses prior to puberty. Physiology & Behavior 2012, 107:104-111.
57. Luine V., Villegas M., Martinez C., McEwen B.S. Repeated stress causes reversible impairments of spatial memory performance. Brain Research 1994, 639:167-170.
58. Lupien S.J., McEwen B.S., Gunnar M.R., Heim C. Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nature Reviews Neuroscience 2009, 10:434-445.
59. Mackintosh N.J. A theory of attention: Variations in the associability of stimuli with reinforcement. Psychological Review 1975, 82:276-298.
60. Malter Cohen M., Tottenham N., Casey B.J. Translational developmental studies of stress on brain and behavior: Implications for adolescent mental health and illness?. Neuroscience 2013, 49:53-62.
61. Mauney S.A., Athanas K.M., Pantazopoulos H., Shaskan N., Passeri E., Berretta S., et al. Developmental pattern of perineuronal nets in the human prefrontal cortex and their deficit in schizophrenia. Biological Psychiatry 2013, 74:427-435.
62. McCallum J., Kim J.H., Richardson R. Impaired extinction retention in adolescent rats: Effects of d-cycloserine. Neuropsychopharmacology 2010, 35:2134-2142.
63. McCormick C.M., Mathews I.Z., Thomas C., Waters P. Investigations of HPA function and the enduring consequences of stressors in adolescence in animal models. Brain and Cognition 2010, 72:73-85.
64. McEwen B.S. Physiology and neurobiology of stress and adaptation: Central role of the brain. Physiological Reviews 2007, 87:873-904.
65. McLaughlin K.J., Gomez J.L., Baran S.E., Conrad C.D. The effects of chronic stress on hippocampal morphology and function: An evaluation of chronic restraint paradigms. Brain Research 2007, 1161:56-64.
66. McNally R.J. Mechanisms of exposure therapy: How neuroscience can improve psychological treatments for anxiety disorders. Clinical Psychology Review 2007, 27:750-759.
67. Milad M.R., Quirk G.J. Fear extinction as a model for translational neuroscience: Ten years of progress. Annual Review of Psychology 2012, 63:129-151.
68. Millan E.Z., Milligan-Saville J., McNally G.P. Memory retrieval, extinction, and reinstatement of alcohol seeking. Neurobiology of Learning and Memory 2013, 101:26-32.
69. Monfils M.H., Cowansage K.K., Klann E., LeDoux J.E. Extinction-reconsolidation boundaries: Key to persistent attenuation of fear memories. Science 2009, 324:951-955.
70. Monk C.S., McClure E.B., Nelson E.E., Zarahn E., Bilder R.M., Leibenluft E., et al. Adolescent immaturity in attention-related brain engagement to emotional facial expressions. NeuroImage 2003, 20:420-428.
71. Moore W.E., Pfeifer J.H., Masten C.L., Mazziotta J.C., Iacoboni M., Dapretto M. Facing puberty: Associations between pubertal development and neural responses to affective facial displays. Social Cognitive and Affective Neuroscience 2012, 7:35-43.
72. Morrissey M.D., Mathews I.Z., McCormick C.M. Enduring deficits in contextual and auditory fear conditioning after adolescent, not adult, social instability stress in male rats. Neurobiology of Learning and Memory 2011, 95:46-56.
73. Nave A.M., Tolin D.F., Stevens M.C. Exposure therapy, d-cycloserine, and functional magnetic resonance imaging in patients with snake phobia: A randomized pilot study. Journal of Clinical Psychiatry 2012, 73:1179-1186.
74. Nelson E.E., Leibenluft E., McClure E.B., Pine D.S. The social re-orientation of adolescence: A neuroscience perspective on the process and its relation to psychopathology. Psychological Medicine 2005, 35:163-174.
75. Neufang S., Specht K., Hausmann M., Güntürkün O., Herpertz-Dahlmann B., Fink G.R., et al. Sex differences and the impact of steroid hormones on the developing human brain. Cerebral Cortex 2009, 19:464-473.
76. Neumann D.L., Waters A.M., Westbury H.R. The use of an unpleasant sound as the unconditional stimulus in aversive Pavlovian conditioning experiments that involve children and adolescent participants. Behavior Research Methods 2008, 40:622-625.
77. Pattwell S.S., Duhoux S., Hartley C.A., Johnson D.C., Jing D., Elliott M.D., et al. Altered fear learning across development in both mouse and human. Proceedings of the National Academy of Sciences 2012, 109:16318-16323.
78. Paus T., Keshavan M., Giedd J.N. Why do many psychiatric disorders emerge during adolescence?. Nature Reviews Neuroscience 2008, 9:947-957.
79. Perlman S.B., Pelphrey K.A. Developing connections for affective regulation: Age-related changes in emotional brain connectivity. Journal of Experimental Child Psychology 2011, 108:607-620.
80. Pizzorusso T., Medini P., Berardi N., Chierzi S., Fawcett J.W., Maffei L. Reactivation of ocular dominance plasticity in the adult visual cortex. Science 2002, 298:1248-1251.
81. Qin S., Young C.B., Supekar K., Uddin L.Q., Menon V. Immature integration and segregation of emotion-related brain circuitry in young children. Proceedings of the National Academy of Sciences 2012, 109:7941-7946.
82. Quirk G.J., Mueller D. Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 2008, 33:56-72.
83. Ressler K.J., Rothbaum B.O., Tannenbaum L., Anderson P., Graap K., Zimand E., et al. Cognitive enhancers as adjuncts to psychotherapy: Use of d-cycloserine in phobic individuals to facilitate extinction of fear. Archives of General Psychiatry 2004, 61:1136-1144.
84. Riddle M.C., McKenna M.C., Yoon Y.J., Pattwell S.S., Santos P.M.G., Casey B.J., Glatt C.E. Caloric Restriction Enhances Fear Extinction Learning in Mice. Neuropsychopharmacology 2013, 38:930-937.
85. Romeo R.D. The teenage brain: The stress response and the adolescent brain. Current Directions in Psychological Science 2013, 22:140-145.
86. Romeo R.D., Lee S.J., Chhua N., McPherson C.R., McEwen B.S. Testosterone cannot activate an adult-like stress response in prepubertal male rats. Neuroendocrinology 2004, 79:125-132.
87. Romeo R.D., Lee S.J., McEwen B.S. Differential stress reactivity in intact and ovariectomized prepubertal and adult female rats. Neuroendocrinology 2004, 80:387-393.
88. Roy A.K., Fudge J.L., Kelly C., Perry J.S.A., Daniele T., Carlisi C., et al. Intrinsic functional connectivity of amygdala-based networks in adolescent generalized anxiety disorder. Journal of the American Academy of Child and Adolescent Psychiatry 2013, 52:290-299.
89. Rubinow M.J., Juraska J.M. Neuron and glia numbers in the basolateral nucleus of the amygdala from preweaning through old age in male and female rats: A stereological study. The Journal of Comparative Neurology 2009, 512:717-725.
90. Saul M.L., Helmreich D.L., Callahan L.M., Fudge J.L. Differences in amygdala cell proliferation between adolescent and young adult rats. Developmental Psychobiology 2013.
91. Scherf K.S., Smyth J.M., Delgado M.R. The amygdala: An agent of change in adolescent neural networks. Hormones and Behavior 2013, 64:298-313.
92. Schiller D., Monfils M.H., Raio C.M., Johnson D.C., Ledoux J.E., Phelps E.A. Preventing the return of fear in humans using reconsolidation update mechanisms. Nature 2010, 463:49-53.
93. Soliman F., Glatt C.E., Bath K.G., Levita L., Jones R.M., Pattwell S.S., et al. A genetic variant BDNF polymorphism alters extinction learning in both mouse and human. Science 2010, 327:863-866.
94. Somerville L.H., Jones R.M., Casey B.J. A time of change: Behavioral and neural correlates of adolescent sensitivity to appetitive and aversive environmental cues. Brain and Cognition 2010, 72:124-133.
95. Sousa N., Lukoyanov N.V., Madeira M.D., Almeida O.F.X., Paula-Barbosa M.M. Reorganization of the morphology of hippocampal neurites and synapses after stress-induced damage correlates with behavioral improvement. Neuroscience 2000, 97:253-266.
96. Spear L.P. The adolescent brain and age-related behavioral manifestations. Neuroscience & Biobehavioral Reviews 2000, 24:417-463.
97. Steinberg L. A social neuroscience perspective on adolescent risk-taking. Developmental Review 2008, 28:78-106.
98. Storch E.A., Murphy T.K., Goodman W.K., Geffken G.R., Lewin A.B., Henin A., et al. A preliminary study of d-cycloserine augmentation of cognitive-behavioral therapy in pediatric obsessive-compulsive disorder. Biological Psychiatry 2010, 68:1073-1076.
99. Stroud L.R., Foster E., Papandonatos G.D., Handwerger K., Granger D.A., Kivlighan K.T., et al. Stress response and the adolescent transition: Performance versus peer rejection stressors. Development and Psychopathology 2009, 21:47-68.
100. Sturman D.A., Moghaddam B. The neurobiology of adolescence: Changes in brain architecture, functional dynamics, and behavioral tendencies. Neuroscience & Biobehavioral Reviews 2011, 35:1704-1712.
101. Toledo-Rodriguez M., Sandi C. Stress before puberty exerts a sex- and age-related impact on auditory and contextual fear conditioning in the rat. Neural Plasticity 2007.
102. Van Damme S., Crombez G., Hermans D., Koster E.H.W., Eccleston C. The role of extinction and reinstatement in attentional bias to threat: A conditioning approach. Behaviour Research and Therapy 2006, 44:1555-1563.
103. Walker D.L., Ressler K.J., 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. The Journal of Neuroscience 2002, 22:2343-2351.
104. Watanabe R., Gould E., McEwen B.S. Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Research 1992, 588:341-345.
105. Zhang W., Rosenkranz J.A. Repeated restraint stress enhances cue-elicited conditioned freezing and impairs acquisition of extinction in an age-dependent manner. Behavioural Brain Research 2013, 248:12-24.