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Cited by 121Memory and Neural MechanismsStress Responses and CortisolAnxiety, Depression, Psychometrics, Treatment, Cognitive Processes

The influence of acute stress on the regulation of conditioned fear

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Raio, Candace M., Phelps, Elizabeth A.·2015·Neurobiology of Stress
DOI 10.1016/j.ynstr.2014.11.004PMC PMC4268774
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Abstract

Fear learning and regulation is a prominent model for describing the pathogenesis of anxiety disorders and stress-related psychopathology. Fear expression can be modulated using a number of regulatory strategies, including extinction, cognitive emotion regulation, avoidance strategies and reconsolidation. In this review, we examine research investigating the effects of acute stress and stress hormones on these regulatory techniques. We focus on what is known about the impact of stress on the ability to flexibly regulate fear responses that are acquired through Pavlovian fear conditioning. Our primary aim is to explore the impact of stress on fear regulation in humans. Given this, we focus on techniques where stress has been linked to alterations of fear regulation in humans (extinction and emotion regulation), and briefly discuss other techniques (avoidance and reconsolidation) where the impact of stress or stress hormones have been mainly explored in animal models. These investigations reveal that acute stress may impair the persistent inhibition of fear, presumably by altering prefrontal cortex function. Characterizing the effects of stress on fear regulation is critical for understanding the boundaries within which existing regulation strategies are viable in everyday life and can better inform treatment options for those who suffer from anxiety and stress-related psychopathology.

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  • Exaggerated fear is a core symptom of clinical anxiety and fear responding is closely linked to stress.

    “Exaggerated fear is a core symptom of clinical anxiety and fear responding is closely linked to stress (Maren and Holmes, 2016;McEwen et al., 2016;Raio and Phelps, 2015), which (as described in Sections VI.G. and VII.H.) is tightly intertwined with gut-brain axis function.”

    From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Raio and Phelps, 2015

  • The decrease of Bacteroidetes phylum is related to reduced LPS-binding protein leading to reduced inflammation in BCAA mixture-supplemented mice.

    “The decrease of Bacteroidetes phylum was related to reduced LPS-binding protein leading to reduced inflammation in BCAA mixture -supplemented mice (Raio and Phelps, 2015;Yang et al., 2016).”

    From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Raio and Phelps, 2015

    The paper’s sections on fear circuitry and acute stress discuss amygdala activity and stress hormones, not gut microbiota or BCAA supplementation. Searches for Bacteroidetes, LPS-binding protein, and branched-chain amino acids found no passage addressing the claimed link to inflammation in supplemented mice; the cited copy does not establish or contradict it. (LLM, conf=0.78)

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References 232 · Cited by 121

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  1. Abrari K. Rashidy-Pour A. Semnanian S. Fathollahi Y. Jadid M. Post-training administration of corticosterone enhances consolidation of contextual fear memory and hippocampal long-term potentiation in rats Neurobiol. Learn Mem. 91 3 2009 260 265 19010430
  2. Aerni A. Traber R. Hock C. Roozendaal B. Schelling G. Papassotiropoulos A. Nitsch R.M. Schnyder U. de Quervain D.J. Low-dose cortisol for symptoms of posttraumatic stress disorder Am. J. Psychiatry 161 2004 1488 1490 15285979
  3. Agren T. Engman J. Frick A. Bjorkstrand J. Larsson E.M. Furmark T. Fredrikson M. Disruption of reconsolidation erases a fear memory trace in the human amygdala Science 337 2012 1550 1552 22997340
  4. Akirav I. Maroun M. The role of the medial prefrontal cortex-amygdala circuit in stress effects on the extinction of fear Neural Plast. 2007 30873 17502909 PMC1838961
  5. Amorapanth P. LeDoux J.E. Nader K. Different lateral amygdala outputs mediate reactions and actions elicited by a fear-arousing stimulus Nat. Neurosci. 3 2000 74 79 10607398
  6. Antov M.I. Wolk C. Stockhorst U. Differential impact of the first and second wave of a stress response on subsequent fear conditioning in healthy men Biol. Psychol. 942 2013 456 468 24005063
  7. Antov M.I. Stockhorst U. Stress exposure prior to fear acquisition interacts with estradiol status to alter recall of fear extinction in humans Psychoneuroendocrinology 49 2014 106 118 25080403
  8. Arnsten A.F.T. Goldman-Rakic P.S. Noise stress impairs prefrontal cortical cognitive function in monkeys: evidence for a hyperdopaminergic mechanism Arch. Gen. Psychiatry 55 1998 362 369 9554432
  9. Barrett D. Gonzalez-Lima F. Behavioral effects of metyrapone on Pavlovian extinction Neurosci. Lett. 371 2004 91 96 15519735
  10. Beck A.T. Dozois D.J.A. Cognitive therapy: current status and future directions Annu. Rev. Med. 62 2011 397 409 20690827
  11. Bentz D. Michael T. Willhelm F.H. Hartmann F.R. Kunz S. von Rohr I.R.R. de Quervain D.J.-F. Influence of stress on fear memory processes in an aversive differential conditioning paradigm in humans Psychoneuroendocrinology 38 2013 1186 1197 23333200
  12. Berlau D.J. McGaugh J.L. Enhancement of extinction memory consolidation: The role of the noradrenergic and GABAergic systems within the basolateral amygdala Neurobiol. Learning Mem. 86 2006 123 132 16458544
  13. Berridge C.W. Waterhouse B.D. The locus coeruleusnoradrenergic system: modulation of behavioral state and state-dependent cognitive processes Brain Res. Brain Res. Rev. 42 2003 33 84 12668290
  14. Birnbaum S.G. Gobeske K.T. Auerbach J. Taylor J.R. Arnsten A.F.T. A role for norepinephrine in stress-induced cognitive deficits: alpha-1-adrenoceptor mediation in prefrontal cortex Biol. Psychiatry 46 1999 1266 1274 10560032
  15. Blechert J. Michael T. Vriends N. Margraf J. Wilhelm F.H. Fear conditioning in posttraumatic stress disorder: evidence for delayed extinction of autonomic, experiential, and behavioural responses Behav. Res. Ther. 45 2007 2019 2033 17442266
  16. Bouton M.E. Context and behavioral processes in extinction Learn. Mem. 11 2004 485 494 15466298
  17. Brunet A. Orr S.P. Tremblay J. Robertson K. Nader K. Pitman R.K. Effect of post-retrieval propranolol on psychophysiologic responding during subsequent script-driven traumatic imagery in post-traumatic stress disorder J. Psychiatr. Res. 42 2008 503 506 17588604
  18. Buchel C. Morris J. Dolan R.J. Friston K.J. Brain systems mediating aversive conditioning: an event-related fMRI study Neuron 20 5 1998 947 9957 9620699
  19. 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. 29 2009 8474 8482 19571138 PMC2733220
  20. Bush D.A. Caparosa E.M. Gekker A. LeDoux J.E. Beta-adrenergic receptors in the lateral nucleus of the amygdala contribute to the acquisition but not the consolidation of auditory fear conditioning Front. Behav. Neurosci. 4 2010 1 7 21152344 PMC2998038
  21. Butler A.C. Chapman J.E. Forman E.M. Beck A.T. The empirical status of cognitive-behavioral therapy: a review of meta-analyses Clin. Psychol. Rev. 26 2006 17 31 16199119
  22. Cacioppo J.T. Berntson G.G. Malarkey W.B. Kiecolt-Glaser J.K. Sheridan J.F. Poehlmann K.M. Burleson M.H. Ernst J.M. Hawkley L.C. Glaser R. Autonomic, neuroendocrine, and immune responses to psychological stress: the reactivity hypothesis Ann. N. Y. Acad. Sci. 840 1998 664 673 9629293
  23. Cai W.H. Blundell J. Han J. Greene R.W. Powell C.M. Postreactivation glucocorticoids impair recall of established fear memory J. Neurosci. 26 2006 9560 9566 16971540 PMC3917138
  24. Clem R.L. Huganir R.L. Calcium-permeable AMPA receptor dynamics mediate fear memory erasure Science 1108 2010 1108 1112 21030604 PMC3001394
  25. Clewett D. Schoeke A. Mather M. Amygdala functional connectivity is reduced after the cold pressor task Cogn. Affect Behav. Neurosci. 13 2013 PMC3778131 23645370
  26. Corcoran K.A. Quirk G.J. Activity in prelimbic cortex is necessary for the expression of learned, but not innate, fears J. Neurosci. 27 2007 840 844 17251424 PMC6672908
  27. Craske M.G. Barlow D.H. A Review of the Relationship between Panic and Avoidance vol. 8 1988 667 685
  28. Critchley H.D. Electrodermal responses: what happens in the brain Neuroscientist 8 2002 132 142 11954558
  29. Critchley H.D. Eccles J. Garfinkel S.N. Interaction between cognition, emotion, and the autonomic nervous system Buijs R.M. Swaab D.F. Handbook of Clinical Neurology vol. 117 2013 59 77 (3rd series) 24095116
  30. Debiec J. LeDoux J.E. Disruption of reconsolidation but not consolidation of auditory fear conditioning by noradrenergic blockade in the amygdala Neuroscience 129 2004 267 272 15501585
  31. Debiec J. Bush D.E.A. LeDoux J.E. Noradrenergic enhancement of reconsolidation in the amygdala impairs extinction of conditioned fear in rats—a possible mechanism for the persistence of traumatic memories in PTSD Depress Anxiety 28 2011 186 193 21394851 PMC3590026
  32. de Kloet E.R. Hormones and the stressed brain Ann. N. Y. Acad. Sci. 1018 2004 1 15 15240347
  33. de Quervain D.J. Bentz D. Michael T. Bolt O.C. Wiederhold B.K. Margraf J. Glucocorticoids enhance extinction-based psychotherapy Proc. Natl. Acad. Sci. U. S. A. 108 2011 6621 6625 21444799 PMC3081033
  34. de Quervain D.J. Margraf J. Glucocorticoids for the treatment of post-traumatic stress disorder and phobias: a novel therapeutic approach Eur. J. Pharmacol. 583 2–3 2008 365 371 18275950
  35. Dedovic K. D'Aguiar C. Pruessner J.C. What stress does to your brain: a review of neuroimaging studies Can. J. Psychiatry 54 2009 6 15 19175975
  36. Delgado M.R. Jou R.L. Ledoux J.E. Phelps E.A. Avoiding negative outcomes: tracking the mechanisms of avoidance learning in humans during fear conditioning Front. Behav. Neurosci. 3 2009 1 9 19847311 PMC2762377
  37. Diorio D. Viau V. Meaney M.J. The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic– pituitary–adrenal responses to stress J. Neurosci. 13 9 1993 3839 3847 8396170 PMC6576467
  38. Duncko R. Johnson L. Merikangas K. Grillon C. Working memory performance after acute exposure to the cold pressor stress in healthy volunteers Neurobiol. Learn Mem. 91 2009 377 381 19340949 PMC2696884
  39. Dunsmoor J.E. Bandettini P.A. Knight D.C. Neural correlates of unconditioned response diminution during Pavlovian conditioning Neuroimage 40 2008 811 817 18203622 PMC2712889
  40. Eifert G.H. Forsyth J.P. From normal anxiety to anxiety disorders: an experiential avoidance perspective Woods D.W. Kanter J.W. Understanding Behavior Disorders: a Contemporary Behavioral Perspective 2007 Context Press Reno, NV 81 116
  41. Einarsson E.Ö. Nader K. Involvement of the anterior cingulate cortex in formation, consolidation, and reconsolidation of recent and remote contextual fear memory Learn Mem. 19 2012 449 452 22984282
  42. Ehrlich I. Humeau Y. Ois Grenier F. Cicchi S. Herry C. Luthi A. Amygdala inhibitory circuits and the control of fear memory Neuron 62 2009 757 771 19555645
  43. Elzinga B.M. Roelofs K. Cortisol-induced impairments of working memory require acute sympathetic activation Behav. Neurosci. 119 2005 98 103 15727516
  44. Farrell M.R. Sayed J.A. Underwood A.R. Wellman C.L. Lesion of infralimbic cortex occludes stress effects on retrieval of extinction but not fear conditioning Neurobiol. Learning Mem. 94 2010 240 246 20538067
  45. Ferry B. Roozendaal B. McGaugh J.L. Basolateral amygdala noradrenergic influences on memory storage are mediated by an interaction between beta- and alpha-1-adrenoceptors J. Neurosci. 19 1999 5119 5123 10366644 PMC6782651
  46. Finsterwald C. Alberini C.M. Stress and glucocorticoid receptor-dependent mechanisms in long-term memory: from adaptive responses to psychopathologies Neurobiol. Learn Mem. 112 2014 17 29 24113652 PMC3979509
  47. Gabriel M. Burhans L. Kashef A. Consideration of a unified model of amygdalar associative functions Ann. N. Y. Acad. Sci. 985 2003 206 217 12724160
  48. Gallagher M. Kapp B.S. Musty R.E. Driscoll P.A. Memory formation: evidence for a specific neurochemical system in the amygdala Science 198 1977 423 425 20664
  49. Garcia R. Spennato G. Nilsson-Todd L. Moreau J.L. Deschaux O. Hippocampal low-frequency stimulation and chronic mild stress similarly disrupt fear extinction memory in rats Neurobiol. Learn Mem. 89 2008 560 566 18039585
  50. Goldstein D.S. Catecholamines and stress Endocr. Regul. 37 2 2003 69 80 12932192
  51. Gourley S.L. Kedves A.T. Olausson P. Taylor J.R. A history of corticosterone exposure regulates fear extinction and cortical NR2B, GluR2/3, and BDNF Neuropsychopharmacology 34 2008 707 716 18719621 PMC3679657
  52. Gross J.J. Thompson R.A. Emotion regulation: conceptual foundations Gross J.J. Handbook of Emotion Regulation 2007 Guilford Press New York 3 24
  53. Gross J.J. Emotion regulation: taking stock and moving forward Emotion 13 3 2013 359 365 23527510
  54. Hartley C.A. Phelps E.A. Changing fear: the neurocircuitry of emotion regulation Neuropsychopharmacology 35 2010 136 146 19710632 PMC3055445
  55. Hartley C.A. Fischl B. Phelps E.A. Brain structure correlates of individual differences in the acquisition and inhibition of conditioned fear Cereb. Cort. 21 2011 1954 1962 PMC3155599 21263037
  56. Heatherton T.F. Wagner D.D. Cognitive neuroscience of self-regulation failure Trends Cogn. Sci. 15 2011 132 139 21273114 PMC3062191
  57. Hermans E.J. Henckens M.J.A.G. Joels M. Fernandez G. Dynamic adaptations of large-scale neural networks in response to acute stressors Trends Neurosci. 37 6 2014 304 314 24766931
  58. Herry C. Ciocchi S. Senn V. Demmou L. Muller C. Luthi A. Switching on and off fear by distinct neuronal circuits Nature 454 2008 600 606 18615015
  59. Herry C. Ferraguti F. Singewald N. Letzkus J.J. Ehrlich I. Luthi A. Neuronal circuits of fear extinction Eur. J. Neurosci. 31 2010 599 612 20384807
  60. Hobin J.A. Goosens K.A. Maren S. Context-dependent neuronal activity in the lateral amygdala represents fear memories after extinction J. Neurosci. 23 2003 8410 8416 12968003 PMC2291151
  61. Holmes A. Wellman C.L. Stress-induced prefrontal reorganization and executive dysfunction in rodents Neurosci. Biobehav. Rev. 33 2009 773 783 19111570 PMC2941982
  62. Holmes A. Quirk G. Pharmacological facilitation of extinction and the search for adjunct treatments for anxiety disorders-the case of yohimbine Trends Pharmol. Sci. 31 1 2010 2 7 PMC2883885 20036429
  63. Hui G.K. Figueroa I.R. Poytress B.S. Roozendaal B. McGaugh J.L. Weinberger N.M. Memory enhancement of classical fear conditioning by post-training injections of corticosterone in rats Neurobiol. Learn. Mem. 81 2004 67 74 14670360
  64. Hui I.R. Hui G.K. Roozendaal B. McGaugh J.L. Weinberger N.M. Posttraining handling facilitates memory for auditory-cue fear conditioning in rats Neurobiol. Learn. Mem. 86 2006 160 163 16647281
  65. Indovina I. Robbins T.W. Núñez-Elizalde A.O. Dunn B.D. Bishop S.J. Fear-conditioning mechanisms associated with trait vulnerability to anxiety in humans Neuron 69 2011 563 571 21315265 PMC3047792
  66. Izquierdo A. Wellman C.L. Holmes A. Brief uncontrollable stress causes dendritic retraction in infralimbic cortex and resistance to fear extinction in mice J. Neurosci. 26 2006 5733 5738 16723530 PMC6675270
  67. Jackson E.D. Payne J.D. Nadel L. Jacobs W.J. Stress differentially modulates fear conditioning in healthy men and women Biol. Psychiatry 59 2006 516 522 16213468
  68. Jin X.C. Lu Y.F. Yang X.F. Ma L. Li B.M. Glucocorticoid receptors in the basolateral nucleus of amygdala are required for postreactivation reconsolidation of auditory fear memory Eur. J. Neurosci. 25 2007 3702 3712 17610589
  69. Joels M. Sarabdjitsingh R.A. Karst H. Unraveling the time domains of corticosteroid hormone influences on brain activity: rapid, slow, and chronic modes Pharmacol. Rev. 64 2012 901 938 23023031
  70. Johnstone T. van Reekum C.M. Urry H.L. Kalin N.H. Davidson R.J. Failure to regulate: counterproductive recruitment of top-down prefrontal subcortical circuitry in major depression J. Neurosci. 27 2007 8877 8884 17699669 PMC6672169
  71. Jovanovic T. Norrholm S.D. Neural mechanisms of impaired fear inhibition in posttraumatic stress disorder Front. Behav. Neurosci. 5 2011 44 21845177 PMC3145245
  72. Karst H. Berger S. Turiult M. Tronche F. Schutz G. Joels M. Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone Proc. Natl. Acad. Sci. 102 52 2005 19204 19207 16361444 PMC1323174
  73. Kern S. Glucose metabolic changes in the prefrontal cortex are associated with HPA axis response to a psychosocial stressor Psychoneuroendocrinology 33 2008 517 529 18337016 PMC2601562
  74. Krettek J.E. Price J.L. A description of the amygdaloid complex in the rat and cat with observations on intra-amygdaloid axonal connections J. Comp. Neurol. 178 1978 255 280 627626
  75. Knight D.C. Cheng D.T. Smith C.N. Stein E.A. Helmstetter F.J. Neural substrate mediating human delay and trace fear conditioning J. Neurosci. 24 1 2004 218 228 14715954 PMC6729570
  76. Knight D.C. Waters N.S. King M.K. Bandettini P.A. Learning-related diminuation of unconditioned SCR and fMRI signal responses Neuroimage 49 2010 843 848 19616105 PMC2764808
  77. Knox D. George S.A. Fitzpatrick C.J. Rabinak C.A. Maren S. Liberzon I. Single prolonged stress disrupts retention of extinguished fear in rats Learn. Mem. 19 2012 43 49 22240323 PMC3262971
  78. LaBar K.S. Gatenby J.C. Gore J.C. LeDoux J.E. Phelps E.A. Human amygdala activation during conditioned fear acquisition and extinction: a mixed-trial fMRI study Neuron 20 1998 937 945 9620698
  79. LeDoux J.E. Emotional circuits in the brain Annu Rev. Neurosci. 23 2000 155 184 10845062
  80. LeDoux J.E. Gorman J.M. A call to action: overcoming anxiety through active coping Am. J. Psychiatry 158 2001 1953 1955 11729007
  81. LeDoux J. The amygdala Curr. Biol. 17 2007 R868 R874 17956742
  82. Lee H.J. Berger S.Y. Stiedl O. Spiess J. Kim J.J. Post-training injections of catecholaminergic drugs do not modulate fear conditioning in rats and mice Neurosci. Lett. 303 2001 123 126 11311508
  83. Liang K.C. Juler R.G. McGaugh J.L. Modulating effects of posttraining epinephrine on memory: involvement of the amygdala noradrenergic system Brain Res. 368 1986 125 133 3955350
  84. Liberzon I. Martis B. Neuroimaging studies of emotional responses in PTSD Ann. N. Y. Acad. Sci. 1071 2006 87 109 16891565
  85. Likhtik E. Popa D. Apergis-Schoute J. Fidacaro G.A. ParéD Amygdala intercalated neurons are required for expression of fear extinction Nature 454 2008 642 645 18615014 PMC2528060
  86. Linnman C. Rougemont-Bücking A. Beucke J.C. Zeffiro T.A. Milad M.R. Unconditioned response and functional fear networks in human classical conditioning Behav. Brain Res. 221 2011 237 245 21377494 PMC3092385
  87. Lissek S. Powers A.S. McClure E.B. Phelps E.A. Woldehawariat G. Grillon C. Pine D.S. Behav. Res. Ther. 43 2005 1391 1424 15885654
  88. Luethi M. Meier B. Sandi C. Stress effects on working memory, explicit memory, and implicit memory for neutral and emotional stimuli in healthy men Front. Behav. Neurosci. 15 2009 1 9 PMC2628592 19169362
  89. Lupien S.J. Maheu F. Fiocco A. Schramek T. The effects of stress and stress hormones on human cognition: implications for the field of brain and cognition Brain Cogn. 65 2007 209 237 17466428
  90. Maren S. Neurobiology of Pavlovian fear conditioning Annu Rev. Neurosci. 24 2001 897 931 11520922
  91. Mason S.T. Fibiger H. Noradrenaline, fear and extinction Brain Res. 165 1979 47 56 427586
  92. McCormick D.A. Thompson R.F. Locus coeruleus lesions and resistance to extinction of a classically conditioned response: involvement of the neocortex and hippocampus Brain Res. 245 1982 239 249 7127072
  93. McEwen B.S. De Kloet E.R. Rostene W. Adrenal steroid receptors and actions in the nervous system Physiol. Rev. 66 1986 1121 1188 3532143
  94. McEwen B. Mood disorders and allostatic load Biol. Psychiatry 54 2003 200 207 12893096
  95. McGaugh J.L. McIntyre C.K. Power A.E. Amygdala modulation of memory consolidation: interaction with other brain systems Neurobiol. Learn Mem. 78 3 2002 539 552 12559833
  96. McDonald A.J. Cortical pathways to the mammalian amygdala Prog. Neurobiol. 55 1998 257 332 9643556
  97. McIntyre C.K. Hatfield T. McGaugh J.L. Amygdala norepinephrine levels after training predict inhibitory avoidance retention performance in rats Eur. J. Neurosci. 16 7 2002 1223 1226 12405982
  98. 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. 118 2004 389 394 15113265
  99. Milad M.R. Quirk G.J. Pitman R.K. Orr S.P. Fischl B. Rauch S.L. A role for the human dorsal anterior cingulate cortex in fear expression Biol. Psychiatry 62 2007 1191 1194 17707349
  100. Milad M.R. Pitman R.K. Ellis C.B. Gold A.L. Shin L.S. Lasko N.B. Zeidan M.A. Handwerger K. OrrSP Rauch SL. Neurobiological basis of failure to recall extinction memory in posttraumatic stress disorder Biol. Psychiatry 66 2009 1075 1082 19748076 PMC2787650
  101. Millhouse O.E. The intercalated cells of the amygdala J. Comp. Neurol. 247 1986 246 271 2424941
  102. Miracle A.D. Brace M.F. Huyck K.D. Singler S.A. Wellman C.L. Chronic stress impairs recall of extinction of conditioned fear Neurobiol. Learn Mem. 85 2006 213 218 16337411
  103. Mitra R.M. Sapolsky R.M. Acute corticosterone treatment is sufficient to induce anxiety and amygdaloid dendritic hypertrophy PNAS 105 2008 5573 5578 18391224 PMC2291109
  104. Muigg P. Hetzenauer A. Hauer G. Hauschild M. Gaburro S. Frank E. Landgraf R. Singewal N. Impaired extinction of learned fear in rats selectively bred for high anxiety – evidence of altered neuronal processing in prefrontal-amygdala pathways Eur. J. Neurosci. 28 2008 2299 2309 19019199 PMC2777258
  105. Mueller D. Cahill S.P. Noradrenergic modulation of extinction learning and exposure therapy Behav. Brain Res. 208 2010 1 11 19931568
  106. Mueller D. Porter J.T. Quirk G.J. Noradrenergic signaling in infralimbic cortex increases cell excitability and strengthens memory for fear extinction J. Neurosci. 28 2008 369 375 18184779 PMC6670514
  107. Murphy B.L. Arnsten A.F.T. Goldman-Rakic P.S. Roth R.H. Increased dopamine turnover in the prefrontal cortex impairs spatial working memory performance in rats and monkeys PNAS 93 1996 1325 1329 8577763 PMC40079
  108. Myers K.M. Davis M. Mechanisms of fear extinction Mol. Psychiatry 12 2007 120 150 17160066
  109. Nader K. Schafe G.E. LeDoux J.E. Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval Nature 406 2000 722 726 10963596
  110. Navarro-Francés C.I. Arenas M.C. Influence of trait anxiety on the effects of acute stress on learning andretention of the passive avoidance task in male and female mice Behav. Process. 105 2014 6 14 24565981
  111. Nikzad S. Vafaei A.A. Rashidy-Pour A. Haghighi S. Systemic and intrahippocampal administrations of the glucocorticoid receptor antagonist RU38486 impairs fear memory reconsolidation in rats Stress 14 4 2011 459 464 21438774
  112. Nyklicek I. Bosch J.A. Amerongen A.V. A generalized physiological hyperreactivity to acute stressors in hypertensives Biol. Psychol. 70 2005 44 51 16038773
  113. Ochsner K.N. Bunge S.A. Gross J.J. Gabrieli J.D.E. Rethinking feelings: an fMRI study of the cognitive regulation of emotion J. Cogn. Neurosci. 14 2002 1215 1229 12495527
  114. Ochsner K.N. Silvers J.A. Buhle J.T. Functional imaging studies of emotion regulation: a synthetic review and evolving model of the cognitive control of emotion Ann. N. Y. Acad. Sci. 1251 2012 E1 E24 23025352 PMC4133790
  115. Otto A.R. Raio C.M. Chiang A. Phelps E.A. Daw N.D. Working-memory capacity protects model-based learning from stress Proc. Natl. Acad. Sci. 110 52 2013 20941 20946 24324166 PMC3876216
  116. Pavlov I. Conditioned Reflexes 1927 Oxford University Press Oxford, UK Gross & Muñoz, 1995
  117. Peri T. Ben-Shakhar G. Orr S.P. Shalev A.Y. Psychophysiologic assessment of aversive conditioning in posttraumatic stress disorder Biol. Psychiatry 47 2000 512 519 10715357
  118. Peters J. Kalivas P.W. Quirk G.J. Extinction circuits for fear and addiction overlap in the prefrontal cortex Learn. Mem. 16 2009 279 288 19380710 PMC4527308
  119. Pitman R.K. Delahanty D.L. Conceptually driven pharmacologic approaches to acute trauma CNS Spectr. 10 2005 99 106 15685120
  120. Plessow F. Fischer R. Kirschbaum C. Goschke T. Inflexibly focused under stress: acute psychosocial stress increases shielding of action goals at the expense of reduced cognitive flexibility with increasing time lag to the stressor J. Cogn. Neurosci. 23 2011 3218 3227 21452940
  121. Przybyslawski J. Roullet P. Sara S.J. Attenuation of emotional and nonemotional memories after their reactivation: role of beta adrenergic receptors Neuroscience 19 1999 6623 6628 10414990 PMC6782794
  122. Quirarte G.L. Roozendaal B. McGaugh J.L. Glucocorticoid enhancement of memory storage involves noradrenergic activation in the basolateral amygdala Proc. Natl. Acad. Sci. U. S. A. 94 1997 14048 14053 9391150 PMC28430
  123. Quirk G.J. Armony J.L. LeDoux J.E. Fear conditioning enhances different tempo- ral components of tone-evoked spike trains in auditory cortex and lateral amygdala Neuron 19 1997 613 624 9331352
  124. Quirk G.J. Likhtik E. Pelletier J.G. Pare D. Stimulation of medial prefrontal cortex decreases the responsiveness of central amygdala output neurons J. Neurosci. 23 2003 8800 8807 14507980 PMC6740415
  125. Radley J.J. Arias C.M. Sawchenko P.E. Regional differentiation of the medial prefrontal cortex in regulating adaptive responses to acute emotional stress J. Neurosci. 26 2006 12967 12976 17167086 PMC6674963
  126. Raio C.M. Orederu T. Palazzolo L. Shurick A. Phelps E.A. Cognitive emotion regulation fails the stress test Proc. Natl. Acad. Sci. 110 37 2013 15139 15144 23980142 PMC3773739
  127. Rau V. DeCola J.P. Fanselow M.S. Stress-induced enhancement of fear learning: an animal model of posttraumatic stress disorder Neurosci. Biobehav. Rev. 29 2005 1207 1223 16095698
  128. Rau V. Fanselow M.S. Exposure to a stressor produces a long lasting enhancement of fear learning in rats Stress 18 2009 1 18609302
  129. Repa J.C. Muller J. Apergis J. Desrochers T.M. Zhou Y. LeDoux J.E. Two different lateral amygdala cell populations contribute to the initiation and storage of memory Nat. Neurosci. 4 2001 724 731 11426229
  130. Rodriguez-Romaguera J. Sotres-Bayon F. Mueller D. Quirk G.J. Systemic propranolol acts centrally to reduce conditioned fear in rats without impairing extinction Biol. Psychiatry 65 2009 887 892 19246030 PMC2695810
  131. Rodrigues S.M. Sapolsky R.M. Disruption of fear memory through dual-hormone gene therapy Biol. Psychiatry 65 2009 441 444 18973875 PMC2660393
  132. Rodrigues S.M. LeDoux J.E. Sapolsky R.M. The influences of stress hormones on fear circuitry Annu. Rev. Neurosci. 32 2009 289 313 19400714
  133. Roozendaal B. McGaugh J.L. Glucocorticoid receptor agonist and antagonist administration into the basolateral but not central amygdala modulates memory storage Neurobiol. Learn Mem. 67 2 1997 176 179 9075247
  134. Roozendaal B. Quirarte G.L. McGaugh J.L. Glucocorticoids interact with the basolateral amygdala alpha-adrenoceptor–cAMP/cAMP/PKA system in influencing memory consolidation Eur. J. Neurosci. 15 2002 553 560 11876783
  135. Roozendaal B. McReynolds J.R. McGaugh J.L. The basolateral amygdala interacts with the medial prefrontal cortex in regulating glucocorticoid effects on working memory impairment J. Neurosci. 24 2004 1385 1392 14960610 PMC6730337
  136. Roozendaal B. Hui G.K. Hui I.R. Berlau D.J. McGaugh J.L. Weinberger N.M. Basolateral amygdala noradrenergic activity mediates corticosterone-induced enhancement of auditory fear conditioning Neurobiol. Learn. Mem. 86 2006 249 255 16630730
  137. Roozendaal B. McEwen B.S. Chattarji S. Stress, memory and the amygdala Nat. Rev. Neurosci. 10 2009 423 433 19469026
  138. Rosenkranz J.A. Moore H. Grace A.A. The prefrontal cortex regulates lateral amygdala neuronal plasticity and responses to previously conditioned stimuli. J Neurosci. 23 2003 11054 11064 PMC6741051 14657162
  139. Schiller D. Delgado M.R. Overlapping neural systems mediating extinction, reversal and regulation of fear Trends Cogn. Sci. 14 2010 268 276 20493762 PMC3848321
  140. 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 463 2009 49 53 20010606 PMC3640262
  141. Schiller D. Phelps E.A. Does reconsolidation occur in humans? Front. Behav. Neurosci. 5 2011 24 21629821 PMC3099269
  142. Schiller D. Kanen J.W. LeDoux J.E. Monfils M.-H. Phelps E.A. Extinction during reconsolidation eliminates prefrontal cortex involvement PNAS 110 50 2014 20040 20045 24277809 PMC3864277
  143. Shi C. Davis M. Pain pathways involved in fear conditioning measured with fear potentiated startle: lesion studies J. Neurosci. 19 1999 420 430 9870970 PMC6782355
  144. Shors T.J. Weiss C. Thompson R.F. Stress-induced facilitation of classical conditioning Science 257 1992 537 539 1636089
  145. Shors T. Acute stress rapidly and persistently enhances memory formation in the male rat Neurobiol. Learn. Mem. 75 2001 10 29 11124044
  146. Sijbranij M. Englehard I.M. Lommen M.J. Leer A. Baas J.M. Impaired fear inhibition learning predicts the persistence of symptoms of posttraumatic stress disorder PTSD) J. Psychiat. Res. 47 2013 1991 1997 24090716
  147. Soeter M. Kindt M. High trait anxiety: a challenge for disrupting fear memory reconsolidation PLoS One 8 2013 PMC3832500 24260096
  148. Soravia L.M. Heinrichs M. Aerni A. Maroni C. Schelling G. Ehlert U. Roozendaal B. de Quervain D.J. Glucocorticoids reduce phobic fear in humans Proc. Natl. Acad. Sci. U. S. A. 103 2006 5585 5590 16567641 PMC1414637
  149. Steinfurth E.C.K. Kanen J.W. Raio C.M. Clem R. Huganir R. Phelps E.A. Recent and remote Pavlovian fear memories can be modified with extinction training during reconsolidation in humans Learn. Mem. 21 7 2014 338 341 24934333 PMC4061428
  150. Suris A. North C. Adinoff B. Powell C.M. Greene R. Effects of glucocorticoid on combat-related PTSD symptoms Ann. Clin. Psychiatry 22 2010 274 279 21180658 PMC3917156
  151. Suzuki A. Josselyn S.A. Frankland P.W. Masushige S. Silva A.J. Kida S. Memory reconsolidation and extinction have distinct temporal and biochemical signatures J. Neurosci. 24 2004 4787 4795 15152039 PMC6729467
  152. Taubenfeld S.M. Riceberg J.S. New A.S. Alberini C.M. Preclinical assessment for selectively disrupting a traumatic memory via postretrieval inhibition of glucocorticoid receptors Biol. Psychiatry 200965 2009 249 257 18708183 PMC2668168
  153. Tully K. Li Y. Tsvetkov E. Bolshakov V.Y. Norepinephrine enables the induction of associative long-term potentiation at thalamo-amygdala synapses Proc. Natl. Acad. Sci. U. S. A. 104 2007 14146 14150 17709755 PMC1955781
  154. Ulrich-Lai Y.A. Herman J.P. Neural regulation of endocrine and autonomic responses to stress Nat. Rev. 10 2009 397 409 PMC4240627 19469025
  155. Vertes R.P. Differential projections of the infralimbic and prelimbic cortex in the rat Synapse 51 2004 32 58 14579424
  156. Vidal-Gonzalez I. Vidal-Gonzalez B. Rauch S.L. Quirk G.J. Microstimulation reveals opposing influences of prelimbic and infralimbic cortex on the expression of conditioned fear Learn. Mem. 13 2006 728 733 17142302 PMC1783626
  157. Wessa M. Flor H. Failure of extinction of fear responses in posttraumatic stress disorder: evidence from second-order conditioning Am. J. Psychiatry 164 2007 1684 1692 17974933
  158. Wilson L.M. Wilson R. DiCara L.V. Pavlovian conditioned cardiodecelerations following preshock in immobilized rats Physiol. Behav. 15 1975 653 658 1241613
  159. Yang Y.L. Chao P.K. Lu K.T. Systemic and intra-amygdala administration of glucocorticoid agonist and antagonist modulate extinction of conditioned fear Neuropsychopharmacology 31 2006 912 924 16205786
  160. Yehuda R. Status of glucocorticoid alterations in pos-traumatic stress disorder Ann. N. Y. Acad. Sci. 1179 2009 56 69 19906232
  161. Young E.A. Haskett R.F. Grunhaus L. Pande A. Weinberg M. Watson S.J. Akil H. Increased evening activation of the hypothalamic-pituitary-adrenal axis in depressed patients Arch. Gen. Psychiatr. 51 1994 701 707 8080346
  162. Zorawski M. Blanding N.Q. Kuhn C.M. LaBar K.S. Effects of stress and sex on acquisition and consolidation of human fear conditioning Learn. Mem. 13 2006 441 450 16847304 PMC1538921

Authors
Raio, C. M., & Phelps, E. A.
Affiliations
  • New York University (US)
  • Nathan Kline Institute for Psychiatric Research (US)
Corresponding author
Phelps, Elizabeth A.
ORCID
Venue
Neurobiology of Stress
Publisher
Elsevier BV
Published
2015-01
Volume
1
Pages
134-146
ISSN
2352-2895 (ISSN-L)
DOI
10.1016/j.ynstr.2014.11.004
PMC
PMC4268774
OpenAlex
W2033174093
Cited by
121
References
232
Citations by year
2026: 17 · 2025: 4 · 2024: 6 · 2023: 4 · 2022: 14 · 2021: 16 · 2020: 10 · 2019: 17 · 2018: 12 · 2017: 12 · 2016: 5 · 2015: 4
FWCI
0.68
Type
journal article
Language
en
Open access
Licence
Locations
  • Neurobiology of Stress (publishedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
  • James S. McDonnell Foundation
  • National Institutes of Health (MH097085)
  • National Institute of Mental Health (R01MH097085)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
  • Social Sciences › Psychology › Experimental and Cognitive Psychology › Anxiety, Depression, Psychometrics, Treatment, Cognitive Processes
Keywords
acute stress, fear conditioning, fear extinction, emotion regulation, cognitive emotion regulation, stress hormones, prefrontal cortex, avoidance, fear reconsolidation, anxiety disorders, stress-related psychopathology

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