The influence of stress hormones on fear circuitry.

Fear arousal, initiated by an environmental threat, leads to activation of the stress response, a state of alarm that promotes an array of autonomic and endocrine changes designed to aid self-preservation. The stress response includes the release of glucocorticoids from the adrenal cortex and catecholamines from the adrenal medulla and sympathetic nerves. These stress hormones, in turn, provide feedback to the brain and influence neural structures that control emotion and cognition. To illustrate this influence, we focus on how it impacts fear conditioning, a behavioral paradigm widely used to study the neural mechanisms underlying the acquisition, expression, consolidation, reconsolidation, and extinction of emotional memories. We also discuss how stress and the endocrine mediators of the stress response influence the morphological and electrophysiological properties of neurons in brain areas that are crucial for fear-conditioning processes, including the amygdala, hippocampus, and prefrontal cortex. The information in this review illuminates the behavioral and cellular events that underlie the feedforward and feedback networks that mediate states of fear and stress and their interaction in the brain.

[1]  E. Ronald de Kloet,et al.  Hormones and the Stressed Brain , 2004 .

[2]  D. Paré,et al.  Amygdala intercalated neurons are required for expression of fear extinction , 2008, Nature.

[3]  Richard F. Thompson,et al.  Inescapable versus escapable shock modulates long-term potentiation in the rat hippocampus. , 1989, Science.

[4]  Joseph E LeDoux,et al.  Somatosensory and auditory convergence in the lateral nucleus of the amygdala. , 1993, Behavioral neuroscience.

[5]  K. Lu,et al.  Systemic and Intra-Amygdala Administration of Glucocorticoid Agonist and Antagonist Modulate Extinction of Conditioned Fear , 2006, Neuropsychopharmacology.

[6]  M. Weinstock.  Gender Differences in the Effects of Prenatal Stress on Brain Development and Behaviour , 2007, Neurochemical Research.

[7]  James L McGaugh,et al.  Amygdala Modulation of Memory Consolidation: Interaction with Other Brain Systems , 2002, Neurobiology of Learning and Memory.

[8]  M. Gallagher,et al.  Memory formation: evidence for a specific neurochemical system in the amygdala. , 1977, Science.

[9]  T. Jay,et al.  Acute stress-induced changes in hippocampal/prefrontal circuits in rats: effects of antidepressants. , 2004, Cerebral cortex.

[10]  M. Fanselow,et al.  Modality-specific retrograde amnesia of fear. , 1992, Science.

[11]  Shantanu P. Jadhav,et al.  Stress duration modulates the spatiotemporal patterns of spine formation in the basolateral amygdala. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[12]  J. Morrison,et al.  Chronic behavioral stress induces apical dendritic reorganization in pyramidal neurons of the medial prefrontal cortex , 2004, Neuroscience.

[13]  Joseph E LeDoux,et al.  Molecular Mechanisms Underlying Emotional Learning and Memory in the Lateral Amygdala , 2004, Neuron.

[14]  J. Price.  Comparative Aspects of Amygdala Connectivity , 2003, Annals of the New York Academy of Sciences.

[15]  Joseph E LeDoux,et al.  Differential Contribution of Amygdala and Hippocampus to Cued and Contextual Fear Conditioning , 1992 .

[16]  A. Grace,et al.  The Prefrontal Cortex Regulates Lateral Amygdala Neuronal Plasticity and Responses to Previously Conditioned Stimuli , 2003, The Journal of Neuroscience.

[17]  R. Sapolsky,et al.  Acute corticosterone treatment is sufficient to induce anxiety and amygdaloid dendritic hypertrophy , 2008, Proceedings of the National Academy of Sciences.

[18]  D. Amaral,et al.  Some observations on cortical inputs to the macaque monkey amygdala: An anterograde tracing study , 2002, The Journal of comparative neurology.

[19]  Joseph E LeDoux,et al.  New vistas on amygdala networks in conditioned fear. , 2004, Journal of neurophysiology.

[20]  J. Fudge,et al.  The extended amygdala and the dopamine system: another piece of the dopamine puzzle. , 2003, The Journal of neuropsychiatry and clinical neurosciences.

[21]  B. McEwen.  Mood disorders and allostatic load , 2003, Biological Psychiatry.

[22]  Yadin Dudai,et al.  Reconsolidation: the advantage of being refocused , 2006, Current Opinion in Neurobiology.

[23]  Simon Killcross,et al.  Posttraining Glucocorticoid Receptor Agonist Enhances Memory in Appetitive and Aversive Pavlovian Discrete-Cue Conditioning Paradigms , 2002, Neurobiology of Learning and Memory.

[24]  Bruce S. McEwen,et al.  Stress and hippocampal plasticity: implications for the pathophysiology of affective disorders , 2001, Human psychopharmacology.

[25]  Gary Aston-Jones,et al.  CHAPTER 11 – Locus Coeruleus, A5 and A7 Noradrenergic Cell Groups , 2004 .

[26]  Yan Li,et al.  Norepinephrine enables the induction of associative long-term potentiation at thalamo-amygdala synapses , 2007, Proceedings of the National Academy of Sciences.

[27]  A. Ylinen,et al.  Reciprocal Connections between the Amygdala and the Hippocampal Formation, Perirhinal Cortex, and Postrhinal Cortex in Rat: A Review , 2000, Annals of the New York Academy of Sciences.

[28]  G. Quirk,et al.  Lesions of the Basal Amygdala Block Expression of Conditioned Fear But Not Extinction , 2005, The Journal of Neuroscience.

[29]  C. Harley.  Norepinephrine and the dentate gyrus. , 2007, Progress in brain research.

[30]  P. Frankland,et al.  Consolidation of CS and US representations in associative fear conditioning , 2004, Hippocampus.

[31]  J. Schulkin,et al.  Glucocorticoid receptor antagonism in the basolateral amygdala and ventral hippocampus interferes with long-term memory of contextual fear , 2005, Behavioural Brain Research.

[32]  D. Quervain.  Glucocorticoid-induced reduction of traumatic memories : implications for the treatment of PTSD , 2008 .

[33]  B. Czéh,et al.  Chronic stress-induced cellular changes in the medial prefrontal cortex and their potential clinical implications: Does hemisphere location matter? , 2008, Behavioural Brain Research.

[34]  M. Fleshner,et al.  A selective role for corticosterone in contextual-fear conditioning. , 1997, Behavioral Neuroscience.

[35]  R. Derijk,et al.  Corticosteroid receptor genetic polymorphisms and stress responsivity , 2005, Endocrine.

[36]  S. Chattarji,et al.  Chronic Stress Induces Contrasting Patterns of Dendritic Remodeling in Hippocampal and Amygdaloid Neurons , 2002, The Journal of Neuroscience.

[37]  R. Joosten,et al.  Dopamine and noradrenaline efflux in the rat prefrontal cortex after classical aversive conditioning to an auditory cue , 2001, The European journal of neuroscience.

[38]  J. Morrison,et al.  Reversibility of apical dendritic retraction in the rat medial prefrontal cortex following repeated stress , 2005, Experimental Neurology.

[39]  Joseph E LeDoux,et al.  Organization of intra-amygdaloid circuitries in the rat: an emerging framework for understanding functions of the amygdala , 1997, Trends in Neurosciences.

[40]  L. Swanson.  The Amygdala and Its Place in the Cerebral Hemisphere , 2003, Annals of the New York Academy of Sciences.

[41]  Alain Brunet,et al.  Effect of post-retrieval propranolol on psychophysiologic responding during subsequent script-driven traumatic imagery in post-traumatic stress disorder. , 2008, Journal of psychiatric research.

[42]  V. Luine,et al.  Sex Differences in Chronic Stress Effects on Memory in Rats , 2002, Stress.

[43]  C. Sandi,et al.  Glucocorticoid Involvement in Memory Formation in a Rat Model for Traumatic Memory , 2002, Stress.

[44]  Joseph E LeDoux.  Emotion: clues from the brain. , 1995, Annual review of psychology.

[45]  T. Robbins,et al.  Enhanced behavioral conditioning to context and impaired behavioral and neuroendocrine responses to conditioned stimuli following ceruleocortical noradrenergic lesions: support for an attentional hypothesis of central noradrenergic function , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[46]  Stephen Maren.  Synaptic Mechanisms of Associative Memory in the Amygdala , 2005, Neuron.

[47]  Stephen Maren.  Neurobiology of Pavlovian fear conditioning. , 2001, Annual review of neuroscience.

[48]  A. Arnsten,et al.  Adrenergic pharmacology and cognition: focus on the prefrontal cortex. , 2007, Pharmacology & therapeutics.

[49]  Frank H Wilhelm,et al.  Fear conditioning in posttraumatic stress disorder: evidence for delayed extinction of autonomic, experiential, and behavioural responses. , 2007, Behaviour research and therapy.

[50]  R. Sapolsky,et al.  Effects of enrichment predominate over those of chronic stress on fear-related behavior in male rats , 2009, Stress.

[51]  H. T. Blair,et al.  Synaptic plasticity in the lateral amygdala: a cellular hypothesis of fear conditioning. , 2001, Learning & memory.

[52]  A. Kavushansky,et al.  Activity and plasticity in the CA1, the dentate gyrus, and the amygdala following controllable vs. uncontrollable water stress , 2006, Hippocampus.

[53]  Roberto Malinow,et al.  Emotion Enhances Learning via Norepinephrine Regulation of AMPA-Receptor Trafficking , 2007, Cell.

[54]  S. Paradiso.  The Emotional Brain: The Mysterious Underpinnings of Emotional Life , 1998 .

[55]  H. Markram,et al.  Actions of norepinephrine in the rat hippocampus. , 1991, Progress in brain research.

[56]  Alicia Izquierdo,et al.  Brief Uncontrollable Stress Causes Dendritic Retraction in Infralimbic Cortex and Resistance to Fear Extinction in Mice , 2006, The Journal of Neuroscience.

[57]  C. Sandi,et al.  Modulation of contextual fear conditioning by chronic stress in rats is related to individual differences in behavioral reactivity to novelty , 2003, Brain Research.

[58]  E. Vizi,et al.  Noradrenergic enhancement of Ca2+ responses of basal dendrites in layer 5 pyramidal neurons of the prefrontal cortex , 2007, Neurochemistry International.

[59]  G. Quirk,et al.  Noradrenergic Signaling in Infralimbic Cortex Increases Cell Excitability and Strengthens Memory for Fear Extinction , 2008, The Journal of Neuroscience.

[60]  S. Korte.  Corticosteroids in relation to fear, anxiety and psychopathology , 2001, Neuroscience & Biobehavioral Reviews.

[61]  B. McEwen,et al.  Plasticity of the Hippocampus: Adaptation to Chronic Stress and Allostatic Load , 2001, Annals of the New York Academy of Sciences.

[62]  Douglas W. Barrett,et al.  Behavioral effects of metyrapone on Pavlovian extinction , 2004, Neuroscience Letters.

[63]  M. Meaney,et al.  Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. , 2001, Annual review of neuroscience.

[64]  Joseph E LeDoux,et al.  Disruption of reconsolidation but not consolidation of auditory fear conditioning by noradrenergic blockade in the amygdala , 2004, Neuroscience.

[65]  Bao-Ming Li,et al.  Deficit in long‐term contextual fear memory induced by blockade of β‐adrenoceptors in hippocampal CA1 region , 2003, The European journal of neuroscience.

[66]  M. Fanselow,et al.  Exposure to a stressor produces a long lasting enhancement of fear learning in rats , 2009, Stress.

[67]  James L. McGaugh,et al.  Memory and Emotion: The Making of Lasting Memories , 2003 .

[68]  D. Diamond,et al.  Differential effects of predator stress and the antidepressant tianeptine on physiological plasticity in the hippocampus and basolateral amygdala , 2006, Stress.

[69]  B. Balleine,et al.  Parallel incentive processing: an integrated view of amygdala function , 2006, Trends in Neurosciences.

[70]  N. Kalin,et al.  Nonhuman Primate Models to Study Anxiety, Emotion Regulation, and Psychopathology , 2003, Annals of the New York Academy of Sciences.

[71]  R Jaffard,et al.  Footshock stress but not contextual fear conditioning induces long‐term enhancement of auditory‐evoked potentials in the basolateral amygdala of the freely behaving rat , 1998, The European journal of neuroscience.

[72]  S. Chattarji,et al.  Recovery after chronic stress fails to reverse amygdaloid neuronal hypertrophy and enhanced anxiety-like behavior , 2004, Neuroscience.

[73]  G. Quirk,et al.  Neuronal signalling of fear memory , 2004, Nature Reviews Neuroscience.

[74]  Andrew M. Poulos,et al.  The neuroscience of mammalian associative learning. , 2005, Annual review of psychology.

[75]  Joseph E. LeDoux,et al.  Emotional processing and motivation: In search of brain mechanisms , 2008 .

[76]  R. Pitman,et al.  Conceptually Driven Pharmacologic Approaches to Acute Trauma , 2005, CNS Spectrums.

[77]  N. Sousa,et al.  Reorganization of the morphology of hippocampal neurites and synapses after stress-induced damage correlates with behavioral improvement , 2000, Neuroscience.

[78]  M. Gabriel,et al.  Consideration of a Unified Model of Amygdalar Associative Functions , 2003, Annals of the New York Academy of Sciences.

[79]  E R Kandel,et al.  Both Protein Kinase A and Mitogen-Activated Protein Kinase Are Required in the Amygdala for the Macromolecular Synthesis-Dependent Late Phase of Long-Term Potentiation , 2000, The Journal of Neuroscience.

[80]  P. E. Gold,et al.  Catecholamines, Stress, and Disease: A Psychobiological Perspective , 1996, Psychosomatic Medicine.

[81]  Robert M. Sapolsky,et al.  Why Zebras Don't Get Ulcers , 1994 .

[82]  B. McEwen.  Stress and hippocampal plasticity. , 1999, Annual review of neuroscience.

[83]  Herta Flor,et al.  Failure of extinction of fear responses in posttraumatic stress disorder: evidence from second-order conditioning. , 2007, The American journal of psychiatry.

[84]  K. Abrari,et al.  Administration of corticosterone after memory reactivation disrupts subsequent retrieval of a contextual conditioned fear memory: Dependence upon training intensity , 2008, Neurobiology of Learning and Memory.

[85]  V. Molina,et al.  Previous Stress Facilitates Fear Memory, Attenuates GABAergic Inhibition, and Increases Synaptic Plasticity in the Rat Basolateral Amygdala , 2005, The Journal of Neuroscience.

[86]  B. Roozendaal,et al.  Can Posttraumatic Stress Disorder Be Prevented with Glucocorticoids? , 2004, Annals of the New York Academy of Sciences.

[87]  Gal Richter-Levin,et al.  The Amygdala, the Hippocampus, and Emotional Modulation of Memory , 2004, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[88]  Andreas Papassotiropoulos,et al.  Low-dose cortisol for symptoms of posttraumatic stress disorder. , 2004, The American journal of psychiatry.

[89]  M. Fendt,et al.  The neuroanatomical and neurochemical basis of conditioned fear , 1999, Neuroscience & Biobehavioral Reviews.

[90]  C. Marsden,et al.  Effects of lesioning noradrenergic neurones in the locus coeruleus on conditioned and unconditioned aversive behaviour in the rat , 2001, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[91]  S. Rauch,et al.  Microstimulation reveals opposing influences of prelimbic and infralimbic cortex on the expression of conditioned fear. , 2006, Learning & memory.

[92]  T. Gray,et al.  Amygdaloid CRF Pathways: Role in Autonomic, Neuroendocrine, and Behavioral Responses to Stress , 1993, Annals of the New York Academy of Sciences.

[93]  S. Orr,et al.  Effects of beta blockade, PTSD diagnosis, and explicit threat on the extinction and retention of an aversively conditioned response , 2006, Biological Psychology.

[94]  I. Izquierdo,et al.  Stress hormones enhance retrieval of fear conditioning acquired either one day or many months before , 2002, Behavioural pharmacology.

[95]  B. Averbeck,et al.  The primate cortical auditory system and neural representation of conspecific vocalizations. , 2009, Annual review of neuroscience.

[96]  J. D. McGaugh,et al.  Glucocorticoid Receptor Agonist and Antagonist Administration into the Basolateral but Not Central Amygdala Modulates Memory Storage , 1997, Neurobiology of Learning and Memory.

[97]  Robert M. Sapolsky,et al.  Stress and Plasticity in the Limbic System , 2003, Neurochemical Research.

[98]  Shannon R. Henning,et al.  Mild, short-term stress alters dendritic morphology in rat medial prefrontal cortex. , 2005, Cerebral cortex.

[99]  Joseph E LeDoux,et al.  Emotional perseveration: an update on prefrontal-amygdala interactions in fear extinction. , 2004, Learning & memory.

[100]  Barry J. Everitt,et al.  Conditioned suppression and freezing as measures of aversive Pavlovian conditioning: effects of discrete amygdala lesions and overtraining , 2005, Behavioural Brain Research.

[101]  Constantine Pavlides,et al.  Effects of chronic stress on hippocampal long‐term potentiation , 2002, Hippocampus.

[102]  J. D. McGaugh,et al.  Modulating effects of posttraining epinephrine on memory: Involvement of the amygdala noradrenergic system , 1986, Brain Research.

[103]  Gal Richter-Levin,et al.  Emotional tagging of memory formation—in the search for neural mechanisms , 2003, Brain Research Reviews.

[104]  P. Fries.  Neuronal gamma-band synchronization as a fundamental process in cortical computation. , 2009, Annual review of neuroscience.

[105]  Joseph E LeDoux,et al.  Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy. , 1999, Behavioral neuroscience.

[106]  M. Maroun,et al.  Exposure to Acute Stress Blocks the Induction of Long-Term Potentiation of the Amygdala–Prefrontal Cortex Pathway In Vivo , 2003, The Journal of Neuroscience.

[107]  J. D. McGaugh,et al.  Role of the Basolateral Amygdala in Memory Consolidation , 2003, Annals of the New York Academy of Sciences.

[108]  J. D. McGaugh,et al.  Clenbuterol Administration into the Basolateral Amygdala Post-training Enhances Retention in an Inhibitory Avoidance Task , 1999, Neurobiology of Learning and Memory.

[109]  C. Alberini,et al.  Persistent Disruption of a Traumatic Memory by Postretrieval Inactivation of Glucocorticoid Receptors in the Amygdala , 2007, Biological Psychiatry.

[110]  A. Kiss,et al.  Some assessments of the amygdala role in suprahypothalamic neuroendocrine regulation: a minireview. , 2007, Endocrine regulations.

[111]  Ricardo Insausti,et al.  Retrograde transport of D-[3H]-aspartate injected into the monkey amygdaloid complex , 2005, Experimental Brain Research.

[112]  J. W. Rudy,et al.  Type II Glucocorticoid Receptor Antagonists Impair Contextual but Not Auditory-Cue Fear Conditioning in Juvenile Rats , 1997, Neurobiology of Learning and Memory.

[113]  Joseph E LeDoux,et al.  Corticosterone Potentiation of Conditioned Fear in Rats a , 1994, Annals of the New York Academy of Sciences.

[114]  M. Jackson,et al.  Distinct patterns of plasticity in prefrontal cortex neurons that encode slow and fast responses to stress , 2006, The European journal of neuroscience.

[115]  Joseph E LeDoux.  Emotion circuits in the brain. , 2009, Annual review of neuroscience.

[116]  Karim Nader,et al.  Memory traces unbound , 2003, Trends in Neurosciences.

[117]  D C Blanchard,et al.  Crouching as an index of fear. , 1969, Journal of comparative and physiological psychology.

[118]  K. J. Parker,et al.  Stress inoculation-induced indications of resilience in monkeys. , 2007, Journal of traumatic stress.

[119]  G. Spennato,et al.  Hippocampal low-frequency stimulation and chronic mild stress similarly disrupt fear extinction memory in rats , 2008, Neurobiology of Learning and Memory.

[120]  Evangelia Charmandari,et al.  Endocrinology of the stress response. , 2005, Annual review of physiology.

[121]  A. McDonald,et al.  Topographical organization of amygdaloid projections to the caudatoputamen, nucleus accumbens, and related striatal-like areas of the rat brain , 1991, Neuroscience.

[122]  J. D. McGaugh,et al.  Glucocorticoid enhancement of memory storage involves noradrenergic activation in the basolateral amygdala. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[123]  R. Greene,et al.  Postreactivation Glucocorticoids Impair Recall of Established Fear Memory , 2006, The Journal of Neuroscience.

[124]  Hongjoo J. Lee,et al.  Post-training injections of catecholaminergic drugs do not modulate fear conditioning in rats and mice , 2001, Neuroscience Letters.

[125]  S. Maier,et al.  Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus , 2005, Nature Neuroscience.

[126]  M. Sarter,et al.  Involvement of the amygdala in learning and memory: a critical review, with emphasis on anatomical relations. , 1985, Behavioral neuroscience.

[127]  J. D. McGaugh,et al.  Basolateral amygdala noradrenergic activity mediates corticosterone-induced enhancement of auditory fear conditioning , 2006, Neurobiology of Learning and Memory.

[128]  J. D. McGaugh.  Memory--a century of consolidation. , 2000, Science.

[129]  K. LaBar,et al.  Effects of stress and sex on acquisition and consolidation of human fear conditioning. , 2006, Learning & memory.

[130]  A. McDonald.  Cortical pathways to the mammalian amygdala , 1998, Progress in Neurobiology.

[131]  J. Morrison,et al.  Repeated stress induces dendritic spine loss in the rat medial prefrontal cortex. , 2006, Cerebral cortex.

[132]  C. Wellman,et al.  Chronic stress impairs recall of extinction of conditioned fear , 2006, Neurobiology of Learning and Memory.

[133]  M. Bouton,et al.  Contextual and Temporal Modulation of Extinction: Behavioral and Biological Mechanisms , 2006, Biological Psychiatry.

[134]  Stephen Maren.  Neurotoxic Basolateral Amygdala Lesions Impair Learning and Memory But Not the Performance of Conditional Fear in Rats , 1999, The Journal of Neuroscience.

[135]  G. Quirk,et al.  Fear Conditioning and Extinction Differentially Modify the Intrinsic Excitability of Infralimbic Neurons , 2008, The Journal of Neuroscience.

[136]  Douglas B. Ehlenberger,et al.  Repeated stress alters dendritic spine morphology in the rat medial prefrontal cortex , 2008, The Journal of comparative neurology.

[137]  Stephen Maren,et al.  Hippocampal involvement in contextual modulation of fear extinction , 2007, Hippocampus.

[138]  Susan C. Cook,et al.  Chronic stress alters dendritic morphology in rat medial prefrontal cortex. , 2004, Journal of neurobiology.

[139]  Y. Dudai.  The neurobiology of consolidations, or, how stable is the engram? , 2004, Annual review of psychology.

[140]  T. Jay,et al.  The Prefrontal Cortex as a Key Target of the Maladaptive Response to Stress , 2007, The Journal of Neuroscience.

[141]  B. Everitt,et al.  Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex , 2002, Neuroscience & Biobehavioral Reviews.

[142]  C. Sandi,et al.  Prior exposure to a single stress session facilitates subsequent contextual fear conditioning in rats Evidence for a role of corticosterone , 2003, Hormones and Behavior.

[143]  F. Mascagni,et al.  Projections of the medial and lateral prefrontal cortices to the amygdala: a Phaseolus vulgaris leucoagglutinin study in the rat , 1996, Neuroscience.

[144]  L. Cahill,et al.  Pilot study of secondary prevention of posttraumatic stress disorder with propranolol , 2002, Biological Psychiatry.

[145]  C. Pavlides,et al.  Effects of mineralocorticoid and glucocorticoid receptors on long-term potentiation in the CA3 hippocampal field , 1999, Brain Research.

[146]  J. W. Rudy,et al.  A selective role for corticosterone in contextual-fear conditioning. , 1997, Behavioral neuroscience.

[147]  J. Warren.  Synaptic Self: How our Brains Become who we Are , 2002 .

[148]  Karim Nader,et al.  Memory consolidation of Pavlovian fear conditioning: a cellular and molecular perspective , 2001, Trends in Neurosciences.

[149]  D. Diamond,et al.  Effects of inescapable stress on LTP in the amygdala versus the dentate gyrus of freely behaving rats , 2004, The European journal of neuroscience.

[150]  R. A. Fuchs,et al.  Influence of chronic corticosterone and glucocorticoid receptor antagonism in the amygdala on fear conditioning , 2004, Neurobiology of Learning and Memory.

[151]  S. Thomas,et al.  A Distinct Role for Norepinephrine in Memory Retrieval , 2004, Cell.

[152]  Michael Davis,et al.  The amygdala , 2000, Current Biology.

[153]  R. Sapolsky,et al.  Disruption of Fear Memory Through Dual-Hormone Gene Therapy , 2009, Biological Psychiatry.

[154]  Shantanu P. Jadhav,et al.  Prolonged behavioral stress enhances synaptic connectivity in the basolateral amygdala , 2006, Neuroscience.

[155]  Jonathan D. Cohen,et al.  Adaptive gain and the role of the locus coeruleus–norepinephrine system in optimal performance , 2005, The Journal of comparative neurology.

[156]  James L. McGaugh,et al.  Enhancement of extinction memory consolidation: The role of the noradrenergic and GABAergic systems within the basolateral amygdala , 2006, Neurobiology of Learning and Memory.

[157]  Joseph E LeDoux,et al.  Rethinking the Fear Circuit: The Central Nucleus of the Amygdala Is Required for the Acquisition, Consolidation, and Expression of Pavlovian Fear Conditioning , 2006, The Journal of Neuroscience.

[158]  D. Paré,et al.  Glucocorticoids Enhance the Excitability of Principal Basolateral Amygdala Neurons , 2007, The Journal of Neuroscience.

[159]  A. Kavushansky,et al.  Effects of stress and corticosterone on activity and plasticity in the amygdala , 2006, Journal of neuroscience research.

[160]  S. Chattarji,et al.  Modulation of different states of anxiety-like behavior by chronic stress. , 2004, Behavioral neuroscience.

[161]  Joseph E LeDoux,et al.  Coping with Danger: The Neural Basis of Defensive Behavior and Fearful Feelings , 2011 .

[162]  L. Sanford,et al.  Transient fear-induced alterations in evoked release of norepinephrine and GABA in amygdala slices , 2007, Brain Research.

[163]  S. Ogawa,et al.  Role of adrenal steroid mineralocorticoid and glucocorticoid receptors in long-term potentiation in the CA1 field of hippocampal slices , 1996, Brain Research.

[164]  P. Lang,et al.  Emotion, motivation, and the brain: reflex foundations in animal and human research. , 2006, Progress in brain research.

[165]  K. Kohda,et al.  Glucocorticoid receptor activation is involved in producing abnormal phenotypes of single-prolonged stress rats: A putative post-traumatic stress disorder model , 2007, Neuroscience.

[166]  R. Sapolsky,et al.  How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. , 2000, Endocrine reviews.

[167]  J. D. McGaugh,et al.  Amygdala norepinephrine levels after training predict inhibitory avoidance retention performance in rats , 2002, The European journal of neuroscience.

[168]  G. Quirk,et al.  Neural Mechanisms of Extinction Learning and Retrieval , 2008, Neuropsychopharmacology.

[169]  Stephen Maren,et al.  The central nucleus of the amygdala is essential for acquiring and expressing conditional fear after overtraining. , 2007, Learning & memory.

[170]  Adam M. Campbell,et al.  The Temporal Dynamics Model of Emotional Memory Processing: A Synthesis on the Neurobiological Basis of Stress-Induced Amnesia, Flashbulb and Traumatic Memories, and the Yerkes-Dodson Law , 2007, Neural plasticity.

[171]  D. D. de Quervain,et al.  Glucocorticoids reduce phobic fear in humans. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[172]  M. Joëls,et al.  Control of neuronal excitability by corticosteroid hormones , 1992, Trends in Neurosciences.

[173]  Gregory J. Quirk,et al.  Prefrontal Mechanisms in Extinction of Conditioned Fear , 2006, Biological Psychiatry.

[174]  C. Wellman,et al.  Dendritic reorganization in pyramidal neurons in medial prefrontal cortex after chronic corticosterone administration. , 2001, Journal of neurobiology.

[175]  Lan Ma,et al.  Glucocorticoid receptors in the basolateral nucleus of amygdala are required for postreactivation reconsolidation of auditory fear memory , 2007, The European journal of neuroscience.

[176]  Marian Joëls,et al.  Stress and cognition: are corticosteroids good or bad guys? , 1999, Trends in Neurosciences.

[177]  S. Chattarji,et al.  Effects of chronic stress on dendritic arborization in the central and extended amygdala , 2003, Brain Research.

[178]  T. Tabira,et al.  Suppression of glucocorticoid secretion enhances cholinergic transmission in rat hippocampus , 2008, Brain Research Bulletin.

[179]  M. Fanselow,et al.  Stress-induced enhancement of fear learning: An animal model of posttraumatic stress disorder , 2005, Neuroscience & Biobehavioral Reviews.

[180]  Benno Roozendaal,et al.  Memory enhancement of classical fear conditioning by post-training injections of corticosterone in rats , 2004, Neurobiology of Learning and Memory.

[181]  Joseph E LeDoux,et al.  Reply — reconsolidation: The labile nature of consolidation theory , 2000, Nature Reviews Neuroscience.

[182]  J. D. McGaugh,et al.  Posttraining handling facilitates memory for auditory-cue fear conditioning in rats , 2006, Neurobiology of Learning and Memory.

[183]  C. A. Morgan,et al.  Effects of the beta-blocker propranolol on cued and contextual fear conditioning in humans , 2004, Psychopharmacology.

[184]  JaneR . Taylor,et al.  A History of Corticosterone Exposure Regulates Fear Extinction and Cortical NR2B, GluR2/3, and BDNF , 2009, Neuropsychopharmacology.

[185]  P Roullet,et al.  Attenuation of Emotional and Nonemotional Memories after Their Reactivation: Role of ␤ Adrenergic Receptors , 1999 .