Pavlovian fear memory circuits and phenotype models of PTSD

Johnson, Luke R.; McGuire, Jennifer; Lazarus, Rachel; Palmer, Abraham A.

doi:10.1016/j.neuropharm.2011.07.004

Cited by 140Memory and Neural MechanismsPosttraumatic Stress Disorder ResearchNeuroscience and Neuropharmacology Research

Pavlovian fear memory circuits and phenotype models of PTSD

Johnson, Luke R., McGuire, Jennifer, Lazarus, Rachel, Palmer, Abraham A.·2012·Neuropharmacology

DOI 10.1016/j.neuropharm.2011.07.004

Open this paper in CoChat — free account

Abstract

Pavlovian fear conditioning, also known as classical fear conditioning is an important model in the study of the neurobiology of normal and pathological fear. Progress in the neurobiology of Pavlovian fear also enhances our understanding of disorders such as posttraumatic stress disorder (PTSD) and with developing effective treatment strategies. Here we describe how Pavlovian fear conditioning is a key tool for understanding both the neurobiology of fear and the mechanisms underlying variations in fear memory strength observed across different phenotypes. First we discuss how Pavlovian fear models aspects of PTSD. Second, we describe the neural circuits of Pavlovian fear and the molecular mechanisms within these circuits that regulate fear memory. Finally, we show how fear memory strength is heritable; and describe genes which are specifically linked to both changes in Pavlovian fear behavior and to its underlying neural circuitry. These emerging data begin to define the essential genes, cells and circuits that contribute to normal and pathological fear. This article is part of a Special Issue entitled 'Post-Traumatic Stress Disorder'.

Integrity signals

Registry

Crossref · 10.1016/j.neuropharm.2011.07.004

Cites

102 of 102 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Fear conditioning provides a potential framework for studying these phenotypes.
“Fear conditioning provides a potential framework for studying these phenotypes [see Ref. (55, 56)].”
From Conditioned fear associated phenotypes as robust, translational indices of trauma-, stressor-, and anxiety-related behaviors (2014) · cites this paper as [56]

Emotion circuits in the brain
LeDoux, J. E. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.155 · Cited by 8,444 · see citing works
Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval
Nader, K., Schafe, G. E., & Le Doux, J. E. (2000) · Nature · doi:10.1038/35021052 · Cited by 2,706 · see citing works
The role of the amygdala in fear and anxiety
Davis, M. (1992) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.15.030192.002033 · Cited by 2,357 · see citing works
Neurons in medial prefrontal cortex signal memory for fear extinction
Milad, M. R., & Quirk, G. J. (2002) · Nature · doi:10.1038/nature01138 · Cited by 1,836 · cited 1× · see citing works
“, 1993; Myers and Davis, 2007), as well as direct electrophysiological recordings (Milad and Quirk, 2002), indicate a key role for the mPFC in extinction.”
Background
The Emotional Brain, Fear, and the Amygdala
LeDoux, J. (2003) · Cellular and Molecular Neurobiology · doi:10.1023/a:1025048802629 · Cited by 1,818 · see citing works
Neuronal signalling of fear memory
Maren, S., & Quirk, G. J. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1535 · Cited by 1,428 · see citing works
Neurobiological Basis of Failure to Recall Extinction Memory in Posttraumatic Stress Disorder
Milad, M. R., Pitman, R. K., Ellis, C. B., Gold, A. L., Shin, L. M., Lasko, N. B., Zeidan, M. A., Handwerger, K., Orr, S. P., & Rauch, S. L. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.06.026 · Cited by 1,339 · see citing works
The amygdala
LeDoux, J. (2007) · Current Biology · doi:10.1016/j.cub.2007.08.005 · Cited by 1,281 · see citing works
Mechanisms of fear extinction
Myers, K. M., & Davis, M. (2007) · Molecular Psychiatry · doi:10.1038/sj.mp.4001939 · Cited by 1,277 · see citing works
Probability of shock in the presence and absence of cs in fear conditioning.
Rescorla, R. A. (1968) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0025984 · Cited by 1,067 · cited 1× · see citing works
“Second, the conditioning paradigm, including the number and contingency of CS and US associations influence the level of fear memory strength (Rescorla, 1968; Bauer et al., 2001).”
Background
Classical fear-conditioning in the anxiety disorders: a meta-analysis
Lissek, S., Powers, A. S., McClure, E. B., Phelps, E. A., Woldehawariat, G., Grillon, C., & Pine, D. S. (2005) · Behaviour Research and Therapy · doi:10.1016/j.brat.2004.10.007 · Cited by 1,034 · see citing works
Extinction-Reconsolidation Boundaries: Key to Persistent Attenuation of Fear Memories
Monfils, M.-H., Cowansage, K. K., Klann, E., & LeDoux, J. E. (2009) · Science · doi:10.1126/science.1167975 · Cited by 960 · see citing works
Switching on and off fear by distinct neuronal circuits
Herry, C., Ciocchi, S., Senn, V., Demmou, L., Müller, C., & Lüthi, A. (2008) · Nature · doi:10.1038/nature07166 · Cited by 950 · see citing works
Why We Think Plasticity Underlying Pavlovian Fear Conditioning Occurs in the Basolateral Amygdala
Fanselow, M. S., & LeDoux, J. E. (1999) · Neuron · doi:10.1016/s0896-6273(00)80775-8 · Cited by 914 · see citing works
Extinction of emotional learning: contribution of medial prefrontal cortex
Morgan, M. A., Romanski, L. M., & LeDoux, J. E. (1993) · Neuroscience Letters · doi:10.1016/0304-3940(93)90241-c · Cited by 897 · cited 1× · see citing works
“Studies using lesions of the mPFC (Morgan et al., 1993; Myers and Davis, 2007), as well as direct electrophysiological recordings (Milad and Quirk, 2002), indicate a key role for the mPFC in extinction.”
Method
Emotion, Memory and the Brain
LeDoux, J. E. (1994) · Scientific American · doi:10.1038/scientificamerican0694-50 · Cited by 892 · see citing works
Localization of a Stable Neural Correlate of Associative Memory
Reijmers, L. G. J. E., Perkins, B. L., Matsuo, N., & Mayford, M. R. (2007) · Science · doi:10.1126/science.1143839 · Cited by 853 · see citing works
New Vistas on Amygdala Networks in Conditioned Fear
Paré, D., Quirk, G. J., & Ledoux, J. E. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00153.2004 · Cited by 841 · see citing works
Blocking of acquisition but not expression of conditioned fear-potentiated startle by NMDA antagonists in the amygdala
Miserendino, M. J. D., Sananes, C. B., Melia, K. R., & Davis, M. (1990) · Nature · doi:10.1038/345716a0 · Cited by 824 · see citing works
Fear conditioning enhances short-latency auditory responses of lateral amygdala neurons: Parallel recordings in the freely behaving rat
Quirk, G. J., Repa, J. C., & LeDoux, J. E. (1995) · Neuron · doi:10.1016/0896-6273(95)90092-6 · Cited by 808 · see citing works
Latent inhibition: The effect of nonreinforced pre-exposure to the conditional stimulus.
Lubow, R. E., & Moore, A. U. (1959) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0046700 · Cited by 806 · see citing works
Postsynaptic receptor trafficking underlying a form of associative learning
Rumpel, S., LeDoux, J., Zador, A., & Malinow, R. (2005) · Science · doi:10.1126/science.1103944 · Cited by 775 · see citing works
Fear conditioning induces a lasting potentiation of synaptic currents in vitro
McKernan, M. G., & Shinnick-Gallagher, P. (1997) · Nature · doi:10.1038/37605 · Cited by 771 · see citing works
A twin study of genetic and environmental contributions to liability for posttraumatic stress symptoms
True, W. R. (1993) · Archives of General Psychiatry · doi:10.1001/archpsyc.1993.01820160019002 · Cited by 704 · see citing works
Neuronal competition and selection during memory formation
Han, J.-H., Kushner, S. A., Yiu, A. P., Cole, C. J., Matynia, A., Brown, R. A., Neve, R. L., Guzowski, J. F., Silva, A. J., & Josselyn, S. A. (2007) · Science · doi:10.1126/science.1139438 · Cited by 682 · see citing works
Activation of ERK/MAP Kinase in the Amygdala Is Required for Memory Consolidation of Pavlovian Fear Conditioning
Schafe, G. E., Atkins, C. M., Swank, M. W., Bauer, E. P., Sweatt, J. D., & LeDoux, J. E. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-21-08177.2000 · Cited by 674 · see citing works
De novo conditioning in trauma-exposed individuals with and without posttraumatic stress disorder.
Orr, S. P., Metzger, L. J., Lasko, N. B., Macklin, M. L., Peri, T., & Pitman, R. K. (2000) · Journal of Abnormal Psychology · doi:10.1037/0021-843x.109.2.290 · Cited by 653 · see citing works
Genetic and Environmental Influences on Trauma Exposure and Posttraumatic Stress Disorder Symptoms: A Twin Study
Stein, M. B., Jang, K. L., Taylor, S. J., Vernon, P. A., & Livesley, W. J. (2002) · American Journal of Psychiatry · doi:10.1176/appi.ajp.159.10.1675 · Cited by 602 · see citing works
Posttraumatic stress disorder following assault: The role of cognitive processing, trauma memory, and appraisals.
Halligan, S. L., Michael, T., Clark, D. M., & Ehlers, A. (2003) · Journal of Consulting and Clinical Psychology · doi:10.1037/0022-006x.71.3.419 · Cited by 585 · see citing works
Fear Conditioning Enhances Different Temporal Components of Tone-Evoked Spike Trains in Auditory Cortex and Lateral Amygdala
Quirk, G. J., Armony, J. L., & LeDoux, J. E. (1997) · Neuron · doi:10.1016/s0896-6273(00)80375-x · Cited by 563 · see citing works
Change in rape narratives during exposure therapy for posttraumatic stress disorder
Foa, E. B., Molnar, C., & Cashman, L. (1995) · Journal of Traumatic Stress · doi:10.1007/bf02102894 · Cited by 515 · see citing works
Fear conditioning in posttraumatic stress disorder: Evidence for delayed extinction of autonomic, experiential, and behavioural responses
Blechert, J., Michael, T., Vriends, N., Margraf, J., & Wilhelm, F. H. (2007) · Behaviour Research and Therapy · doi:10.1016/j.brat.2007.02.012 · Cited by 479 · see citing works
Are the neural substrates of memory the final common pathway in posttraumatic stress disorder (PTSD)?
Elzinga, B. (2002) · Journal of Affective Disorders · doi:10.1016/s0165-0327(01)00351-2 · Cited by 473 · see citing works
Brief Uncontrollable Stress Causes Dendritic Retraction in Infralimbic Cortex and Resistance to Fear Extinction in Mice
Izquierdo, A., Wellman, C. L., & Holmes, A. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.0474-06.2006 · Cited by 459 · see citing works
Long-Term Memory Is Facilitated by cAMP Response Element-Binding Protein Overexpression in the Amygdala
Josselyn, S. A., Shi, C., Carlezon, W. A., Neve, R. L., Nestler, E. J., & Davis, M. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-07-02404.2001 · Cited by 451 · see citing works
The spino(trigemino)pontoamygdaloid pathway: electrophysiological evidence for an involvement in pain processes
Bernard, J., & Besson, J. (1990) · Journal of Neurophysiology · doi:10.1152/jn.1990.63.3.473 · Cited by 447 · see citing works
Somatosensory and auditory convergence in the lateral nucleus of the amygdala.
Romanski, L. M., Clugnet, M.-C., Bordi, F., & LeDoux, J. E. (1993) · Behavioral Neuroscience · doi:10.1037/0735-7044.107.3.444 · Cited by 446 · see citing works
How the Neurocircuitry and Genetics of Fear Inhibition May Inform Our Understanding of PTSD
Jovanović, T., & Ressler, K. J. (2010) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2009.09071074 · Cited by 441 · see citing works
Two different lateral amygdala cell populations contribute to the initiation and storage of memory
Repa, J. C., Muller, J., Apergis, J., Desrochers, T. M., Zhou, Y., & LeDoux, J. E. (2001) · Nature Neuroscience · doi:10.1038/89512 · Cited by 440 · see citing works
Brain mechanisms of fear extinction: historical perspectives on the contribution of prefrontal cortex
Sotres-Bayon, F., Cain, C. K., & LeDoux, J. E. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.10.012 · Cited by 433 · see citing works
Fear Extinction in Traumatized Civilians with Posttraumatic Stress Disorder: Relation to Symptom Severity
Norrholm, S. D., Jovanovic, T., Olin, I. W., Sands, L. A., Karapanou, I., Bradley, B., & Ressler, K. J. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.09.013 · Cited by 397 · see citing works
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
BREMNER, J. D., VERMETTEN, E., SCHMAHL, C., VACCARINO, V., VYTHILINGAM, M., AFZAL, N., GRILLON, C., & CHARNEY, D. S. (2005) · Psychological Medicine · doi:10.1017/s0033291704003290 · Cited by 370 · see citing works
Impaired stress-coping and fear extinction and abnormal corticolimbic morphology in serotonin transporter knock-out mice
Wellman, C. L., Izquierdo, A., Garrett, J. E., Martin, K. P., Carroll, J., Millstein, R., Lesch, K.-P., Murphy, D. L., & Holmes, A. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.4595-06.2007 · Cited by 366 · see citing works
Extending animal models of fear conditioning to humans
Delgado, M. R., Olsson, A., & Phelps, E. A. (2006) · Biological Psychology · doi:10.1016/j.biopsycho.2006.01.006 · Cited by 366 · see citing works
Activation of Mitogen-Activated Protein Kinase/Extracellular Signal-Regulated Kinase in Hippocampal Circuitry Is Required for Consolidation and Reconsolidation of Recognition Memory
Kelly, A. M., Laroche, S., & Davis, S. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-12-05354.2003 · Cited by 361 · see citing works
The role of amygdala glutamate receptors in fear learning, fear-potentiated startle, and extinction
Walker, D. L., & Davis, M. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(01)00698-0 · Cited by 356 · see citing works
Psychophysiologic assessment of aversive conditioning in posttraumatic stress disorder
Peri, T., Ben‐Shakhar, G., Orr, S. P., & Shalev, A. Y. (2000) · Biological Psychiatry · doi:10.1016/s0006-3223(99)00144-4 · Cited by 349 · see citing works
Dopamine-mediated modulation of odour-evoked amygdala potentials during pavlovian conditioning
Rosenkranz, J. A., & Grace, A. A. (2002) · Nature · doi:10.1038/417282a · Cited by 348 · see citing works
Lesions in the bed nucleus of the stria terminalis disrupt corticosterone and freezing responses elicited by a contextual but not by a specific cue-conditioned fear stimulus
Sullivan, G. M., Apergis, J., Bush, D. E. A., Johnson, L. R., Hou, M., & Ledoux, J. E. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.06.015 · Cited by 327 · see citing works
Self-citation
Cellular and systems mechanisms of memory strength as a constraint on auditory fear reconsolidation
Wang, S., Alvares, L. D. O., & Nader, K. (2009) · Nature Neuroscience · doi:10.1038/nn.2350 · Cited by 305 · see citing works
Acquisition of Fear Extinction Requires Activation of NR2B-Containing NMDA Receptors in the Lateral Amygdala
Sotres-Bayon, F., Bush, D. E. A., & LeDoux, J. E. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301316 · Cited by 293 · see citing works
Behavioral profiles of inbred strains on novel olfactory, spatial and emotional tests for reference memory in mice
Holmes, A., Wrenn, C. C., Harris, A. P., Thayer, K. E., & Crawley, J. N. (2002) · Genes Brain & Behavior · doi:10.1046/j.1601-1848.2001.00005.x · Cited by 275 · see citing works
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
Dębiec, J., Bush, D. E. A., & LeDoux, J. E. (2011) · Depression and Anxiety · doi:10.1002/da.20803 · Cited by 218 · see citing works
Synapse-specific reconsolidation of distinct fear memories in the lateral amygdala
Doyère, V., Dębiec, J., Monfils, M.-H., Schafe, G. E., & LeDoux, J. E. (2007) · Nature Neuroscience · doi:10.1038/nn1871 · Cited by 200 · see citing works
Retrograde amnesia after hippocampal damage: Recent vs. remote memories in two tasks
Sutherland, R. J., Weisend, M. P., Mumby, D. G., Astur, R. S., Hanlon, F. M., Koerner, A., Thomas, M. J., Wu, Y., Moses, S. N., Cole, C., et al. (2001) · Hippocampus · doi:10.1002/1098-1063(2001)11:1 · Cited by 190 · see citing works
Visual Pathways Involved in Fear Conditioning Measured with Fear-Potentiated Startle: Behavioral and Anatomic Studies
Shi, C., & Davis, M. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-24-09844.2001 · Cited by 179 · see citing works
Genetics of Post-Traumatic Stress Disorder: Review and Recommendations for Genome-Wide Association Studies
Cornelis, M. C., Nugent, N. R., Amstadter, A. B., & Koenen, K. C. (2010) · Current Psychiatry Reports · doi:10.1007/s11920-010-0126-6 · Cited by 178 · see citing works
A Twin Study of the Genetics of Fear Conditioning
Hettema, J. M., Annas, P., Neale, M. C., Kendler, K. S., & Fredrikson, M. (2003) · Archives of General Psychiatry · doi:10.1001/archpsyc.60.7.702 · Cited by 175 · see citing works
Quantitative trait locus analysis of contextual fear conditioning in mice
Wehner, J. M., Radcliffe, R. A., Rosmann, S. T., Christensen, S. C., Rasmussen, D. L., Fulker, D. W., & Wiles, M. (1997) · Nature Genetics · doi:10.1038/ng1197-331 · Cited by 163 · see citing works
Genetics of PTSD: fear conditioning as a model for future research
Amstadter, A. B., Nugent, N. R., & Koenen, K. C. (2009) · Psychiatric Annals · doi:10.3928/00485713-20090526-01 · Cited by 150 · see citing works
Quantitative trait loci analysis affecting contextual conditioning in mice
Caldarone, B. J., Saavedra, C., Tartaglia, K., Wehner, J. M., Dudek, B. C., & Flaherty, L. A. (1997) · Nature Genetics · doi:10.1038/ng1197-335 · Cited by 148 · see citing works
Dendritic Spine Heterogeneity Determines Afferent-Specific Hebbian Plasticity in the Amygdala
Humeau, Y., Herry, C., Kemp, N., Shaban, H., Fourcaudot, E., Bissière, S., & Lüthi, A. (2005) · Neuron · doi:10.1016/j.neuron.2004.12.019 · Cited by 148 · see citing works
Convergent but temporally separated inputs to lateral amygdala neurons from the auditory thalamus and auditory cortex use different postsynaptic receptors: in vivo intracellular and extracellular recordings in fear conditioning pathways.Preprint
Li, X.-F., Stutzmann, G. E., & LeDoux, J. E. (1996) · Learning & Memory · doi:10.1101/lm.3.2-3.229 · Cited by 146 · see citing works
Differential Effects of Amygdala Lesions on Early and Late Plastic Components of Auditory Cortex Spike Trains during Fear Conditioning
Armony, J. L., Quirk, G. J., & LeDoux, J. E. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-07-02592.1998 · Cited by 143 · see citing works
Variant brain‐derived neurotrophic factor Val66Met endophenotypes: implications for posttraumatic stress disorder
Frielingsdorf, H., Bath, K. G., Soliman, F., Difede, J., Casey, B. J., & Lee, F. S. (2010) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2010.05722.x · Cited by 136 · see citing works
Gene‐environment interaction in posttraumatic stress disorder: An update
Koenen, K. C., Amstadter, A. B., & Nugent, N. R. (2009) · Journal of Traumatic Stress · doi:10.1002/jts.20435 · Cited by 129 · see citing works
Contribution of Ventrolateral Prefrontal Cortex to the Acquisition and Extinction of Conditioned Fear in Rats
Morgan, M. A., & LeDoux, J. E. (1999) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1999.3907 · Cited by 123 · see citing works
Relationship of a common polymorphism of the glucocorticoid receptor gene to traumatic memories and posttraumatic stress disorder in patients after intensive care therapy
Hauer, D., Weis, F. C., Papassotiropoulos, A., Schmoeckel, M., Beiras-Fernández, A., Lieke, J., Kaufmann, I., Kirchhoff, F., Vogeser, M., Roozendaal, B., et al. (2010) · Critical Care Medicine · doi:10.1097/ccm.0b013e318206bae6 · Cited by 115 · see citing works
An anatomically constrained neural network model of fear conditioning.
Armony, J. L., Servan‐Schreiber, D., Cohen, J. D., & LeDoux, J. E. (1995) · Behavioral Neuroscience · doi:10.1037//0735-7044.109.2.246 · Cited by 113 · see citing works
Fear conditioning and LTP in the lateral amygdala are sensitive to the same stimulus contingencies
Bauer, E. P., LeDoux, J. E., & Nader, K. (2001) · Nature Neuroscience · doi:10.1038/89465 · Cited by 112 · see citing works
Inbred mouse strain differences in the establishment of long-term fear memory
Balogh, S. A., & Wehner, J. M. (2003) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00279-6 · Cited by 97 · see citing works
An anatomically constrained neural network model of fear conditioning.
Armony, J. L., Servan‐Schreiber, D., Cohen, J. D., et al. (1995) · Behavioral Neuroscience · doi:10.1037/0735-7044.109.2.246 · Cited by 96 · see citing works
Selection for contextual fear conditioning affects anxiety‐like behaviors and gene expression
Ponder, C. A., Kliethermes, C. L., Drew, M. R., Muller, J., Das, K., Risbrough, V. B., Crabbe, J. C., Gilliam, T. C., & Palmer, A. A. (2007) · Genes, Brain and Behavior · doi:10.1111/j.1601-183x.2007.00306.x · Cited by 95 · see citing works
Self-citation
Post-traumatic stress behavioural responses in inbred mouse strains: can genetic predisposition explain phenotypic vulnerability?
Cohen, H., Geva, A. B., Matar, M. A., Zohar, J., & Kaplan, Z. (2007) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145707007912 · Cited by 89 · see citing works
Unconditioned stimulus pathways to the amygdala: Effects of lesions of the posterior intralaminar thalamus on foot-shock-induced c-Fos expression in the subdivisions of the lateral amygdala
Lanuza, E., Moncho-Bogani, J., & LeDoux, J. E. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.06.028 · Cited by 84 · see citing works
Impaired Pavlovian fear extinction is a common phenotype across genetic lineages of the 129 inbred mouse strain
Camp, M., Norcross, M. A., Whittle, N., Feyder, M. J., D’Hanis, W., Yilmazer‐Hanke, D., Singewald, N., & Holmes, A. (2009) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2009.00519.x · Cited by 69 · see citing works
Volition diminishes genetically mediated amygdala hyperreactivity
Schardt, D. M., Erk, S., Nüsser, C., Nöthen, M. M., Cichon, S., Rietschel, M., Treutlein, J., Goschke, T., & Walter, H. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.11.078 · Cited by 69 · see citing works
The circuit of fear
Sah, P., & Westbrook, R. F. (2008) · Nature · doi:10.1038/454589a · Cited by 66 · see citing works
Phosphorylation of ERK/MAP kinase is required for long-term potentiation in anatomically restricted regions of the lateral amygdala in vivoPreprint
Schafe, G. E., Swank, M. W., Rodrigues, S. M., Dębiec, J., & Doyère, V. (2008) · Learning & Memory · doi:10.1101/lm.746808 · Cited by 64 · see citing works
Effect of noxious somesthetic stimulation on the activity of neurons of the nucleus centralis of the amygdala
Bernard, J., Huang, G.-F., & Besson, J. (1990) · Brain Research · doi:10.1016/0006-8993(90)91512-f · Cited by 57 · see citing works
Fearfulness in a large N/Nih genetically heterogeneous rat stock: Differential profiles of timidity and defensive flight in males and females
López-Aumatell, R., Guitart‐Masip, M., Vicens-Costa, E., Giménez‐Llort, L., Valdar, W. S. J., Johannesson, M., Jonathan Flint, C., Tobeña, A., & Fernández‐Teruel, A. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.10.015 · Cited by 53 · see citing works
Induction- and conditioning-protocol dependent involvement of NR2B-containing NMDA receptors in synaptic potentiation and contextual fear memory in the hippocampal CA1 region of rats
Zhang, X.-H., Wu, L., Gong, B., Ren, M., Li, B.-M., & Zhuo, M. (2008) · Molecular Brain · doi:10.1186/1756-6606-1-9 · Cited by 53 · see citing works
Identification of plasticity‐associated genes regulated by Pavlovian fear conditioning in the lateral amygdala
Ploski, J. E., Park, K. W., Ping, J., Monsey, M. S., & Schafe, G. E. (2009) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2009.06491.x · Cited by 52 · see citing works
Genetic relationship between anxiety-related and fear-related behaviors in BXD recombinant inbred mice
Brigman, J. L., Mathur, P., Lu, L., Williams, R. W., & Holmes, A. (2008) · Behavioural Pharmacology · doi:10.1097/fbp.0b013e32830c368c · Cited by 49 · see citing works
PTSD and dopaminergic genes, DRD2 and DAT, in multigenerational families exposed to the Spitak earthquake
Bailey, J. N., Goenjian, A. K., Noble, E. P., Walling, D. P., Ritchie, T. L., & Goenjian, H. A. (2010) · Psychiatry Research · doi:10.1016/j.psychres.2010.04.043 · Cited by 46 · see citing works
PTSD and traumatic stress
Ursano, R. J., Zhang, L., He, L., Johnson, L. R., Carlton, J. R., Fullerton, C. S., & Benedek, D. M. (2009) · Brain Research · doi:10.1016/j.brainres.2009.03.030 · Cited by 45 · see citing works
Self-citation
Distinct Functional Characteristics of the Lateral/Basolateral Amygdala GABAergic System in C57BL/6J and DBA/2J Mice
DuBois, D. W., Perlegas, A. S., Floyd, D. W., Weiner, J. L., & McCool, B. A. (2006) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.105.100552 · Cited by 43 · see citing works
Pavlovian Fear Conditioning Activates a Common Pattern of Neurons in the Lateral Amygdala of Individual Brains
Bergstrom, H. C., McDonald, C. G., & Johnson, L. R. (2011) · PLoS ONE · doi:10.1371/journal.pone.0015698 · Cited by 42 · see citing works
Self-citation
Confirmation of Contextual Fear Conditioning QTLs by Short-Term Selection
Radcliffe, R. A., Lowe, M. V., & Wehner, J. M. (2000) · Behavior Genetics · doi:10.1023/a:1001910107167 · Cited by 40 · see citing works
Fear-Potentiated Startle Response in Mice
McCaughran, J. A., Bell, J., & HITZEMANN, R. J. (2000) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(99)00216-6 · Cited by 39 · see citing works
A recurrent network in the lateral amygdala: a mechanism for coincidence detection
Johnson, L. R. (2008) · Frontiers in Neural Circuits · doi:10.3389/neuro.04.003.2008 · Cited by 36 · see citing works
Self-citation
Fear and Anxiety: The Benefits of Translational Research
Ruiz, P. (2004) · American Journal of Psychiatry · doi:10.1176/appi.ajp.162.1.200 · Cited by 36 · see citing works
A mutant mouse with a highly specific contextual fear-conditioning deficit found in an N-ethyl-N-nitrosourea (ENU) mutagenesis screenPreprint
Reijmers, L. G. J. E., Coats, J., Pletcher, M. T., Wiltshire, T., Tarantino, L. M., & Mayford, M. R. (2006) · Learning & Memory · doi:10.1101/lm.98606 · Cited by 35 · see citing works
Heritabilities of symptoms of posttraumatic stress disorder, anxiety, and depression in earthquake exposed Armenian families
Goenjian, A. K., Noble, E. P., Walling, D. P., Goenjian, H. A., Karayan, I., Ritchie, T. L., & Bailey, J. N. (2008) · Psychiatric Genetics · doi:10.1097/ypg.0b013e3283060f48 · Cited by 33 · see citing works
Hebbian reverberations in emotional memory micro circuits
Johnson, L. R., LeDoux, J. E., & Doyère, V. (2009) · Figshare · Cited by 30 · see citing works
Self-citation
Genetic architecture of fear conditioning in chromosome substitution strains: relationship to measures of innate (unlearned) anxiety-like behavior
Ponder, C. A., Munoz, M. B., Gilliam, T. C., & Palmer, A. A. (2007) · Mammalian Genome · doi:10.1007/s00335-007-9013-9 · Cited by 25 · see citing works
Self-citation
Rapid Selection Response for Contextual Fear Conditioning in a Cross Between C57BL/6J and A/J: Behavioral, QTL and Gene Expression Analysis
Ponder, C. A., Huded, C. P., Munoz, M. B., Gulden, F. O., Gilliam, T. C., & Palmer, A. A. (2008) · Behavior Genetics · doi:10.1007/s10519-008-9203-6 · Cited by 24 · see citing works
Self-citation
Fear memory and the amygdala: insights from a molecular perspective
Stork, O., & Pape, H. (2002) · Cell and Tissue Research · doi:10.1007/s00441-002-0656-2 · Cited by 23 · see citing works
Genes and neurons: molecular insights to fear and anxiety
Stoppel, C., Albrecht, A., Pape, H., & Stork, O. (2006) · Genes, Brain and Behavior · doi:10.1111/j.1601-183x.2006.00229.x · Cited by 20 · see citing works
The Genetic Covariation Between Fear Conditioning and Self-Report Fears
Hettema, J. M., Annas, P., Neale, M. C., Fredrikson, M., & Kendler, K. S. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.06.009 · Cited by 15 · see citing works
The anatomy of fear: microcircuits of the lateral amygdala
Johnson, L. R., & LeDoux, J. E. (2004) · QUT ePrints (Queensland University of Technology) · Cited by 11 · see citing works
Self-citation
Pre-Traumatic Vaccination Intervention: Can Dissociative Symptoms be Reduced?
Essar, N., Palgi, Y., Saar, R., & Ben‐Ezra, M. (2010) · Prehospital and Disaster Medicine · doi:10.1017/s1049023x00008165 · Cited by 8 · see citing works

Flagged first, then by citations

Sorted by citations

Psychometric Evaluation of the Moral Injury Events Scale
Nash, W. P., Carper, T. L. M., Mills, M. A., Au, T. M., Goldsmith, A. A., & Litz, B. T. (2013) · Military Medicine · doi:10.7205/milmed-d-13-00017 · Cited by 620 · see citing works
From Pavlov to PTSD: The extinction of conditioned fear in rodents, humans, and anxiety disorders
VanElzakker, M. B., Kathryn Dahlgren, M., Caroline Davis, F., Dubois, S., & Shin, L. M. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.11.014 · Cited by 482 · see citing works
Moral Injury: A Mechanism for War-Related Psychological Trauma in Military Family Members
Nash, W. P., & Litz, B. T. (2013) · Clinical Child and Family Psychology Review · doi:10.1007/s10567-013-0146-y · Cited by 259 · see citing works
Single-Prolonged Stress: A Review of Two Decades of Progress in a Rodent Model of Post-traumatic Stress Disorder
Lisieski, M. J., Eagle, A. L., Conti, A. C., Liberzon, I., & Perrine, S. A. (2018) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2018.00196 · Cited by 224 · see citing works
Epigenetic Mechanisms in Learned Fear: Implications for PTSD
Zovkic, I. B., & Sweatt, J. D. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2012.79 · Cited by 186 · see citing works
The centrality of fear extinction in linking risk factors to PTSD: A narrative review
Zuj, D. V., Palmer, M. A., Lommen, M. J. J., & Felmingham, K. L. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.07.014 · Cited by 141 · see citing works
Ketamine accelerates fear extinction via mTORC1 signaling
Girgenti, M. J., Ghosal, S., Lopresto, D., Taylor, J. R., & Duman, R. S. (2016) · Neurobiology of Disease · doi:10.1016/j.nbd.2016.12.026 · Cited by 123 · see citing works
Psychosocial animal model of PTSD produces a long-lasting traumatic memory, an increase in general anxiety and PTSD-like glucocorticoid abnormalities
Zoladz, P. R., Fleshner, M., & Diamond, D. M. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.02.007 · Cited by 120 · see citing works
Fear load: The psychophysiological over-expression of fear as an intermediate phenotype associated with trauma reactions
Norrholm, S. D., Glover, E. M., Stevens, J. S., Fani, N., Galatzer‐Levy, I. R., Bradley, B., Ressler, K. J., & Jovanović, T. (2014) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2014.11.005 · Cited by 115 · see citing works
Animal Models of PTSD: A Critical Review
Flandreau, E. I., & Tóth, M. (2017) · Current topics in behavioral neurosciences · doi:10.1007/7854_2016_65 · Cited by 108 · see citing works
A Review of the Relationship Between Emotional Learning and Memory, Sleep, and PTSD
Colvonen, P. J., Straus, L. D., Acheson, D. T., & Gehrman, P. (2019) · Current Psychiatry Reports · doi:10.1007/s11920-019-0987-2 · Cited by 109 · see citing works
The advent of fear conditioning as an animal model of post-traumatic stress disorder: Learning from the past to shape the future of PTSD research
Bienvenu, T., Déjean, C., Jercog, D., Aouizerate, B., Lemoine, M., & Herry, C. (2021) · Neuron · doi:10.1016/j.neuron.2021.05.017 · Cited by 107 · see citing works
Conditioned fear associated phenotypes as robust, translational indices of trauma-, stressor-, and anxiety-related behaviors
Briscione, M. A., Jovanovic, T., & Norrholm, S. D. (2014) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2014.00088 · Cited by 105 · see citing works
The Current Evidence for Acute Stress Disorder
Bryant, R. A. (2018) · Current Psychiatry Reports · doi:10.1007/s11920-018-0976-x · Cited by 105 · see citing works
The neurocircuitry of remote cued fear memory
Bergstrom, H. C. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.09.028 · Cited by 92 · see citing works
Reflections on the interaction of psychogenic stress systems in humans: The stress coherence/compensation model
Andrews, J., Ali, N., & Pruessner, J. C. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.02.010 · Cited by 87 · see citing works
Fear Conditioning, Safety Learning, and Sleep in Humans
Marshall, A. J., Acheson, D. T., Risbrough, V. B., Straus, L. D., & Drummond, S. P. A. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0478-14.2014 · Cited by 86 · see citing works
The clinical applications and practical relevance of human conditioning paradigms for posttraumatic stress disorder
Zuj, D., & Norrholm, S. (2019) · Progress in Neuro-psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2018.08.014 · Cited by 78 · see citing works
The neuroenergetics of stress hormones in the hippocampus and implications for memory
Osborne, D. M., Pearson-Leary, J., & McNay, E. C. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00164 · Cited by 78 · see citing works
Diverse therapeutic developments for post-traumatic stress disorder (PTSD) indicate common mechanisms of memory modulation
Raut, S. B., Marathe, P. A., van Eijk, L., Eri, R. D., Ravindran, M., Benedek, D. M., Ursano, R. J., Canales, J. J., & Johnson, L. R. (2022) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2022.108195 · Cited by 71 · see citing works
Self-citation
nNOS and Neurological, Neuropsychiatric Disorders: A 20-Year Story
Zhu, L., Li, F. Y., & Zhu, D. (2023) · Neuroscience Bulletin · doi:10.1007/s12264-023-01060-7 · Cited by 51 · see citing works
Soldiers With Posttraumatic Stress Disorder See a World Full of Threat: Magnetoencephalography Reveals Enhanced Tuning to Combat-Related Cues
Todd, R. M., MacDonald, M. J., Sedge, P. A., Robertson, A., Jetly, R., Taylor, M. J., & Pang, E. W. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.05.011 · Cited by 50 · see citing works
Measuring the biological embedding of racial trauma among Black Americans utilizing the RDoC approach
Carter, S. E., Gibbons, F. X., & Beach, S. R. H. (2021) · Development and Psychopathology · doi:10.1017/s0954579421001073 · Cited by 47 · see citing works
Genome-Wide Association for Fear Conditioning in an Advanced Intercross Mouse Line
Parker, C. C., Sokoloff, G., Cheng, R., & Palmer, A. A. (2012) · Behavior Genetics · doi:10.1007/s10519-011-9524-8 · Cited by 47 · see citing works
Self-citation
Comparative effects of intranasal neuropeptide Y and HS014 in preventing anxiety and depressive-like behavior elicited by single prolonged stress
Sabban, E. L., Serova, L. I., Alaluf, L. G., Lauková, M., & Peddu, C. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.12.038 · Cited by 47 · see citing works
Effects of propranolol on the modification of trauma memory reconsolidation in PTSD patients: A systematic review and meta-analysis
Raut, S. B., Canales, J. J., Ravindran, M., Eri, R. D., Benedek, D. M., Ursano, R. J., & Johnson, L. R. (2022) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2022.03.045 · Cited by 45 · see citing works
Self-citation
Epigenetic Mechanisms Are Involved in the Regulation of Ethanol Consumption in Mice
Qiang, M., Li, J. G., Denny, A. D., Yao, J.-M., Lieu, M., Zhang, K., & Carreon, S. (2015) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyu072 · Cited by 45 · see citing works
The Research Domain Criteria (RDoC) Project and Studies of Risk and Resilience in Maltreated Children
Kaufman, J., Gelernter, J. E., Hudziak, J. J., Tyrka, A. R., & Coplan, J. D. (2015) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2015.06.001 · Cited by 45 · see citing works
A critical review of negative affect and the application of CBT for PTSD
Brown, W. J., Dewey, D., Bunnell, B. E., Boyd, S. J., Wilkerson, A. K., Mitchell, M. A., & Bruce, S. E. (2018) · Trauma, Violence, & Abuse · doi:10.1177/1524838016650188 · Cited by 43 · see citing works
An organization of visual and auditory fear conditioning in the lateral amygdala
Bergstrom, H. C., & Johnson, L. R. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.07.008 · Cited by 45 · see citing works
Self-citation
A Rodent Model of Exposure Therapy: The Use of Fear Extinction as a Therapeutic Intervention for PTSD
Paredes, D., & Morilak, D. A. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00046 · Cited by 41 · see citing works
Neuroepigenetics of Post-Traumatic Stress Disorder
Kim, G. S., Smith, A. K., Nievergelt, C. M., & Uddin, M. (2018) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2018.04.001 · Cited by 37 · see citing works
Posttraumatic Stress Disorder: Perspectives for the Use of Deep Brain Stimulation
Reznikov, R., & Hamani, C. (2016) · Neuromodulation Technology at the Neural Interface · doi:10.1111/ner.12551 · Cited by 37 · see citing works
PSD95 and nNOS interaction as a novel molecular target to modulate conditioned fear: relevance to PTSD
Li, L., Dustrude, E. T., Haulcomb, M. M., de Abreu, A. R. R., Fitz, S. D., Johnson, P. L., Thakur, G. A., Molosh, A. I., Lai, Y. Y., & Shekhar, A. (2018) · Translational Psychiatry · doi:10.1038/s41398-018-0208-5 · Cited by 37 · see citing works
Neuromodulation Strategies in Post-Traumatic Stress Disorder: From Preclinical Models to Clinical Applications
Gouveia, F. V., Gidyk, D. C., Giacobbe, P., Ng, E., Meng, Y., Davidson, B., Abrahão, A., Lipsman, N., & Hamani, C. (2019) · Brain Sciences · doi:10.3390/brainsci9020045 · Cited by 37 · see citing works
Rethinking mental disorders: The role of learning and brain plasticity
Morris, S. E., Rumsey, J. M., & Cuthbert, B. N. (2014) · Restorative Neurology and Neuroscience · doi:10.3233/rnn-139015 · Cited by 35 · see citing works
The Formation of a Neural Fear Network in Posttraumatic Stress Disorder
Wilker, S., & Kolassa, I. (2013) · Clinical Psychological Science · doi:10.1177/2167702613479583 · Cited by 35 · see citing works
Clinical significance of pericardial effusion after heart transplantation.
Vandenberg, B. F., Mohanty, P. K., Craddock, K., Barnhart, G. R., Hanrahan, J. S., Szentpetery, S., & Lower, R. R. (1988) · PubMed · Cited by 34 · see citing works
APT1-Mediated Depalmitoylation Regulates Hippocampal Synaptic Plasticity
Shen, Z.-C., Xia, Z.-X., Liu, J.-M., Zheng, J.-Y., Luo, Y.-F., Yang, H., Li, M.-D., Cao, T., Liu, H.-P., Jin, G.-L., et al. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.1741-21.2022 · Cited by 32 · see citing works
Acetazolamide impairs fear memory consolidation in rodents
Yang, M., Chien, W., Lu, D., Liou, H., & Fu, W. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.11.031 · Cited by 31 · see citing works
Characterizing the nature of emotional-associative learning deficits in panic disorder: An fMRI study on fear conditioning, extinction training and recall
Schwarzmeier, H., Kleint, N. I., Wïttchen, H., Ströhle, A., Hamm, A. O., & Lueken, U. (2018) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2018.11.1108 · Cited by 31 · see citing works
Ketamine reverses the impaired fear memory extinction and accompanied depressive-like behaviors in adolescent mice
Wei, M.-D., Wang, Y., Lu, K., Lv, B.-J., Wang, Y., & Chen, W. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.112342 · Cited by 30 · see citing works
Activation of Sigma-1 receptor ameliorates anxiety-like behavior and cognitive impairments in a rat model of post-traumatic stress disorder
Ji, L.-L., Peng, J., Fu, C.-H., Cao, D., Li, D., Tong, L., & Wang, Z. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.05.056 · Cited by 30 · see citing works
Behavioral evaluation of eight rat lines selected for high and low anxiety-related responses
Gomes, V. D. C., Hassan, W., Maisonnette, S. S., Johnson, L. R., Ramos, A., & Landeira-Fernández, J. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.09.028 · Cited by 29 · see citing works
Self-citation
Neurons Activated During Fear Memory Consolidation and Reconsolidation are Mapped to a Common and New Topography in the Lateral Amygdala
Bergstrom, H. C., McDonald, C. G., Dey, S., Fernandez, G. M., & Johnson, L. R. (2013) · Brain Topography · doi:10.1007/s10548-012-0266-6 · Cited by 29 · see citing works
Self-citation
A conceptual framework for a neurophysiological basis of art therapy for PTSD
Malhotra, B., Jones, L. C., Spooner, H., Levy, C. E., Kaimal, G., & Williamson, J. B. (2024) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2024.1351757 · Cited by 26 · see citing works
Contextual Fear Extinction Induces Hippocampal Metaplasticity Mediated by Metabotropic Glutamate Receptor 5
Stansley, B. J., Fisher, N. M., Gogliotti, R. G., Lindsley, C. W., Conn, P. J., & Niswender, C. M. (2017) · Cerebral Cortex · doi:10.1093/cercor/bhx282 · Cited by 23 · see citing works
Chemogenetic stimulation of the infralimbic cortex reverses alcohol-induced fear memory overgeneralization
Scarlata, M., Lee, S. H., Lee, D., Kandigian, S. E., Hiller, A. J., Dishart, J. G., Mintz, G. E., Wang, Z., Coste, G., Mousley, A., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-43159-w · Cited by 26 · see citing works
Bromodomain and Extra-Terminal Proteins in Brain Physiology and Pathology: BET-ing on Epigenetic Regulation
Martella, N., Pensabene, D., Varone, M., Colardo, M., Petraroia, M., Sergio, W., Rosa, P. L., Moreno, S., & Segatto, M. (2023) · Biomedicines · doi:10.3390/biomedicines11030750 · Cited by 26 · see citing works
Thinking of attachment figures blocks differential fear conditioning
Toumbelekis, M., Liddell, B. J., & Bryant, R. A. (2018) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsy065 · Cited by 24 · see citing works
Environmental enrichment mitigates PTSD-like behaviors in adult male rats exposed to early life stress by regulating histone acetylation in the hippocampus and amygdala
Xu, H., Li, B., Li, L., Fan, Z., Gong, X., Wu, L., & Yan, C. (2022) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2022.07.067 · Cited by 22 · see citing works
Microtopography of fear memory consolidation and extinction retrieval within prefrontal cortex and amygdala
Jacques, A., Chaaya, N., Hettiarachchi, C., Carmody, M.-L., Beecher, K., Belmer, A., Chehrehasa, F., Bartlett, S. E., Battle, A. R., & Johnson, L. R. (2019) · Psychopharmacology · doi:10.1007/s00213-018-5068-4 · Cited by 23 · see citing works
Self-citation
Epidemiology and Prevention of Combat-Related Post-Traumatic Stress in OEF/OIF/OND Service Members
Hermann, B. A., Shiner, B. R., & Friedman, M. J. (2012) · Military Medicine · doi:10.7205/milmed-d-12-00114 · Cited by 22 · see citing works
Traits of fear resistance and susceptibility in an advanced intercross line
McGuire, J. L., Bergstrom, H. C., Parker, C. C., Le, T., Morgan, M. A., Tang, H., Selwyn, R. G., Silva, A. C., Choi, K. H., Ursano, R. J., et al. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12337 · Cited by 21 · see citing works
Self-citation
Rodent Gymnastics: Neurobehavioral Assays in Ischemic Stroke
Nampoothiri, S. S., Potluri, T., Subramanian, H., & Rajanikant, G. K. (2016) · Molecular Neurobiology · doi:10.1007/s12035-016-0195-6 · Cited by 21 · see citing works
Study on the mechanism of TMRK electroacupuncture in repairing synaptic plasticity in amygdala and hippocampus to relieve fear memory in PTSD rats
Li, M., Li, K., Zhang, H., & Jiang, Y. (2019) · Technology and Health Care · doi:10.3233/thc-199038 · Cited by 21 · see citing works
Posttraumatic Stress Disorder
Wynn, G. H., Benedek, D. M., Johnson, L. R., Choi, K. H., Zhang, L., Hu, X., Pollard, H. B., & Ursano, R. J. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-802381-5.00036-1 · Cited by 21 · see citing works
Self-citation
Neural circuits involved in the renewal of extinguished fear
Chen, W.-H., Wang, Y., Wang, X.-Q., & Li, H. (2017) · IUBMB Life - A Journal of the International Union of Biochemistry and Molecular Biology · doi:10.1002/iub.1636 · Cited by 20 · see citing works
Resveratrol: A Multifaceted Guardian against Anxiety and Stress Disorders—An Overview of Experimental Evidence
Цейликман, В. Э., Tseilikman, O. B., Yegorov, O. N., Brichagina, A. A., Karpenko, M. N., Tseilikman, D., Shatilov, V. A., Zhukov, M. S., & Novak, J. (2024) · Nutrients · doi:10.3390/nu16172856 · Cited by 19 · see citing works
Mice heterozygous for an inactivated allele of the schizophrenia associated Brd1 gene display selective cognitive deficits with translational relevance to schizophrenia
Qvist, P., Rajkumar, A. P., Redrobe, J. P., Nyegaard, M., Christensen, J., Mors, O. N., Wegener, G., Didriksen, M., & Børglum, A. D. (2017) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2017.03.009 · Cited by 19 · see citing works
Effects of repeated anodal transcranial direct current stimulation on auditory fear extinction in C57BL/6J mice
Schuerbeek, A. V., Vanderhasselt, M., Baeken, C., Pierre, A., Smolders, I. J., Waes, V. V., & Bundel, D. D. (2021) · Brain stimulation · doi:10.1016/j.brs.2021.01.005 · Cited by 18 · see citing works
Hypobaric hypoxia induced fear and extinction memory impairment and effect of Ginkgo biloba in its amelioration: Behavioral, neurochemical and molecular correlates
Kumari, P., Wadhwa, M., Chauhan, G., Alam, S., Roy, K., Jha, P. K., Kishore, K., Ray, K., Kumar, S., Nag, T. C., et al. (2020) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.112595 · Cited by 18 · see citing works
Cued and contextual fear conditioning in BTBR mice is improved with training or atomoxetine
Stapley, N. W., Guariglia, S. R., & Chadman, K. K. (2013) · Neuroscience Letters · doi:10.1016/j.neulet.2013.06.032 · Cited by 17 · see citing works
Behavioral and neural mechanisms of latent inhibitionPreprint
Miller, D. B., Rassaby, M. M., Collins, K. A., & Milad, M. R. (2022) · Learning & Memory · doi:10.1101/lm.053439.121 · Cited by 17 · see citing works
Adolescence alcohol exposure impairs fear extinction and alters medial prefrontal cortex plasticity
Lawson, K., Scarlata, M. J., Cho, W. C., Mangan, C., Petersen, D., Thompson, H. M., Ehnstrom, S., Mousley, A. L., Bezek, J. L., & Bergstrom, H. C. (2022) · Neuropharmacology · doi:10.1016/j.neuropharm.2022.109048 · Cited by 16 · see citing works
A prolonged stress rat model recapitulates some PTSD-like changes in sleep and neuronal connectivity
Lo, Y., Yi, P.-L., Hsiao, Y., Lee, T.-Y., & Chang, F. (2023) · Communications Biology · doi:10.1038/s42003-023-05090-9 · Cited by 16 · see citing works
Habenula kisspeptin retrieves morphine impaired fear memory in zebrafish
Sivalingam, M., Ogawa, S., & Parhar, I. S. (2020) · Scientific Reports · doi:10.1038/s41598-020-76287-9 · Cited by 16 · see citing works
Developing Multimodal Dynamic Functional Connectivity as a Neuroimaging Biomarker
Kundu, S., Jin, M., & Stevens, J. S. (2021) · Brain Connectivity · doi:10.1089/brain.2020.0900 · Cited by 15 · see citing works
Secure attachment priming protects against relapse of fear in young adults
Toumbelekis, M., Liddell, B. J., & Bryant, R. A. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01715-x · Cited by 15 · see citing works
Eyeblink classical conditioning and post-traumatic stress disorder – a model systems approach
Schreurs, B. G. (2015) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2015.00050 · Cited by 14 · see citing works
Multiple factors contribute to flight behaviors during fear conditioning
Furuyama, T., Imayoshi, A., Iyobe, T., Ono, M., Ishikawa, T., Ozaki, N., Kato, N., & Yamamoto, R. (2023) · Scientific Reports · doi:10.1038/s41598-023-37612-0 · Cited by 14 · see citing works
Mice selectively bred for High and Low fear behavior show differences in the number of pMAPK (p44/42 ERK) expressing neurons in lateral amygdala following Pavlovian fear conditioning
Coyner, J. L., McGuire, J. L., Parker, C. C., Ursano, R. J., Palmer, A. A., & Johnson, L. R. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.06.010 · Cited by 16 · see citing works
Self-citation
Apelin-13 Impaires Acquisition but Not Consolidation or Expression of Contextual Fear in Rats
Han, L., Luo, H., Huang, F., Tian, S., & Qin, X. (2016) · Neurochemical Research · doi:10.1007/s11064-016-1948-3 · Cited by 13 · see citing works
Pavlovian Olfactory Fear Conditioning: Its Neural Circuity and Importance for Understanding Clinical Fear-Based Disorders
Hakim, M., Battle, A. R., Belmer, A., Bartlett, S. E., Johnson, L. R., & Chehrehasa, F. (2019) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2019.00221 · Cited by 13 · see citing works
Self-citation
Prolonged contextual fear memory in AMPA receptor palmitoylation-deficient mice
Oota-Ishigaki, A., Takao, K., Yamada, D., Sekiguchi, M., Itoh, M., Koshidata, Y., Abe, M., Natsume, R., Kaneko, M., Adachi, T., et al. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-022-01347-9 · Cited by 12 · see citing works
A large QTL for fear and anxiety mapped using an F2 cross can be dissected into multiple smaller QTLs
Parker, C. C., Sokoloff, G., Leung, E., Kirkpatrick, S. L., & Palmer, A. A. (2013) · Genes Brain & Behavior · doi:10.1111/gbb.12064 · Cited by 12 · see citing works
Self-citation
Differential Histone Acetylation in Sub-Regions of Bed Nucleus of the Stria Terminalis Underlies Fear Consolidation and Extinction
Ranjan, V., Singh, S., Siddiqui, S. A., Tripathi, S., Khan, M. Y., & Prakash, A. (2017) · Psychiatry Investigation · doi:10.4306/pi.2017.14.3.350 · Cited by 11 · see citing works
Early life social experience affects adulthood fear extinction deficit and associated dopamine profile abnormalities in a rat model of PTSD
Lin, C.-C., Chen, T., Cheng, P., & Liu, Y. (2020) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.109914 · Cited by 12 · see citing works
A dendritic organization of lateral amygdala neurons in fear susceptible and resistant mice
Gomes, V. D. C., Bergstrom, H. C., McGuire, J. L., Parker, C. C., Coyner, J. L., Landeira-Fernández, J., Ursano, R. J., Palmer, A. A., & Johnson, L. R. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.11.010 · Cited by 11 · see citing works
Self-citation
The clinically relevant MEK inhibitor mirdametinib combined with D-cycloserine and prediction error disrupts fear memory in PTSD models
Raut, S. B., Joly, F., Haass, N. K., Eri, R. D., Canales, J. J., Benedek, D. M., Ursano, R. J., & Johnson, L. R. (2024) · Translational Psychiatry · doi:10.1038/s41398-024-03190-6 · Cited by 10 · see citing works
Self-citation
Impact of Mephedrone on Fear Memory in Adolescent Rats: Involvement of Matrix Metalloproteinase-9 (MMP-9) and N-Methyl-D-aspartate (NMDA) Receptor
Grochecki, P., Smaga, I., Wydra, K., Marszałek‐Grabska, M., Słowik, T., Kędzierska, E., Listos, J., Gibuła‐Tarłowska, E., Filip, M., & Kotlinska, J. H. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24031941 · Cited by 10 · see citing works
Fear conditioning in mouse lines genetically selected for binge-like ethanol drinking
Crabbe, J. C., Schlumbohm, J. P., Hack, W. R., Barkley‐Levenson, A. M., Metten, P., & Lattal, K. M. (2016) · Alcohol · doi:10.1016/j.alcohol.2016.01.004 · Cited by 10 · see citing works
Functional Neuronal Topography: A Statistical Approach to Micro Mapping Neuronal Location
Jacques, A., Wright, A., Chaaya, N., Overell, A., Bergstrom, H. C., McDonald, C. G., Battle, A. R., & Johnson, L. R. (2018) · Frontiers in Neural Circuits · doi:10.3389/fncir.2018.00084 · Cited by 11 · see citing works
Self-citation
Localization of Contextual and Context Removed Auditory Fear Memory within the Basolateral Amygdala Complex
Chaaya, N., Jacques, A., Belmer, A., Richard, D. J., Bartlett, S. E., Battle, A. R., & Johnson, L. R. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.12.004 · Cited by 10 · see citing works
Self-citation
Sex differences in BNST signaling and BNST CRF in fear processingPreprint
Hon, O. J., Neira, S., Flanigan, M. E., Roland, A. V., Caira, C. M., Sides, T. R., D'Ambrosio, S. L., Lee, S., Simpson, Y., Buccini, M. C., et al. (2023) · eLife · doi:10.7554/elife.89189 · Cited by 10 · see citing works
Neural Circuits for Fear Relapse
Goode, T. D., Jin, J., & Maren, S. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-813693-5.00010-1 · Cited by 9 · see citing works
Sex differences in acetylcholinesterase modulation during spatial and fear memory extinction in the amygdala; an animal study in the single prolonged stress model of PTSD
Mohammadi-Farani, A., Farhangian, S., & Shirooie, S. (2022) · Research in Pharmaceutical Sciences · doi:10.4103/1735-5362.359435 · Cited by 9 · see citing works
Acute stress disorder and associated factors among adult trauma patients in Ethiopia: a multi-institutional study
Hagos, T. G., Tamir, T. T., Workneh, B. S., Abrha, N. N., Demissie, N. G., & Gebeyehu, D. A. (2024) · BMC Psychiatry · doi:10.1186/s12888-024-05861-6 · Cited by 8 · see citing works
Brd4 participates in epigenetic regulation of the extinction of remote auditory fear memory
Huang, F., Li, F., Zhang, W., Li, S.-J., Yang, Z.-H., Yang, T., Qi, J., Duan, Q., & Li, C.-Q. (2021) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2021.107383 · Cited by 8 · see citing works
Editorial: How Fear and Stress Shape the Mind
Johnson, L. R. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2016.00024 · Cited by 8 · see citing works
Self-citation
Effects of extinction treatments on the reduction of conditioned responding and conditioned hyperarousal in a rabbit model of posttraumatic stress disorder (PTSD).
Burhans, L. B., Smith‐Bell, C. A., & Schreurs, B. G. (2015) · Behavioral Neuroscience · doi:10.1037/bne0000092 · Cited by 7 · see citing works
Paeoniflorin exerts anti-PTSD effects in adult rats by modulating hippocampus and amygdala histone acetylation modifications in response to early life stress
Xu, H., Zhang, T., Li, L., Qu, Y., Li, L., Yan, Y., Wu, L., & Yan, C. (2024) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2024.111035 · Cited by 7 · see citing works
Memory Reconsolidation Therapy for Police Officers with Post-traumatic Stress Disorder
Kerswell, N. L., Strodl, E. S., Hawkins, D., & Johnson, L. R. (2020) · Journal of Police and Criminal Psychology · doi:10.1007/s11896-020-09363-5 · Cited by 9 · see citing works
Self-citation
Secure attachment primes reduce fear consolidation
Toumbelekis, M., Liddell, B. J., & Bryant, R. A. (2021) · Depression and Anxiety · doi:10.1002/da.23166 · Cited by 7 · see citing works
Blockade of D-serine signaling and adult hippocampal neurogenesis attenuates remote contextual fear memory following multiple memory retrievals in male mice
Inoue, R., Ni, X., & Mori, H. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.1030702 · Cited by 6 · see citing works
Pharmacological Implications of Adjusting Abnormal Fear Memory: Towards the Treatment of Post-Traumatic Stress Disorder
Lin, C.-C., & Liu, Y. (2022) · Pharmaceuticals · doi:10.3390/ph15070788 · Cited by 5 · see citing works
Emotionales Lernen: Ein naturalistisches experimentelles Paradigma zur Untersuchung von Angsterwerb und Extinktion mittels aversiver Filme
Wegerer, M., Jens Blechert, A., & Wilhelm, F. H. (2013) · Zeitschrift für Psychiatrie Psychologie und Psychotherapie · doi:10.1024/1661-4747/a000146 · Cited by 5 · see citing works
Adapting rodent cued threat conditioning to planarians: Memory acquisition, consolidation, and reconsolidation
James, F. L. J., Ahamed, S. K., Yang, C., Thinley, J., Vicario, C. M., Canales, J. J., Sohal, S. S., Wilson, R., Johnson, L. R., & Caruso, V. (2025) · Behavioural Processes · doi:10.1016/j.beproc.2025.105321 · Cited by 4 · see citing works
Self-citation
Retrieval of olfactory fear memory alters cell proliferation and expression of pCREB and pMAPK in the corticomedial amygdala and piriform cortex
Hakim, M., Beecher, K., Jacques, A., Chaaya, N., Belmer, A., Battle, A. R., Johnson, L. R., Bartlett, S. E., & Chehrehasa, F. (2022) · Chemical Senses · doi:10.1093/chemse/bjac021 · Cited by 4 · see citing works
Self-citation
Genetic influences on posttraumatic stress disorder (PTSD): inspirations from a memory-centered approach.
Wilker, S., & Kolassa, I. (2012) · PubMed · Cited by 4 · see citing works

Genes and neurons: molecular insights to fear and anxiety
Stoppel, C., Albrecht, A., Pape, H., & Stork, O. (2006) · Genes, Brain and Behavior · doi:10.1111/j.1601-183x.2006.00229.x · Cited by 20 · see citing works
Fear conditioning, synaptic plasticity and the amygdala: implications for posttraumatic stress disorder
Mahan, A. L., & Ressler, K. J. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.06.007 · Cited by 616 · see citing works
The Formation of a Neural Fear Network in Posttraumatic Stress Disorder
Wilker, S., & Kolassa, I. (2013) · Clinical Psychological Science · doi:10.1177/2167702613479583 · Cited by 35 · see citing works
The neural circuits and molecular mechanisms underlying fear dysregulation in posttraumatic stress disorder
Iqbal, J., Huang, G.-D., Xue, Y.-X., Yang, M., & Jia, X. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1281401 · Cited by 49 · see citing works
Behavioral Neuroscience of Circuits Involved in Fear Processing
Bauer, E. P., & Paré, D. (2016) · Oxford University Press eBooks · doi:10.1093/med/9780190215422.003.0002

Authors: Johnson, L. R., McGuire, J., Lazarus, R., & Palmer, A. A.
Affiliations: Uniformed Services University of the Health Sciences (US)
University of Chicago (US)
Corresponding author: Johnson, Luke R.
ORCID: Johnson, Luke R.
McGuire, Jennifer
Palmer, Abraham A.
Venue: Neuropharmacology
Publisher: Elsevier BV
Published: 2012-02
Volume: 62
Issue: 2
Pages: 638-646
ISSN: 0028-3908 (ISSN-L)
DOI: 10.1016/j.neuropharm.2011.07.004
OpenAlex: W2055555487
Cited by: 140
References: 101
Citations by year: 2026: 3 · 2025: 7 · 2024: 7 · 2023: 11 · 2022: 12 · 2021: 8 · 2020: 6 · 2019: 11 · 2018: 12 · 2017: 7 · 2016: 17 · 2015: 10 · 2014: 8 · 2013: 14 · 2012: 6
FWCI: 4.54
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neuropharmacology (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health
National Institute of Mental Health (R01MH079103, MH079103)
National Institute of General Medical Sciences (R01GM097737)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Social Sciences › Psychology › Clinical Psychology › Posttraumatic Stress Disorder Research
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: fear conditioning, post-traumatic stress disorder, fear memory, neurobiology of fear
MeSH terms: Animals, Association Learning, Brain, Conditioning, Classical, Disease Models, Animal, Fear, Nerve Net, Phenotype, Stress Disorders, Post-Traumatic

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Pavlovian fear memory circuits and phenotype models of PTSD

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks