Neural circuits and mechanisms involved in Pavlovian fear conditioning: A critical review

Kim, Jeansok J.; Jung, Min Whan

doi:10.1016/j.neubiorev.2005.06.005

Cited by 636Memory and Neural MechanismsNeuroscience and Neuropharmacology ResearchMemory Processes and Influences

Neural circuits and mechanisms involved in Pavlovian fear conditioning: A critical review

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Kim, Jeansok J., Jung, Min Whan·2006·Neuroscience & Biobehavioral Reviews

DOI 10.1016/j.neubiorev.2005.06.005PMC PMC4342048

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Abstract

Pavlovian or classical fear conditioning is recognized as a model system to investigate the neurobiological mechanisms of learning and memory in the mammalian brain and to understand the root of fear-related disorders in humans. In recent decades, important progress has been made in delineating the essential neural circuitry and cellular-molecular mechanisms of fear conditioning. Converging lines of evidence indicate that the amygdala is necessarily involved in the acquisition, storage and expression of conditioned fear memory, and long-term potentiation (LTP) in the lateral nucleus of the amygdala is often proposed as the underlying synaptic mechanism of associative fear memory. Recent studies further implicate the prefrontal cortex-amygdala interaction in the extinction (or inhibition) of conditioned fear. Despite these advances, there are unresolved issues and findings that challenge the validity and sufficiency of the current amygdalar LTP hypothesis of fear conditioning. The purpose of this review is to critically evaluate the strengths and weaknesses of evidence indicating that fear conditioning depend crucially upon the amygdalar circuit and plasticity.

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Context-associated memory deficit is typical in AD patients and manifested as dysfunction of fear conditioning involving neural circuits of the amygdala, hippocampus, and prefrontal cortex.
“Context-associated memory: This deficit is typical in AD patients [128][129][130] and manifested as dysfunction of fear conditioning 82 involving neural circuits of the amygdala, hippocampus, and prefrontal cortex 131,132 .”
From NAD+ hydrolase Sarm1 is a key driver of synapse degeneration and memory loss in Alzheimer’s disease (2025) · cites this paper as [131]

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
Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning.
Phillips, R. G., & LeDoux, J. E. (1992) · Behavioral Neuroscience · doi:10.1037/0735-7044.106.2.274 · Cited by 3,292 · see citing works
Modality-Specific Retrograde Amnesia of Fear
Kim, J. J., & Fanselow, M. S. (1992) · Science · doi:10.1126/science.1585183 · Cited by 2,483 · see citing works
Self-citation
A differential neural response in the human amygdala to fearful and happy facial expressions
Morris, J. S., Frith, C. D., Perrett, D. I., Rowland, D., Young, A. W., Calder, A. J., & Dolan, R. J. (1996) · Nature · doi:10.1038/383812a0 · Cited by 2,013 · see citing works
Conditioned emotional reactions.
Watson, J. B., & Rayner, R. (1920) · Journal of Experimental Psychology · doi:10.1037/h0069608 · Cited by 2,005 · cited 3× · see citing works
“Perhaps the best-known example of fear conditioning is the Little Albert experiment by Watson and Rayner in 1920 (Watson and Rayner, 1920).”
Background
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 4× · see citing works
“Milad and Quirk (2002) have shown that neurons in rat infralimbic cortex signal extinction memory.”
BackgroundResultInfluential
Extinction Learning in Humans
Phelps, E. A., Delgado, M. R., Nearing, K. I., & LeDoux, J. E. (2004) · Neuron · doi:10.1016/j.neuron.2004.08.042 · Cited by 1,753 · see citing works
Fear conditioning induces associative long-term potentiation in the amygdala
Rogan, M. T., Stäubli, U. V., & LeDoux, J. E. (1997) · Nature · doi:10.1038/37601 · Cited by 1,310 · see citing works
The neuroanatomical and neurochemical basis of conditioned fear
Fendt, M., & Fanselow, M. S. (1999) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(99)00016-0 · Cited by 1,092 · 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 3× · see citing works
“…studies employ simple temporal pairings (or contiguity) of CS and US to produce fear conditioning, it is the informational relationship (or contingency) between the CS and US that is the essential determinant of classical conditioning (Kamin, 1968; Rescorla, 1968; Wagner et al., 1968).”
Background
The role of ventromedial prefrontal cortex in the recovery of extinguished fear
Quirk, G. J., Russo, G. K., Barron, J. L., & Lebron, K. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-16-06225.2000 · Cited by 957 · cited 3× · see citing works
“Quirk et al. (2000), using a different conditioning–extinction protocol (conditioning and extinction in 1”
MethodResult
Behavioral and Neural Analysis of Extinction
Myers, K. M., & Davis, M. (2002) · Neuron · doi:10.1016/s0896-6273(02)01064-4 · Cited by 918 · 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 5× · see citing works
“Because previous studies (Gewirtz et al., 1997; Morgan et al., 1993) employed extinction across multiple days, no extinction memory in lesioned animals on day 2 is not consistent with the report by Gewirtz et al.”
BackgroundResultInfluential
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 · cited 1× · see citing works
“It is generally accepted that sensory information enters the amygdala through its basal and lateral nuclei (BLA) (Aggleton, 2000; LeDoux, 1996; but see Pare et al., 2004 for an alternative view) where CS–”
Background
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
Hippocampus and trace conditioning of the rabbit's classically conditioned nictitating membrane response.
Solomon, P. R., Vander Schaaf, E. R., Thompson, R. F., & Weisz, D. J. (1986) · Behavioral Neuroscience · doi:10.1037/0735-7044.100.5.729 · Cited by 724 · see citing works
Conditioned fear as revealed by magnitude of startle response to an auditory stimulus.
Brown, J. S., Kalish, H. I., & Farber, I. E. (1951) · Journal of Experimental Psychology · doi:10.1037/h0060166 · Cited by 637 · see citing works
Synaptic plasticity in the lateral amygdala: a cellular hypothesis of fear conditioning
Blair, H. T., Schafe, G. E., Bauer, E. P., Rodrigues, S. M., & LeDoux, J. E. (2001) · Learning & Memory · doi:10.1101/lm.30901 · Cited by 610 · see citing works
Amygdala central nucleus lesions: Effect on heart rate conditioning in the rabbit
Kapp, B. S., Frysinger, R. C., Gallagher, M., & Haselton, J. R. (1979) · Physiology & Behavior · doi:10.1016/0031-9384(79)90304-4 · Cited by 590 · see citing works
Role of the amygdala in the coordination of behavioral, neuroendocrine, and prefrontal cortical monoamine responses to psychological stress in the rat
Goldstein, L. E., Rasmusson, A. M., Bunney, B. S., & Roth, R. H. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-15-04787.1996 · Cited by 387 · see citing works
Functional inactivation of the lateral and basal nuclei of the amygdala by muscimol infusion prevents fear conditioning to an explicit conditioned stimulus and to contextual stimuli.
Muller, J., Corodimas, K. P., Fridel, Z., & LeDoux, J. E. (1997) · Behavioral Neuroscience · doi:10.1037/0735-7044.111.4.683 · Cited by 382 · cited 2× · see citing works
“Similarly, reversible inactivation of neurons in BLA prior to fear conditioning, via infusing the γ-aminobutyric acid (GABAA) receptor agonist muscimol, blocks the acquisition of conditioned fear, while amygdalar muscimol infusions (prior to retention testing) in previously fear conditioned rats impair the expression…”
Background
Inverse amygdala and medial prefrontal cortex responses to surprised faces
Kim, H., Somerville, L. H., Johnstone, T., Alexander, A. L., & Whalen, P. J. (2003) · NeuroReport · doi:10.1097/00001756-200312190-00006 · Cited by 359 · see citing works
Human orbitofrontal cortex mediates extinction learning while accessing conditioned representations of value
Gottfried, J. A., & Dolan, R. J. (2004) · Nature Neuroscience · doi:10.1038/nn1314 · Cited by 353 · see citing works
Intra-Amygdala Blockade of the NR2B Subunit of the NMDA Receptor Disrupts the Acquisition But Not the Expression of Fear Conditioning
Rodrigues, S. M., Schafe, G. E., & LeDoux, J. E. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-17-06889.2001 · Cited by 350 · see citing works
NMDA-Receptor-Independent Long-Term Potentiation
Johnston, D., Williams, S., Jaffe, D., & Gray, R. (1992) · Annual Review of Physiology · doi:10.1146/annurev.ph.54.030192.002421 · Cited by 300 · cited 2× · see citing works
“…ambiguous and may depend on the particular synapses and input pathway (Chapman et al., 1990; LeDoux, 2000; Weisskopf and LeDoux, 1999), as demonstrated in the hippocampus (Grover and Teyler, 1990; Harris and Cotman, 1986; Johnston et al., 1992; Staubli and Lynch, 1990; Zalutsky and Nicoll, 1990).”
Background
Cardiovascular responses elicited by stimulation of neurons in the central amygdaloid nucleus in awake but not anesthetized rats resemble conditioned emotional responses
Iwata, J., Chida, K., & LeDoux, J. E. (1987) · Brain Research · doi:10.1016/0006-8993(87)90978-4 · Cited by 272 · see citing works
Selective Neurotoxic Lesions of Basolateral and Central Nuclei of the Amygdala Produce Differential Effects on Fear Conditioning
Koo, J. W., Han, J.-S., & Kim, J. J. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.1644-04.2004 · Cited by 179 · see citing works
Self-citation
Role of the Amygdala in Fear Extinction Measured with Potentiated Startle
DAVIS, M., WALKER, D. L., & MYERS, K. M. (2003) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2003.tb07084.x · Cited by 152 · cited 2× · see citing works
“Because injection of an NMDA receptor antagonist or a mitogen-activated protein kinase inhibitor into the amygdala blocks extinction of fear (Davis et al., 2003), it has been proposed that extinction memory goes through a consolidation process, initially from the amygdala afterward to the vmPFC…”
Background

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Neuronal circuits for fear and anxiety
Tovote, P., Fadok, J. P., & Lüthi, A. (2015) · Nature Reviews Neuroscience · doi:10.1038/nrn3945 · Cited by 1,786 · see citing works
Childhood adversity and neural development: Deprivation and threat as distinct dimensions of early experience
McLaughlin, K. A., Sheridan, M. A., & Lambert, H. K. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.10.012 · Cited by 1,389 · see citing works
Molecular mechanisms of fear learning and memory
Johansen, J. P., Cain, C. K., Ostroff, L. E., & LeDoux, J. E. (2011) · Cell · doi:10.1016/j.cell.2011.10.009 · Cited by 1,012 · see citing works
Plastic Synaptic Networks of the Amygdala for the Acquisition, Expression, and Extinction of Conditioned Fear
Pape, H.-C., & Pare, D. (2010) · Physiological Reviews · doi:10.1152/physrev.00037.2009 · Cited by 994 · see citing works
Don’t fear “fear conditioning”: Methodological considerations for the design and analysis of studies on human fear acquisition, extinction, and return of fear
Lonsdorf, T. B., Menz, M. M., Andreatta, M., Fullana, M. A., Golkar, A., Haaker, J., Heitland, I., Hermann, A., Kuhn, M., Kruse, O., et al. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.02.026 · Cited by 837 · see citing works
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
Diamond, D. M., Campbell, A. M., Park, C. R., Halonen, J., & Zoladz, P. R. (2007) · Neural Plasticity · doi:10.1155/2007/60803 · Cited by 762 · see citing works
“This topic has been reviewed extensively by others (LeDoux [333]; McIn-tyre et al. [334]; Fanselow and Gale [335]; McGaugh [88]; Dityatev and Bolshakov [336]; Maren [337]; Kim and Jung [21]; Sigurdsson et al. [338]) and will not be discussed at length here.”
BackgroundInfluential
Neural signatures of human fear conditioning: an updated and extended meta-analysis of fMRI studies
Fullana, M. A., Harrison, B. J., Soriano-Mas, C., Vervliet, B., Cardoner, N., Àvila-Parcet, A., & Radua, J. (2016) · Molecular Psychiatry · doi:10.1038/mp.2015.88 · Cited by 702 · see citing works
Dimensions of early experience and neural development: deprivation and threat
Sheridan, M. A., & McLaughlin, K. A. (2014) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2014.09.001 · Cited by 697 · see citing works
Emotion regulation and the anxiety disorders: An integrative review
Cisler, J. M., Olatunji, B. O., Feldner, M. T., & Forsyth, J. P. (2010) · Journal of Psychopathology and Behavioral Assessment · doi:10.1007/s10862-009-9161-1 · Cited by 607 · see citing works
Human Fear Conditioning and Extinction in Neuroimaging: A Systematic Review
Sehlmeyer, C., Schöning, S., Zwitserlood, P., Pfleiderer, B., Kircher, T., Arolt, V., & Konrad, C. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005865 · Cited by 543 · see citing works
Context-Dependent Human Extinction Memory Is Mediated by a Ventromedial Prefrontal and Hippocampal Network
Kalisch, R., Korenfeld, E., Stephan, K. E., Weiskopf, N., Seymour, B., & Dolan, R. J. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.2021-06.2006 · Cited by 493 · see citing works
Fear memory
Izquierdo, I., Furini, C. R. G., & Myskiw, J. C. (2016) · Physiological Reviews · doi:10.1152/physrev.00018.2015 · Cited by 453 · see citing works
Sleep-specific mechanisms underlying posttraumatic stress disorder: integrative review and neurobiological hypotheses
Germain, A., Buysse, D. J., & Nofzinger, E. (2008) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2007.09.003 · Cited by 421 · see citing works
Nightmares: A new neurocognitive model
Nielsen, T., & Levin, R. (2007) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2007.03.004 · Cited by 378 · see citing works
Hippocampal involvement in contextual modulation of fear extinction
Ji, J., & Maren, S. (2007) · Hippocampus · doi:10.1002/hipo.20331 · Cited by 297 · see citing works
Differential associations of threat and deprivation with emotion regulation and cognitive control in adolescence
Lambert, H. K., King, K. M., Monahan, K. C., & McLaughlin, K. A. (2017) · Development and Psychopathology · doi:10.1017/s0954579416000584 · Cited by 267 · see citing works
Enhancement of extinction memory consolidation: the role of the noradrenergic and GABAergic systems within the basolateral amygdala
BERLAU, D., & MCGAUGH, J. (2006) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2005.12.008 · Cited by 220 · see citing works
The translational neural circuitry of anxiety
Robinson, O. J., Pike, A. C., Cornwell, B., & Grillon, C. (2019) · Journal of Neurology, Neurosurgery & Psychiatry · doi:10.1136/jnnp-2019-321400 · Cited by 158 · see citing works
Controllable versus uncontrollable stressors bi-directionally modulate conditioned but not innate fear
Baratta, M. V., Christianson, J. P., Gomez, D. M., Zarza, C. M., Amat, J., Masini, C. V., Watkins, L. R., & Maier, S. F. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.03.042 · Cited by 156 · see citing works
Trauma associated sleep disorder: a parasomnia induced by trauma
Mysliwiec, V., Brock, M. S., Creamer, J. L., O'Reilly, B. M., Germain, A., & Roth, B. J. (2018) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2017.01.004 · Cited by 150 · see citing works
Cognitive and neural correlates of depression-like behaviour in socially defeated mice: an animal model of depression with cognitive dysfunction
Yu, T., Guo, M., Garza, J., Rendon, S., Sun, X.-L., Zhang, W., & Lu, X.-Y. (2011) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145710000945 · Cited by 137 · see citing works
Mouse chronic social stress increases blood and brain kynurenine pathway activity and fear behaviour: Both effects are reversed by inhibition of indoleamine 2,3-dioxygenase
Fuertig, R., Azzinnari, D., Bergamini, G., Cathomas, F., Sigrist, H., Seifritz, E., Vavassori, S., Luippold, A., Hengerer, B., Ceci, A., et al. (2016) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2015.12.020 · Cited by 135 · see citing works
Resilience: A psychobiological construct for psychiatric disorders
Shrivastava, A., & Desousa, A. (2016) · Indian Journal of Psychiatry · doi:10.4103/0019-5545.174365 · Cited by 127 · see citing works
Bridging the interval: Theory and neurobiology of trace conditioning
Raybuck, J. D., & Lattal, K. M. (2014) · Behavioural Processes · doi:10.1016/j.beproc.2013.08.016 · Cited by 114 · see citing works
Safety Signals Mitigate the Consequences of Uncontrollable Stress Via a Circuit Involving the Sensory Insular Cortex and Bed Nucleus of the Stria Terminalis
Christianson, J. P., Jennings, J. H., Ragole, T., Flyer, J. G. N., Benison, A. M., Barth, D. S., Watkins, L. R., & Maier, S. F. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.04.004 · Cited by 104 · see citing works
The Sensory Insular Cortex Mediates the Stress-Buffering Effects of Safety Signals But Not Behavioral Control
Christianson, J. P., Benison, A. M., Jennings, J., Sandsmark, E. K., Amat, J., Kaufman, R. D., Baratta, M. V., Paul, E. D., Campeau, S., Watkins, L. R., et al. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.4270-08.2008 · Cited by 97 · see citing works
Effect of cannabidiol on sleep disruption induced by the repeated combination tests consisting of open field and elevated plus-maze in rats
Hsiao, Y.-T., Yi, P.-L., Li, C.-L., & Chang, F.-C. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.08.013 · Cited by 91 · see citing works
Neurobiology of hedonic tone: the relationship between treatment-resistant depression, attention-deficit hyperactivity disorder, and substance abuse
Katzman, M., & Sternat, T. (2016) · Neuropsychiatric Disease and Treatment · doi:10.2147/ndt.s111818 · Cited by 83 · see citing works
Neural substrates of individual differences in human fear learning: Evidence from concurrent fMRI, fear-potentiated startle, and US-expectancy data
van Well, S., Visser, R. M., Scholte, H. S., & Kindt, M. (2012) · Cognitive, Affective, & Behavioral Neuroscience · doi:10.3758/s13415-012-0089-7 · Cited by 75 · see citing works
Long-term changes in fear conditioning and anxiety-like behavior following nicotine exposure in adult versus adolescent rats
SMITH, L., MCDONALD, C., BERGSTROM, H., BRIELMAIER, J., EPPOLITO, A., WHEELER, T., FALCO, A., & SMITH, R. (2006) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2006.07.014 · Cited by 70 · see citing works
Linking Social Cognition to Learning and Memory
Leblanc, H., & Ramirez, S. (2020) · The Journal of Neuroscience · doi:10.1523/jneurosci.1280-20.2020 · Cited by 69 · see citing works
Functional Imaging of Stimulus Convergence in Amygdalar Neurons during Pavlovian Fear Conditioning
Barot, S. K., Chung, A., Kim, J. J., & Bernstein, I. L. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006156 · Cited by 66 · see citing works
Self-citation
Impaired long-term potentiation and enhanced neuronal excitability in the amygdala of CaV1.3 knockout mice
McKinney, B. C., Sze, W., Lee, B., & Murphy, G. G. (2009) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2009.06.012 · Cited by 63 · see citing works
5-hydroxytryptamine 2C receptors in the dorsal striatum mediate stress-induced interference with negatively reinforced instrumental escape behavior
Strong, P. V., Christianson, J. P., Loughridge, A. B., Amat, J., Maier, S. F., Fleshner, M., & Greenwood, B. N. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.09.041 · Cited by 61 · see citing works
Age-dependent Effects of Tobacco Smoke and Nicotine on Cognition and the Brain: A Systematic Review of the Human and Animal Literature Comparing Adolescents and Adults.
Colyer-Patel, K., Kuhns, L., Weidema, A., Lesscher, H., & Cousijn, J. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105038 · Cited by 54 · see citing works
“Whilst the amygdala is implicated in both forms of fear conditioning (Kim and Jung, 2006), cued fear conditioning involves links from thalamic and cortical inputs to the lateral amygdala (Sachella et al., 2021), whilst context fear conditioning involves circuits within the hippocampus which send…”
Aversive Learning in Adolescents: Modulation by Amygdala–Prefrontal and Amygdala–Hippocampal Connectivity and Neuroticism
IMAGEN consortium, Tzschoppe, J., Nees, F., Banaschewski, T., Barker, G. J., Büchel, C., Conrod, P. J., Garavan, H., Heinz, A., Loth, E., et al. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2013.287 · Cited by 49 · see citing works
Intra-amygdala microinfusion of IL-6 impairs the auditory fear conditioning of rats via JAK/STAT activation
Hao, Y., Jing, H., Bi, Q., Zhang, J., Qin, L., & Yang, P. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.08.052 · Cited by 38 · see citing works
Micro-Positron Emission Tomography Imaging of Rat Brain Metabolism during Expression of Contextual Conditioning
Luyten, L., Casteels, C., Vansteenwegen, D., van Kuyck, K., Koole, M., Van Laere, K., & Nuttin, B. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.3701-11.2012 · Cited by 39 · see citing works
Memory corticalization triggered by REM sleep: mechanisms of cellular and systems consolidation
Almeida-Filho, D. G., Queiroz, C. M., & Ribeiro, S. (2018) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-018-2886-9 · Cited by 38 · see citing works
Conditioned associations and economic decision biases.
Guitart-Masip, M., Talmi, D., & Dolan, R. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.06.021 · Cited by 36 · see citing works
Neurological sequelae induced by alphavirus infection of the CNS are attenuated by treatment with the glutamine antagonist 6-diazo-5-oxo-l-norleucine
Potter, M. C., Baxter, V. K., Mathey, R. W., Alt, J., Rojas, C., Griffin, D. E., & Slusher, B. S. (2015) · Journal of NeuroVirology · doi:10.1007/s13365-015-0314-6 · Cited by 32 · see citing works
Postweaning, forebrain-specific perturbation of the oxytocin system impairs fear conditioning
Pagani, J. H., Lee, H.-J., & Young, W. S. (2011) · Genes, Brain and Behavior · doi:10.1111/j.1601-183x.2011.00709.x · Cited by 30 · see citing works
Exposure in vivo as a treatment approach to target pain-related fear: theory and new insights from research and clinical practice
den Hollander, M., Smeets, R. J. E. M., van Meulenbroek, T., van Laake-Geelen, C. C. M., Baadjou, V. A., & Timmers, I. (2022) · Physical Therapy · doi:10.1093/ptj/pzab270 · Cited by 30 · see citing works
Intra-amygdala microinjection of TNF-α impairs the auditory fear conditioning of rats via glutamate toxicity
Jing, H., Hao, Y., Bi, Q., Zhang, J., & Yang, P. (2015) · Neuroscience Research · doi:10.1016/j.neures.2014.10.015 · Cited by 28 · see citing works
Classical conditioning in borderline personality disorder: an fMRI study
Krause-Utz, A., Keibel-Mauchnik, J., Ebner-Priemer, U., Bohus, M., & Schmahl, C. (2016) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-015-0593-1 · Cited by 24 · see citing works
Excess Neonatal Testosterone Causes Male-Specific Social and Fear Memory Deficits in Wild-Type Mice
Quiñones-Labernik, P., Blocklinger, K. L., Bruce, M. R., Hagan, E., Preuschl, D., Tesar, C., & Ferri, S. L. (2025) · eneuro · doi:10.1523/eneuro.0020-25.2025 · Cited by 4 · see citing works
NAD+ hydrolase Sarm1 is a key driver of synapse degeneration and memory loss in Alzheimer’s disease
Fan, F., Joshi, P., Liu, X., Kotturu, S. K., Abiola, M., Liu, Q., & Lou, X. (2025) · doi:10.64898/2025.12.21.695860

Authors: Kim, J. J., & Jung, M. W.
Affiliations: University of Washington (US)
Ajou University (KR)
Corresponding author: Kim, Jeansok J.
ORCID: Kim, Jeansok J.
Jung, Min Whan
Venue: Neuroscience & Biobehavioral Reviews
Publisher: Elsevier BV
Published: 2006-01
Volume: 30
Issue: 2
Pages: 188-202
ISSN: 0149-7634 (ISSN-L)
DOI: 10.1016/j.neubiorev.2005.06.005
PMC: PMC4342048
OpenAlex: W2155158396
Cited by: 636
References: 28
Citations by year: 2026: 14 · 2025: 22 · 2024: 33 · 2023: 34 · 2022: 16 · 2021: 29 · 2020: 27 · 2019: 40 · 2018: 36 · 2017: 31 · 2016: 32 · 2015: 38 · 2014: 46 · 2013: 39 · 2012: 39
FWCI: 1.98
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neuroscience & Biobehavioral Reviews (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
AJOU Open Repository (Ajou University) (submittedVersion)
Funders: National Institute of Mental Health (R01 MH64457, R01MH064457)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
Keywords: fear conditioning, amygdala, long-term potentiation, lateral amygdala, fear extinction, conditioned fear memory, synaptic plasticity, neural circuits, fear-related disorders
MeSH terms: Amygdala, Animals, Association Learning, Avoidance Learning, Brain, Conditioning, Classical, Extinction, Psychological, Fear, Memory, Neural Pathways, Prefrontal Cortex

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Neural circuits and mechanisms involved in Pavlovian fear conditioning: A critical review

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