Neuronal signalling of fear memory

Maren, Stephen; Quirk, Gregory J.

doi:10.1038/nrn1535

Cited by 1,428Memory and Neural MechanismsNeuroscience and Neuropharmacology ResearchMemory Processes and Influences

Neuronal signalling of fear memory

Open access

Maren, Stephen, Quirk, Gregory J.·2004·Nature Reviews Neuroscience

DOI 10.1038/nrn1535

Open this paper in CoChat — free account Open PDF

Abstract

The learning and remembering of fearful events depends on the integrity of the amygdala, but how are fear memories represented in the activity of amygdala neurons? Here, we review recent electrophysiological studies indicating that neurons in the lateral amygdala encode aversive memories during the acquisition and extinction of Pavlovian fear conditioning. Studies that combine unit recording with brain lesions and pharmacological inactivation provide evidence that the lateral amygdala is a crucial locus of fear memory. Extinction of fear memory reduces associative plasticity in the lateral amygdala and involves the hippocampus and prefrontal cortex. Understanding the signalling of aversive memory by amygdala neurons opens new avenues for research into the neural systems that support fear behaviour.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1038/nrn1535

Cites

112 of 112 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

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?

The amygdala has been implicated as a key neural region in emotional dysregulation in psychiatric disorders.
“The amygdala has been implicated as a key neural region in emotional dysregulation in psychiatric disorders.”
From The Adolescent Brain (2008) · cites this paper as Maren & Quirk 2004
The ‘Fear-related plasticity in the lateral amygdala’ section describes the amygdala as necessary for acquiring and expressing Pavlovian fear memories. ‘Fear not: amygdala inhibition after extinction’ links amygdala-dependent fear extinction to treatments for anxiety disorders, including panic disorder and post-traumatic stress. The paper does not establish the broader claim that the amygdala is a key region in emotional dysregulation across psychiatric disorders. Page numbers were unavailable in our copy. (LLM, conf=0.83)
Experimental — accuracy not yet measured
The amygdala is essential to learning the emotional significance of cues in the environment.
“This region is essential to learning the emotional significance of cues in the environment (see Maren & Quirk 2004 for review).”
From The Adolescent Brain (2008) · cites this paper as Maren & Quirk 2004
The section “Fear-related plasticity in the lateral amygdala” says the amygdala is necessary for acquiring Pavlovian fear memories. The claim extends that finding to learning the emotional significance of environmental cues generally, whereas the review focuses on fear conditioning and explicitly notes that the amygdala is not necessary for all forms of aversive memory. The indexed copy provides no page number for this section. (LLM, conf=0.86)
Experimental — accuracy not yet measured
The basolateral amygdala (BLA) is critical for both reconsolidation and extinction of pavlovian memories.
“for pavlovian memories the basolateral amygdala (BLA) is critical for both (Maren and Quirk, 2004; Nader, 2015).”
From Retrieval-Dependent Mechanisms Affecting Emotional Memory Persistence: Reconsolidation, Extinction, and the Space in Between (2020) · cites this paper as Maren and Quirk, 2004
The section “Fear not: amygdala inhibition after extinction” says the amygdala has a vital role in extinction of learned fear and that disrupting its activity or plasticity impairs extinction. The paper addresses Pavlovian fear conditioning, not Pavlovian memories generally; a search for reconsolidation and memory reactivation found no passage supporting the reconsolidation part of the claim. Page numbers were not available in our copy. (LLM, conf=0.87)
Experimental — accuracy not yet measured
The expression and inhibition of learned fear is largely regulated by the amygdala, hippocampus, and PFC in adult rodents and humans.
“The expression and inhibition of learned fear is largely regulated by the amygdala, hippocampus, and PFC in adult rodents and humans (Knapska et al., 2012;LeDoux, 2003;Maren and Quirk, 2004;Tovote et al., 2015)”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Maren and Quirk, 2004
The review describes roles for the amygdala, medial prefrontal cortex, and hippocampus in learned-fear expression and extinction, including rat evidence in the Reviews section and their interaction in the Conclusions (page numbers unavailable). It discusses clinical relevance but does not establish that these three regions regulate learned fear in adult humans; that extension is unsupported by this copy. (LLM, conf=0.85)
Experimental — accuracy not yet measured
Association between a shock-predicting stimulus and shock forms in basolateral amygdala.
“Briefly, the association between a stimulus predicting shock and the shock forms in basolateral regions of the amygdala.”
From Learned helplessness at fifty: Insights from neuroscience. (2016) · cites this paper as Maren & Quirk, 2004

Information passes from basolateral amygdala to central nucleus, which projects to regions controlling fear behaviors and physiological responses.
“From there the information passes to the central nucleus of the amygdala, which in turns projects to the regions that control the behaviors and physiological responses that are the symptoms of fear (Davis, Rainnie, & Cassell, 1994; LeDoux, 2003; Maren & Quirk, 2004).”
From Learned helplessness at fifty: Insights from neuroscience. (2016) · cites this paper as Maren & Quirk, 2004
The frontal cortex is an important component of brain circuitry involved in the extinction of conditioned responses, behavioral inhibition, coping with controllable stressors, and interacting with the temporal lobe to facilitate memory formation and retrieval.
“In addition, the frontal cortex, in general, is an important component of brain circuitry involved in the extinction of conditioned responses (Maren and Quirk [378]; Likhtik et al. [379]; Milad et al. [380]; Milad et al. [381]), behavioral inhibition (Tillfors [382]; Levy [383]), and coping with controllable stressors (Ter Horst [384]; Gerrits et al. [385]; Rangel et al. [386]; Bland et al. [387];”
From 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) · cites this paper as Maren and Quirk [378]
Many processes involving alteration of synaptic plasticity have been shown to be influenced by gut microbes.
“Examples of processes that involve alteration of synaptic plasticity include synaptic remodeling (Ziv and Brenner, 2018), synaptogenesis (Bednarek and Caroni, 2011), axonal sprouting/ pruning and dendritic remodeling (Selemon, 2013), as well as (neurogenesis) and recruitment (Ganguly and Poo, 2013) many of which have been shown to be influenced by gut microbes (984).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as [984]
The review’s “R E V I E W S” section discusses forms of experience-dependent plasticity, and Box 2 discusses synaptic plasticity in fear memory. Neither addresses whether gut microbes influence these processes. Searches for gut microbes and microbiota in our copy found no passage on that link; page numbers were unavailable. (LLM, conf=0.76)
Experimental — accuracy not yet measured
Processing of sensory information in the BLA results in the formation of associations between neutral predictive stimuli and outcomes of positive or negative valence via Hebbian mechanisms.
“Processing of this sensory information in the BLA results in the formation of associations between neutral predictive stimuli and outcomes of positive or negative valence56 via Hebbian mechanisms57-59.”
From Resolving the neural circuits of anxiety (2015) · cites this paper as [57]
The lateral nucleus of the amygdala (LA) is a site of associative plasticity, where US-evoked depolarization of LA pyramidal neurons is thought to instruct plasticity at synapses formed by CS inputs onto the same neurons.
“The lateral nucleus of the amygdala (LA) is a site of associative plasticity, where US-evoked depolarization of LA pyramidal neurons is thought to instruct plasticity at synapses formed by CS inputs onto the same neurons (5–7).”
From Optical activation of lateral amygdala pyramidal cells instructs associative fear learning (2010) · cites this paper as [7]
A large number of studies have provided convincing evidence that associative plasticity in the LA contributes to fear memory formation.
“A large number of studies have provided convincing evidence that associative plasticity in the LA contributes to fear memory formation (4, 6, 7).”
From Optical activation of lateral amygdala pyramidal cells instructs associative fear learning (2010) · cites this paper as [7]
Extinction results from procedures aimed at decreasing the threat value of the CS, while adaptation refers to reduced threat elicited by the US.
“Extinction results from procedures aimed at decreasing the threat value of the CS23–25 while adaptation refers to reduced threat elicited by the US26,27.”
From Dopamine dynamics as a regulatory mechanism for shifting between defensive and reward-seeking behaviors (2026) · cites this paper as [23]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

The Organization of Behavior
Hebb, D. O. (2005) · doi:10.4324/9781410612403 · Cited by 9,825 · see citing works
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
The organization of behavior.
indicated, N. A. (1950) · Journal of Consulting Psychology · doi:10.1037/h0049612 · Cited by 6,984 · see citing works
THE AMYGDALA MODULATES THE CONSOLIDATION OF MEMORIES OF EMOTIONALLY AROUSING EXPERIENCES
McGaugh, J. L. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.27.070203.144157 · Cited by 2,296 · see citing works
Large-scale recording of neuronal ensembles
Buzsáki, G. (2004) · Nature Neuroscience · doi:10.1038/nn1233 · Cited by 1,875 · 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
“This is precisely the time when mPFC neurons show robust increases in CS-elicited firin”
BackgroundSelf-citation
Neurobiology of Pavlovian Fear Conditioning
Maren, S. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.897 · Cited by 1,805 · see citing works
Self-citation
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 lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning
LeDoux, J., Cicchetti, P., Xagoraris, A., & Romanski, L. (1990) · The Journal of Neuroscience · doi:10.1523/jneurosci.10-04-01062.1990 · Cited by 1,167 · see citing works
A modern learning theory perspective on the etiology of panic disorder.
Bouton, M. E., Mineka, S., & Barlow, D. H. (2001) · Psychological Review · doi:10.1037/0033-295x.108.1.4 · Cited by 1,017 · see citing works
Organization of intra-amygdaloid circuitries in the rat: an emerging framework for understanding functions of the amygdala
Pitkänen, A., Savander, V., & LeDoux, J. E. (1997) · Trends in Neurosciences · doi:10.1016/s0166-2236(97)01125-9 · Cited by 980 · see citing works
Reciprocal Connections between the Amygdala and the Hippocampal Formation, Perirhinal Cortex, and Postrhinal Cortex in Rat: A Review
Pitkänen, A., Pikkarainen, M., Nurminen, N., & Ylinen, A. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb06738.x · Cited by 962 · see citing works
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 1× · see citing works
“Rats with mPFC lesions can learn to extinguish fear CRs, but have difficulty recalling the extinction memory 24 hours after trainin”
BackgroundSelf-citation
Stimulation of medial prefrontal cortex decreases the responsiveness of central amygdala output neurons
Quirk, G. J., Likhtik, E., Pelletier, J. G., & Paré, D. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-25-08800.2003 · Cited by 927 · see citing works
Self-citation
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
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
“Rats with mPFC lesions can learn to extinguish fear CRs, but have difficulty recalling the extinction memory 24 hours after trainin”
Background
Amygdaloid projections to the mesencephalon, pons and medulla oblongata in the cat
Hopkins, D. A., & Holstege, G. (1978) · Experimental Brain Research · doi:10.1007/bf00239551 · Cited by 866 · 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
Self-citation
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
Amygdalar and Hippocampal Theta Rhythm Synchronization During Fear Memory Retrieval
Seidenbecher, T., Laxmi, T. R., Stork, O., & Pape, H.-C. (2003) · Science · doi:10.1126/science.1085818 · Cited by 728 · see citing works
A description of the amygdaloid complex in the rat and cat with observations on intra‐amygdaloid axonal connections
Krettek, J. E., & Price, J. L. (1978) · Journal of Comparative Neurology · doi:10.1002/cne.901780205 · Cited by 727 · see citing works
Different types of fear-conditioned behaviour mediated by separate nuclei within amygdala
Killcross, S., Robbins, T., & Everitt, B. (1997) · Nature · doi:10.1038/41097 · Cited by 697 · see citing works
Extinction of fear-potentiated startle: blockade by infusion of an NMDA antagonist into the amygdala
Falls, W., Miserendino, M., & Davis, M. (1992) · The Journal of Neuroscience · doi:10.1523/jneurosci.12-03-00854.1992 · Cited by 673 · 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
Neural Substrates of Eyeblink Conditioning: Acquisition and RetentionPreprint
Christian, K. M., & Thompson, R. F. (2003) · Learning & Memory · doi:10.1101/lm.59603 · Cited by 609 · see citing works
Specific long-term memory traces in primary auditory cortex
Weinberger, N. M. (2004) · Nature reviews. Neuroscience · doi:10.1038/nrn1366 · Cited by 600 · 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
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
Self-citation
Topographic organization of neurons in the acoustic thalamus that project to the amygdala
LeDoux, J., Farb, C. R., & Ruggiero, D. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-04-01043.1990 · Cited by 546 · see citing works
Subcortical efferent projections of the medial geniculate nucleus mediate emotional responses conditioned to acoustic stimuli
LeDoux, J., Sakaguchi, A., & Reis, D. (1984) · The Journal of Neuroscience · doi:10.1523/jneurosci.04-03-00683.1984 · Cited by 532 · see citing works
Projections to the subcortical forebrain from anatomically defined regions of the medial geniculate body in the rat
LeDoux, J. E., Ruggiero, D. A., & Reis, D. J. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902420204 · Cited by 530 · see citing works
Memory consolidation of Pavlovian fear conditioning: a cellular and molecular perspective
Schafe, G. E., Nader, K., Blair, H. T., & LeDoux, J. E. (2001) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01969-x · Cited by 510 · see citing works
Synaptic plasticity in the basolateral amygdala induced by hippocampal formation stimulation in vivo
Maren, S., & Fanselow (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-11-07548.1995 · Cited by 499 · see citing works
Self-citation
Equipotentiality of thalamo-amygdala and thalamo-cortico-amygdala circuits in auditory fear conditioning
Romanski, L. M., & LeDoux, J. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-11-04501.1992 · Cited by 461 · see citing works
Long-term potentiation in the amygdala: a mechanism for emotional learning and memory
Maren, S. (1999) · Trends in Neurosciences · doi:10.1016/s0166-2236(99)01465-4 · Cited by 456 · see citing works
Self-citation
Hippocampal Inactivation Disrupts Contextual Retrieval of Fear Memory after Extinction
Corcoran, K. A., & Maren, S. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-05-01720.2001 · Cited by 455 · cited 1× · see citing works
“A recent study indicates that the hippocampus modulates the expression of extinction memorie”
BackgroundSelf-citation
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
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
Learning centers of rat brain mapped by measuring latencies of conditioned unit responses.
Olds, J., Disterhoft, J. F., Segal, M., Kornblith, C. L., & Hirsh, R. (1972) · Journal of Neurophysiology · doi:10.1152/jn.1972.35.2.202 · Cited by 427 · see citing works
Information Cascade from Primary Auditory Cortex to the Amygdala: Corticocortical and Corticoamygdaloid Projections of Temporal Cortex in the Rat
Romanski, L. M., & LeDoux, J. E. (1993) · Cerebral Cortex · doi:10.1093/cercor/3.6.515 · Cited by 398 · see citing works
The role of the amygdala in conditioned and unconditioned fear and anxiety
Davis, M. (2000) · The Amygdala · doi:10.1093/oso/9780198505013.003.0006 · Cited by 384 · 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 · 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 1× · see citing works
“However, this seems unlikely, because inactivation of the BASOLATERAL AMYGDALA (BLA) with the GABA A (γ-aminobutyric acid, type A) receptor agonist muscimol prevents the acquisition of fear conditioning, as well as the expression of fear memory, 24 hours after training when rats are tested drug-fre”
Background
N-methyl-D-aspartate receptors in the basolateral amygdala are required for both acquisition and expression of conditional fear in rats.
Maren, S., Aharonov, G., Stote, D. L., & Fanselow, M. S. (1996) · Behavioral Neuroscience · doi:10.1037//0735-7044.110.6.1365 · Cited by 372 · see citing works
Self-citation
Memory for extinction of conditioned fear is long-lasting and persists following spontaneous recovery
Quirk, G. J. (2002) · Learning & Memory · doi:10.1101/lm.49602 · Cited by 360 · cited 1× · see citing works
“This means that extinction is expressed only in the context in which extinction was given, and even in that context, fear responses will spontaneously recover over tim”
BackgroundSelf-citation
Electrical Stimulation of Medial Prefrontal Cortex Reduces Conditioned Fear in a Temporally Specific Manner.
Milad, M. R., Vidal-Gonzalez, I., & Quirk, G. J. (2004) · Behavioral Neuroscience · doi:10.1037/0735-7044.118.2.389 · Cited by 354 · see citing works
Self-citation
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
An Inhibitory Interface Gates Impulse Traffic between the Input and Output Stations of the Amygdala
Royer, S., Martina, M., & Paré, D. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-23-10575.1999 · Cited by 350 · 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
The Prefrontal Cortex Regulates Lateral Amygdala Neuronal Plasticity and Responses to Previously Conditioned Stimuli
Rosenkranz, J. A., Moore, H., & Grace, A. A. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-35-11054.2003 · Cited by 344 · see citing works
The Basolateral Amygdala Interacts with the Medial Prefrontal Cortex in Regulating Glucocorticoid Effects on Working Memory Impairment
Roozendaal, B., McReynolds, J. R., & McGaugh, J. L. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.4664-03.2004 · Cited by 327 · see citing works
N-methyl-D-aspartate receptors in the basolateral amygdala are required for both acquisition and expression of conditional fear in rats.
Maren, S., Aharonov, G., Stote, D. L., & Fanselow, M. S. (1996) · Behavioral Neuroscience · doi:10.1037/0735-7044.110.6.1365 · Cited by 325 · see citing works
Self-citation
Prefrontal Cortex Long-Term Potentiation, But Not Long-Term Depression, Is Associated with the Maintenance of Extinction of Learned Fear in Mice
Herry, C., & Garcia, R. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-02-00577.2002 · Cited by 323 · see citing works
Fear Conditioning Occludes LTP-Induced Presynaptic Enhancement of Synaptic Transmission in the Cortical Pathway to the Lateral Amygdala
Tsvetkov, E., Carlezon, W. A., Benes, F. M., Kandel, E. R., & Bolshakov, V. Y. (2002) · Neuron · doi:10.1016/s0896-6273(02)00645-1 · Cited by 321 · see citing works
Synaptic plasticity in fear conditioning circuits: induction of LTP in the lateral nucleus of the amygdala by stimulation of the medial geniculate body
Clugnet, M.-C., & LeDoux, J. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-08-02818.1990 · Cited by 316 · see citing works
Exposure therapy for posttraumatic stress disorder
Rothbaum, B. O., & Schwartz, A. C. (2002) · American Journal of Psychotherapy · doi:10.1176/appi.psychotherapy.2002.56.1.59 · Cited by 313 · see citing works
Response properties of single units in areas of rat auditory thalamus that project to the amygdala
Bordi, F., & LeDoux, J. E. (1994) · Experimental Brain Research · doi:10.1007/bf00228415 · Cited by 291 · see citing works
Intrinsic neurons in the amygdaloid field projected to by the medial geniculate body mediate emotional responses conditioned to acoustic stimuli
Iwata, J., LeDoux, J. E., Meeley, M. P., Arnerić, S. P., & Reis, D. J. (1986) · Brain Research · doi:10.1016/0006-8993(86)90020-x · Cited by 279 · see citing works
Effects of muscimol applied to the basolateral amygdala on acquisition and expression of contextual fear conditioning in rats.
Helmstetter, F. J., & Bellgowan, P. S. F. (1994) · Behavioral Neuroscience · doi:10.1037//0735-7044.108.5.1005 · Cited by 265 · see citing works
Parallels between cerebellum- and amygdala-dependent conditioning
Medina, J. F., Repa, J. C., Mauk, M. D., & LeDoux, J. E. (2002) · Nature reviews. Neuroscience · doi:10.1038/nrn728 · Cited by 265 · see citing works
Neuronal Correlates of Fear in the Lateral Amygdala: Multiple Extracellular Recordings in Conscious Cats
Paré, D., & Collins, D. R. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-07-02701.2000 · Cited by 262 · see citing works
Overlapping projections to the amygdala and striatum from auditory processing areas of the thalamus and cortex
LeDoux, J. E., Farb, C. R., & Romanski, L. M. (1991) · Neuroscience Letters · doi:10.1016/0304-3940(91)90526-y · Cited by 261 · see citing works
Hormonal Influences on Memory
McGaugh, J. L. (1983) · Annual Review of Psychology · doi:10.1146/annurev.ps.34.020183.001501 · Cited by 259 · see citing works
Long‐Term synaptic potentiation in the amygdala
Chapman, P. F., Kairiss, E. W., Keenan, C. L., & Brown, T. H. (1990) · Synapse · doi:10.1002/syn.890060306 · Cited by 234 · see citing works
Electrophysiological characteristics of amygdaloid central nucleus neurons during Pavlovian fear conditioning in the rabbit
Pascoe, J. P., & Kapp, B. S. (1985) · Behavioural Brain Research · doi:10.1016/0166-4328(85)90087-7 · Cited by 233 · see citing works
Mitogen-Activated Protein Kinase Cascade in the Basolateral Nucleus of Amygdala Is Involved in Extinction of Fear-Potentiated Startle
Lu, K., Walker, D. L., & Davis, M. E. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-16-j0005.2001 · Cited by 222 · see citing works
Effects of muscimol applied to the basolateral amygdala on acquisition and expression of contextual fear conditioning in rats.
Helmstetter, F. J., & Bellgowan, P. S. F. (1994) · Behavioral Neuroscience · doi:10.1037/0735-7044.108.5.1005 · Cited by 219 · see citing works
Functional Inactivation of the Amygdala before But Not after Auditory Fear Conditioning Prevents Memory Formation
Wilensky, A. E., Schafe, G. E., & LeDoux, J. E. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-24-j0006.1999 · Cited by 217 · see citing works
Associative retuning in the thalamic source of input to the amygdala and auditory cortex: Receptive field plasticity in the medial division of the medial geniculate body.
Edeline, J., & Weinberger, N. M. (1992) · Behavioral Neuroscience · doi:10.1037//0735-7044.106.1.81 · Cited by 214 · see citing works
Delayed Recall of Fear Extinction in Rats With Lesions of Ventral Medial Prefrontal CortexPreprint
Lebrón‐Milad, K., Milad, M. R., & Quirk, G. J. (2004) · Learning & Memory · doi:10.1101/lm.78604 · Cited by 208 · see citing works
Self-citation
Interruption of projections from the medial geniculate body to an archi-neostriatal field disrupts the classical conditioning of emotional responses to acoustic stimuli
LeDoux, J. E., Sakaguchi, A., Iwata, J., & Reis, D. J. (1986) · Neuroscience · doi:10.1016/0306-4522(86)90034-5 · Cited by 207 · see citing works
Context-Dependent Neuronal Activity in the Lateral Amygdala Represents Fear Memories after Extinction
Hobin, J. A., Goosens, K. A., & Maren, S. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-23-08410.2003 · Cited by 187 · see citing works
Self-citation
The Amygdala Is Essential for the Development of Neuronal Plasticity in the Medial Geniculate Nucleus during Auditory Fear Conditioning in Rats
Maren, S., Yap, S. A., & Goosens, K. A. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-06-j0001.2001 · Cited by 186 · see citing works
Self-citation
Basolateral amygdala is not critical for cognitive memory of contextual fear conditioning
Vazdarjanova, A., & McGaugh, J. L. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.25.15003 · Cited by 176 · see citing works
Neuronal responsiveness to various sensory stimuli, and associative learning in the rat amygdala.
Uwano, T., Nishijo, H., Ono, T., & Tamura, R. (1995) · Neuroscience · doi:10.1016/0306-4522(95)00125-3 · Cited by 176 · see citing works
Differential Fear Conditioning Induces Reciprocal Changes in the Sensory Responses of Lateral Amygdala Neurons to the CS+ and CS−
Collins, D. R., & Paré, D. (2000) · Learning & Memory · doi:10.1101/lm.7.2.97 · Cited by 171 · see citing works
Associative retuning in the thalamic source of input to the amygdala and auditory cortex: Receptive field plasticity in the medial division of the medial geniculate body.
Edeline, J., & Weinberger, N. M. (1992) · Behavioral Neuroscience · doi:10.1037/0735-7044.106.1.81 · Cited by 162 · see citing works
Multiple unit activity recorded from amygdala central nucleus during Pavlovian heart rate conditioning in rabbit
Applegate, C. D., Frysinger, R. C., Kapp, B. S., & Gallagher, M. (1982) · Brain Research · doi:10.1016/0006-8993(82)90123-8 · Cited by 147 · 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
Self-citation
Auditory fear conditioning increases CS‐elicited spike firing in lateral amygdala neurons even after extensive overtraining
Maren, S. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.00281.x · Cited by 139 · see citing works
Self-citation
Auditory-Evoked Spike Firing in the Lateral Amygdala and Pavlovian Fear Conditioning
Goosens, K. A., Hobin, J. A., & Maren, S. (2003) · Neuron · doi:10.1016/s0896-6273(03)00728-1 · Cited by 135 · see citing works
Self-citation
How the Brain Processes Emotional Information
Armony, J. L., & LeDoux, J. E. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb48285.x · Cited by 132 · see citing works
Multielectrode recordings: the next steps
Nicolelis, M. A. L., & Ribeiro, S. T. G. (2002) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(02)00374-4 · Cited by 119 · see citing works
Injections of the NMDA Receptor Antagonist Aminophosphonopentanoic Acid into the Lateral Nucleus of the Amygdala Block the Expression of Fear-Potentiated Startle and Freezing
Fendt, M. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-11-04111.2001 · Cited by 117 · see citing works
Putative Cortical and Thalamic Inputs Elicit Convergent Excitation in a Population of GABAergic Interneurons of the Lateral Amygdala
Szinyei, C., Heinbockel, T., Montagne, J., & Pape, H. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-23-08909.2000 · Cited by 111 · see citing works
Modification of auditory and somatosensory system activity during pupillary conditioning in the paralyzed cat
Oleson, T., Ashe, J. H., & Weinberger, N. M. (1975) · Journal of Neurophysiology · doi:10.1152/jn.1975.38.5.1114 · Cited by 111 · see citing works
NMDA receptors are essential for the acquisition, but not expression, of conditional fear and associative spike firing in the lateral amygdala
Goosens, K. A., & Maren, S. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03513.x · Cited by 108 · see citing works
Self-citation
Neurobiological mechanisms of emotionally influenced, long-term memory
Cahill, L. (2000) · Progress in Brain Research · doi:10.1016/s0079-6123(00)26004-4 · Cited by 102 · see citing works
Conditioned eye blink: unit activity at coronal-precruciate cortex of the cat.
Woody, C. D., Vassilevsky, N. N., & Engel, J. (1970) · Journal of Neurophysiology · doi:10.1152/jn.1970.33.6.851 · Cited by 99 · see citing works
Effects of contextual conditioning and unconditional stimulus presentation on performance in appetitive conditioning.
Bouton, M. E., Rosengard, C., Achenbach, G. G., Peck, C. A., & Brooks, D. C. (1993) · PubMed · Cited by 90 · see citing works
Trial sequence of changed unit activity in auditory system of alert rat during conditioned response acquisition and extinction
Disterhoft, J. F., & Stuart, D. K. (1976) · Journal of Neurophysiology · doi:10.1152/jn.1976.39.2.266 · Cited by 89 · see citing works
Amygdalar Efferents Initiate Auditory Thalamic Discriminative Training-Induced Neuronal Activity
Poremba, A., & Gabriel, M. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-01-00270.2001 · Cited by 82 · see citing works
Differential development of conditioned unit changes in thalamus and cortex of rat.
Disterhoft, J. F., & Olds, J. (1972) · Journal of Neurophysiology · doi:10.1152/jn.1972.35.5.665 · Cited by 75 · see citing works
Role of amygdala oscillations in the consolidation of emotional memories
Pelletier, J. G., & Paré, D. (2004) · Biological Psychiatry · doi:10.1016/j.biopsych.2003.08.019 · Cited by 71 · see citing works
Fear and the modification of acoustically evoked potentials during conditioning.
Hall, R. D., & Mark, R. G. (1967) · Journal of Neurophysiology · doi:10.1152/jn.1967.30.4.893 · Cited by 65 · see citing works
Extralemniscal activation of auditory cortex in cats
Galambos, R., Myers, R. E., & Sheatz, G. C. (1961) · American Journal of Physiology-Legacy Content · doi:10.1152/ajplegacy.1961.200.1.23 · Cited by 62 · see citing works
Discriminative long-term retention of rapidly induced multiunit changes in the hippocampus, medial geniculate and auditory cortex
Edeline, J., Massioui, N. E., & Dutrieux, G. (1990) · Behavioural Brain Research · doi:10.1016/0166-4328(90)90101-j · Cited by 51 · see citing works
Response patterns of thalamic neurons during classical conditioning
KAMIKAWA, K., McIlwain, J. T., & ADEY, W. R. (1964) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(64)90178-6 · Cited by 49 · see citing works
Plasticity at unitary level. II. Modifications during sensory-sensory association procedures
Ben‐Ari, Y., & Salle, G. L. G. L. (1972) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(72)90103-4 · Cited by 46 · see citing works
Serotonin-1A antagonists attenuate the effects of nicotine withdrawal on the auditory startle response
Rasmussen, K., Kallman, M. J., & Helton, D. R. (1997) · Synapse · doi:10.1002/(sici)1098-2396(199710)27:2 · Cited by 43 · see citing works
Single-cell activity in cat motor cortex. I. Modifications during classical conditioning procedures.
O’Brien, J. H., & Fox, S. S. (1969) · Journal of Neurophysiology · doi:10.1152/jn.1969.32.3.267 · Cited by 43 · see citing works
Intrinsic circuitry of the amygdaloid complex: common principles of organization in rats and cats
Paré, D., & Smith, Y. (1998) · Trends in Neurosciences · doi:10.1016/s0166-2236(98)01240-5 · Cited by 41 · see citing works
Lateral amygdala unit activity: II. Habituating and non-habituating neurons
Ben‐Ari, Y., & Salle, G. L. G. L. (1974) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(74)90087-x · Cited by 29 · see citing works
Short-latency discriminative unit response: Engram or bias?
Gabriel, M. (1976) · Physiological Psychology · doi:10.3758/bf03332870 · Cited by 25 · see citing works
Experimental procedures affecting evoked responses recorded from auditory cortex
Gerken, G. M., & Neff, W. D. (1963) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(63)90139-1 · Cited by 23 · see citing works
Modification of unit discharges in the medial geniculate nucleus by click-shock pairing
Weinberger, N. M., Imig, T. J., & Lippe, W. R. (1972) · Experimental Neurology · doi:10.1016/0014-4886(72)90135-5 · Cited by 15 · see citing works
Acquisition and Retention
Salthouse, T. A. (1982) · Springer series in cognitive development · doi:10.1007/978-1-4613-9484-6_7 · Cited by 12 · see citing works
Learning Not to Fear, Faster: Figure 1Preprint
Quirk, G. J. (2004) · Learning & Memory · doi:10.1101/lm.75404 · Cited by 12 · see citing works
Self-citation
Cortico-hippocampal communication by way of parallel parahippocampal-subicular pathways.
Lavenex (2000) · Pure Amsterdam UMC · doi:10.1002/1098-1063(2000)10:4 · Cited by 1 · see citing works

Flagged first, then by citations

Research works printed but not linked: 1

Davis, M. in The Amygdala (ed. Aggleton, J. P.) 213-288 (Oxford Univ. Press, Oxford, 2000).

Sorted by citations

The Microbiota-Gut-Brain Axis
Cryan, J. F., O'Riordan, K. J., Cowan, C. S. M., Sandhu, K. V., Bastiaanssen, T. F. S., Boehme, M., Codagnone, M. G., Cussotto, S., Fulling, C., Golubeva, A. V., et al. (2019) · Physiological Reviews · doi:10.1152/physrev.00018.2018 · Cited by 5,286 · see citing works
The Adolescent Brain
Casey, B. J., Jones, R. M., & Hare, T. A. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1440.010 · Cited by 3,345 · see citing works
5-HTTLPR polymorphism impacts human cingulate-amygdala interactions: a genetic susceptibility mechanism for depression
Pezawas, L., Meyer-Lindenberg, A., Drabant, E. M., Verchinski, B. A., Munoz, K. E., Kolachana, B. S., Egan, M. F., Mattay, V. S., Hariri, A. R., & Weinberger, D. R. (2005) · Nature Neuroscience · doi:10.1038/nn1463 · Cited by 1,980 · see citing works
Cognitive neuroscience of emotional memory
LaBar, K. S., & Cabeza, R. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1825 · Cited by 1,834 · see citing works
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
Stress, memory and the amygdala
Roozendaal, B., McEwen, B. S., & Chattarji, S. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2651 · Cited by 1,760 · see citing works
Neural Mechanisms of Extinction Learning and Retrieval
Quirk, G. J., & Mueller, D. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301555 · Cited by 1,645 · see citing works
Self-citation
Optimizing inhibitory learning during exposure therapy
Craske, M. G., Kircanski, K., Zelikowsky, M., Mystkowski, J., Chowdhury, N., & Baker, A. (2008) · Behaviour Research and Therapy · doi:10.1016/j.brat.2007.10.003 · Cited by 1,607 · see citing works
The contextual brain: implications for fear conditioning, extinction and psychopathology
Maren, S., Phan, K. L., & Liberzon, I. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3492 · Cited by 1,547 · see citing works
Self-citation
Rethinking the Emotional Brain
LeDoux, J. (2012) · Neuron · doi:10.1016/j.neuron.2012.02.004 · Cited by 1,594 · see citing works
“…medial CEA (CEm) to the ventrolateral PAG (PAGvl) (Johansen et al., 2011; LeDoux, 2000; Maren, 2001; Fanselow and Poulos, 2005; Davis et al., 1997; Rosenkranz and Grace, 2002; Cousens and Otto, 1998; Paré et al., 2004; Maren and Quirk, 2004; Quirk and Mueller, 2008; Haubensak et al., 2010).”
The neural bases of emotion regulation
Etkin, A., Büchel, C., & Gross, J. J. (2015) · Nature Reviews Neuroscience · doi:10.1038/nrn4044 · Cited by 1,244 · 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
Epigenetics and the biological definition of gene×environment interactions
Meaney, M. J. (2010) · Child Development · doi:10.1111/j.1467-8624.2009.01381.x · Cited by 1,239 · see citing works
Recall of Fear Extinction in Humans Activates the Ventromedial Prefrontal Cortex and Hippocampus in Concert
Milad, M. R., Wright, C. I., Orr, S. P., Pitman, R. K., Quirk, G. J., & Rauch, S. L. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.10.011 · Cited by 1,197 · see citing works
Self-citation
Failure to Regulate: Counterproductive Recruitment of Top-Down Prefrontal-Subcortical Circuitry in Major Depression
Johnstone, T., van Reekum, C. M., Urry, H. L., Kalin, N. H., & Davidson, R. J. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2063-07.2007 · Cited by 1,051 · 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
Neurocognitive mechanisms of anxiety: An integrative account
Bishop, S. J. (2007) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2007.05.008 · Cited by 976 · see citing works
Cortico-Basal Ganglia Reward Network: Microcircuitry
Sesack, S. R., & Grace, A. A. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.93 · Cited by 985 · see citing works
Engineering a memory with LTD and LTP
Nabavi, S., Fox, R., Proulx, C. D., Lin, J. Y., Tsien, R. Y., & Malinow, R. (2014) · Nature · doi:10.1038/nature13294 · Cited by 980 · see citing works
Encoding of conditioned fear in central amygdala inhibitory circuits
Ciocchi, S., Herry, C., Grenier, F., Wolff, S. B. E., Letzkus, J. J., Vlachos, I., Ehrlich, I., Sprengel, R., Deisseroth, K., Stadler, M. B., et al. (2010) · Nature · doi:10.1038/nature09559 · Cited by 924 · see citing works
Creating a False Memory in the Hippocampus
Ramirez, S., Liu, X., Lin, P.-A., Suh, J., Pignatelli, M., Redondo, R. L., Ryan, T. J., & Tonegawa, S. (2013) · Science · doi:10.1126/science.1239073 · Cited by 968 · see citing works
The primate amygdala represents the positive and negative value of visual stimuli during learning
Paton, J. J., Belova, M. A., Morrison, S. E., & Salzman, C. D. (2006) · Nature · doi:10.1038/nature04490 · Cited by 917 · 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
Learned helplessness at fifty: Insights from neuroscience.
Maier, S. F., & Seligman, M. E. P. (2016) · Psychological Review · doi:10.1037/rev0000033 · Cited by 919 · see citing works
“From there the information passes to the central nucleus of the amygdala, which in turns projects to the regions that control the behaviors and physiological responses that are the symptoms of fear (Davis, Rainnie, & Cassell, 1994; Le- Doux, 2003; Maren & Quirk, 2004).”
Background
Excitatory transmission from the amygdala to nucleus accumbens facilitates reward seeking
Stuber, G. D., Sparta, D. R., Stamatakis, A. M., van Leeuwen, W. A., Hardjoprajitno, J. E., Cho, S., Tye, K. M., Kempadoo, K. A., Zhang, F., Deisseroth, K., et al. (2011) · Nature · doi:10.1038/nature10194 · Cited by 878 · see citing works
Amygdala inhibitory circuits and the control of fear memory
Ehrlich, I., Humeau, Y., Grenier, F., Ciocchi, S., Herry, C., & Lüthi, A. (2009) · Neuron · doi:10.1016/j.neuron.2009.05.026 · Cited by 878 · see citing works
Genetic dissection of an amygdala microcircuit that gates conditioned fear
Haubensak, W., Kunwar, P. S., Cai, H., Ciocchi, S., Wall, N. R., Ponnusamy, R., Biag, J., Dong, H.-W., Deisseroth, K., Callaway, E. M., et al. (2010) · Nature · doi:10.1038/nature09553 · Cited by 840 · see citing works
“To avoid masking of the consequences of the experimental manipulation by ceiling and floor effects, the number of training trials (3-6) was adjusted such that freezing levels averaged around 50 % in the genetic/viral control.”
Method
Signaling Mechanisms Linking Neuronal Activity to Gene Expression and Plasticity of the Nervous System
Flavell, S. W., & Greenberg, M. E. (2008) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.31.060407.125631 · Cited by 832 · 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
Histone Deacetylase Inhibitors Enhance Memory and Synaptic Plasticity via CREB: CBP-Dependent Transcriptional Activation
Vecsey, C. G., Hawk, J. D., Lattal, K. M., Stein, J. M., Fabian, S., Attner, M. A., Cabrera, S. M., McDonough, C. B., Brindle, P. K., Abel, T. G., et al. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.0296-07.2007 · Cited by 828 · see citing works
Perineuronal Nets Protect Fear Memories from Erasure
Gogolla, N., Caroni, P., Lüthi, A., & Herry, C. (2009) · Science · doi:10.1126/science.1174146 · Cited by 760 · see citing works
Post-traumatic stress disorder is associated with PACAP and the PAC1 receptor
Ressler, K. J., Mercer, K. B., Bradley, B., Jovanovic, T., Mahan, A., Kerley, K., Norrholm, S. D., Kilaru, V., Smith, A. K., Myers, A. J., et al. (2011) · Nature · doi:10.1038/nature09856 · Cited by 800 · see citing works
ENDOCANNABINOID-MEDIATED SYNAPTIC PLASTICITY IN THE CNS
Chevaleyre, V., Takahashi, K. A., & Castillo, P. E. (2006) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.29.051605.112834 · Cited by 779 · 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
“Descending projections from the PFC appear to provide an inhibitory inﬂuence over lower brain structures involved in emotion-ality, such as the amygdala, dorsal raphe and hypothalamus (Arnsten and Goldman-Rakic [428]; Sesack and Pickel [429]; Rempel-Clower and Barbas [430]; Haj´os et al. [431]; Quirk and Gehlert [432]…”
Background
Resolving the neural circuits of anxiety
Calhoon, G. G., & Tye, K. M. (2015) · Nature Neuroscience · doi:10.1038/nn.4101 · Cited by 766 · see citing works
The propositional nature of human associative learning
Mitchell, C. J., Houwer, J. D., & Lovibond, P. F. (2009) · Behavioral and Brain Sciences · doi:10.1017/s0140525x09000855 · Cited by 749 · see citing works
Dopamine system dysregulation in major depressive disorders
Belujon, P., & Grace, A. A. (2017) · International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyx056 · Cited by 754 · see citing works
A framework for studying emotions across species
Anderson, D. J., & Adolphs, R. (2014) · Cell · doi:10.1016/j.cell.2014.03.003 · Cited by 691 · see citing works
A unified framework for inhibitory control
Munakata, Y., Herd, S. A., Chatham, C. H., Depue, B. E., Banich, M. T., & O’Reilly, R. C. (2011) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2011.07.011 · Cited by 699 · see citing works
Contextual and temporal modulation of extinction: behavioral and biological mechanisms
Bouton, M. E., Westbrook, R. F., Corcoran, K. A., & Maren, S. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.12.015 · Cited by 671 · see citing works
Self-citation
From Synapse to Nucleus: Calcium-Dependent Gene Transcription in the Control of Synapse Development and Function
Greer, P. L., & Greenberg, M. E. (2008) · Neuron · doi:10.1016/j.neuron.2008.09.002 · Cited by 661 · see citing works
Prefrontal control of fear: more than just extinction
Sotres-Bayon, F., & Quirk, G. J. (2010) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2010.02.005 · Cited by 625 · see citing works
“However, unlike neurons in lateral amygdala whose conditioned responses last only a few hundred milliseconds [32], PL neurons show sustained increases in activity that mirror the time course of freezing responses, lasting tens of seconds [31 ].”
BackgroundSelf-citation
Stress effects on the hippocampus: a critical review
Kim, E. J., Pellman, B., & Kim, J. J. (2015) · Learning & Memory · doi:10.1101/lm.037291.114 · Cited by 620 · see citing works
Why ritualized behavior? Precaution Systems and action parsing in developmental, pathological and cultural rituals
Boyer, P., & Liénard, P. (2006) · Behavioral and Brain Sciences · doi:10.1017/s0140525x06009332 · Cited by 601 · see citing works
Memory Engram Cells Have Come of Age
Tonegawa, S., Liu, X., Ramirez, S., & Redondo, R. L. (2015) · Neuron · doi:10.1016/j.neuron.2015.08.002 · Cited by 613 · see citing works
Fear extinction in rats: Implications for human brain imaging and anxiety disorders
Milad, M. R., Rauch, S. L., Pitman, R. K., & Quirk, G. J. (2006) · Biological Psychology · doi:10.1016/j.biopsycho.2006.01.008 · Cited by 597 · see citing works
Self-citation
Water associated zero maze: a novel rat test for long term traumatic re-experiencing
Ritov, G., & Richter‐Levin, G. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00001 · Cited by 579 · see citing works
Selective Erasure of a Fear Memory
Han, J., Kushner, S. A., Yiu, A. P., Hsiang, H., Buch, T., Waisman, A., Bontempi, B., Neve, R. L., Frankland, P. W., & Josselyn, S. A. (2009) · Science · doi:10.1126/science.1164139 · Cited by 570 · see citing works
Epigenetics and the environmental regulation of the genome and its function
Zhang, T.-Y., & Meaney, M. J. (2010) · Annual Review of Psychology · doi:10.1146/annurev.psych.60.110707.163625 · Cited by 565 · see citing works
Sustained Conditioned Responses in Prelimbic Prefrontal Neurons Are Correlated with Fear Expression and Extinction Failure
Burgos-Robles, A., Vidal-Gonzalez, I., & Quirk, G. J. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0378-09.2009 · Cited by 530 · see citing works
Self-citation
Disturbed dreaming, posttraumatic stress disorder, and affect distress: A review and neurocognitive model.
Levin, R., & Nielsen, T. A. (2007) · Psychological Bulletin · doi:10.1037/0033-2909.133.3.482 · Cited by 554 · see citing works
The Influence of Stress Hormones on Fear Circuitry
Rodrigues, S. M., LeDoux, J. E., & Sapolsky, R. M. (2009) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.051508.135620 · Cited by 556 · see citing works
Dynamics of Retrieval Strategies for Remote Memories
Goshen, I., Brodsky, M., Prakash, R., Wallace, J. L., Gradinaru, V., Ramakrishnan, C., & Deisseroth, K. A. (2011) · Cell · doi:10.1016/j.cell.2011.09.033 · Cited by 546 · see citing works
Presence and acquired origin of reduced recall for fear extinction in PTSD: Results of a twin study
Milad, M. R., Orr, S. P., Lasko, N. B., Chang, Y., Rauch, S. L., & Pitman, R. K. (2008) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2008.01.017 · Cited by 512 · see citing works
Consolidation of Fear Extinction Requires NMDA Receptor-Dependent Bursting in the Ventromedial Prefrontal Cortex
Burgos-Robles, A., Vidal-Gonzalez, I., Santini, E., & Quirk, G. J. (2007) · Neuron · doi:10.1016/j.neuron.2007.02.021 · Cited by 516 · see citing works
Self-citation
The Role of the Medial Prefrontal Cortex in the Conditioning and Extinction of Fear
Giustino, T. F., & Maren, S. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00298 · Cited by 519 · see citing works
Self-citation
Experience-dependent modification of a central amygdala fear circuit
Li, H., Penzo, M. A., Taniguchi, H., Kopec, C. D., Huang, Z. J., & Li, B. (2013) · Nature Neuroscience · doi:10.1038/nn.3322 · Cited by 497 · see citing works
Amygdala interneuron subtypes control fear learning through disinhibition
Wolff, S. B. E., Gründemann, J., Tovote, P., Krabbe, S., Jacobson, G. A., Müller, C. R., Herry, C., Ehrlich, I., Friedrich, R. W., Letzkus, J. J., et al. (2014) · Nature · doi:10.1038/nature13258 · Cited by 489 · see citing works
Basolateral Amygdala Neurons Facilitate Reward-Seeking Behavior by Exciting Nucleus Accumbens Neurons
Ambroggi, F., Ishikawa, A., Fields, H. L., & Nicola, S. M. (2008) · Neuron · doi:10.1016/j.neuron.2008.07.004 · Cited by 488 · see citing works
A Role for the Human Dorsal Anterior Cingulate Cortex in Fear Expression
Milad, M. R., Quirk, G. J., Pitman, R. K., Orr, S. P., Fischl, B., & Rauch, S. L. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.04.032 · Cited by 485 · see citing works
Self-citation
Neuronal circuits of fear extinction
Herry, C., Ferraguti, F., Singewald, N., Letzkus, J. J., Ehrlich, I., & Lüthi, A. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07101.x · Cited by 484 · see citing works
Encoding of fear learning and memory in distributed neuronal circuits
Herry, C., & Johansen, J. P. (2014) · Nature Neuroscience · doi:10.1038/nn.3869 · Cited by 474 · 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
The default mode network and social understanding of others: what do brain connectivity studies tell us
Li, W., Mai, X., & Liu, C. (2014) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2014.00074 · Cited by 459 · 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
Gating of Fear in Prelimbic Cortex by Hippocampal and Amygdala Inputs
Sotres-Bayón, F., Sierra‐Mercado, D., Pardilla‐Delgado, E., & Quirk, G. J. (2012) · Neuron · doi:10.1016/j.neuron.2012.09.028 · Cited by 451 · see citing works
Self-citation
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
Neural and cellular mechanisms of fear and extinction memory formation
Orsini, C. A., & Maren, S. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.12.014 · Cited by 429 · see citing works
Self-citation
Thickness of ventromedial prefrontal cortex in humans is correlated with extinction memory
Milad, M. R., Quinn, B. T., Pitman, R. K., Orr, S. P., Fischl, B., & Rauch, S. L. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0502441102 · Cited by 412 · see citing works
Morphological and functional reorganization of rat medial prefrontal cortex in neuropathic pain
Metz, A. E., Yau, H.-J., Centeno, M. V., Apkarian, A. V., & Martina, M. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0809897106 · Cited by 407 · see citing works
Stress and Fear Extinction
Maren, S., & Holmes, A. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2015.180 · Cited by 412 · see citing works
Self-citation
Disinhibition, a Circuit Mechanism for Associative Learning and Memory
Letzkus, J. J., Wolff, S. B. E., & Lüthi, A. (2015) · Neuron · doi:10.1016/j.neuron.2015.09.024 · Cited by 401 · see citing works
The Study of Fear Extinction: Implications for Anxiety Disorders
Graham, B. M., & Milad, M. R. (2011) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2011.11040557 · Cited by 387 · see citing works
Behavioral and neurobiological mechanisms of pavlovian and instrumental extinction learning
Bouton, M. E., Maren, S., & McNally, G. P. (2020) · Physiological Reviews · doi:10.1152/physrev.00016.2020 · Cited by 399 · see citing works
Self-citation
A validated network of effective amygdala connectivity
Stein, J. L., Wiedholz, L. M., Bassett, D. S., Weinberger, D. R., Zink, C. F., Mattay, V. S., & Meyer-Lindenberg, A. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.03.022 · Cited by 392 · see citing works
Hippocampal Inactivation Disrupts the Acquisition and Contextual Encoding of Fear Extinction
Corcoran, K., Desmond, T., Frey, K., & Maren, S. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2246-05.2005 · Cited by 390 · see citing works
Self-citation
Cognitive Impairment in Pain through Amygdala-Driven Prefrontal Cortical Deactivation
Ji, G., Sun, H., Fu, Y., Li, Z., Pais-Vieira, M., Galhardo, V., & Neugebauer, V. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0225-10.2010 · Cited by 387 · 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
Synaptic Encoding of Fear Extinction in mPFC-amygdala Circuits
Cho, J.-H., Deisseroth, K. A., & Bolshakov, V. Y. (2013) · Neuron · doi:10.1016/j.neuron.2013.09.025 · Cited by 367 · see citing works
Regulation of neuronal GABAB receptor functions by subunit composition
Gassmann, M., & Bettler, B. (2012) · Nature reviews. Neuroscience · doi:10.1038/nrn3249 · Cited by 364 · see citing works
Parvalbumin-Positive Basket Cells Differentiate among Hippocampal Pyramidal Cells
Lee, S.-H., Marchionni, I., Bezaire, M., Varga, C., Danielson, N., Lovett-Barron, M., Losonczy, A., & Soltesz, I. (2014) · Neuron · doi:10.1016/j.neuron.2014.03.034 · Cited by 358 · see citing works
Affective communication in rodents: ultrasonic vocalizations as a tool for research on emotion and motivation
Wöhr, M., & Schwarting, R. K. W. (2013) · Cell and Tissue Research · doi:10.1007/s00441-013-1607-9 · Cited by 371 · see citing works
Neural ensemble dynamics underlying a long-term associative memory
Grewe, B. F., Gründemann, J., Kitch, L. J., Lecoq, J. A., Parker, J. G., Marshall, J. D., Larkin, M. C., Jercog, P. E., Grenier, F., Li, J. Z., et al. (2017) · Nature · doi:10.1038/nature21682 · Cited by 351 · see citing works
Synaptic Mechanisms of Associative Memory in the Amygdala
Maren, S. (2005) · Neuron · doi:10.1016/j.neuron.2005.08.009 · Cited by 341 · see citing works
Self-citation
Amygdala inputs to prefrontal cortex guide behavior amid conflicting cues of reward and punishment
Burgos-Robles, A., Kimchi, E. Y., Izadmehr, E. M., Porzenheim, M. J., Ramos-Guasp, W. A., Nieh, E. H., Felix-Ortiz, A. C., Namburi, P., Leppla, C. A., Presbrey, K. N., et al. (2017) · Nature Neuroscience · doi:10.1038/nn.4553 · Cited by 318 · see citing works
Coherent amygdalocortical theta promotes fear memory consolidation during paradoxical sleep
Popa, D., Duvarci, S., Popescu, A. T., Léna, C., & Paré, D. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0913016107 · Cited by 338 · see citing works
Neural substrates for expectation-modulated fear learning in the amygdala and periaqueductal gray
Johansen, J. P., Tarpley, J. W., LeDoux, J. E., & Blair, H. T. (2010) · Nature Neuroscience · doi:10.1038/nn.2594 · Cited by 312 · see citing works
Emotion, decision making, and the amygdala.
Seymour, B., & Dolan, R. (2008) · Neuron · doi:10.1016/j.neuron.2008.05.020 · Cited by 324 · see citing works
Multiple anatomical systems embedded within the primate medial temporal lobe: Implications for hippocampal function
Aggleton, J. P. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.09.005 · Cited by 319 · see citing works
The amygdala and medial prefrontal cortex: partners in the fear circuit
Marek, R., Strobel, C., Bredy, T. W., & Sah, P. (2013) · The Journal of Physiology · doi:10.1113/jphysiol.2012.248575 · Cited by 304 · see citing works
Placing prediction into the fear circuit
McNally, G. P., Johansen, J. P., & Blair, H. T. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.03.005 · Cited by 298 · see citing works
Prefrontal-Hippocampal Interactions in Memory and Emotion
Jin, J., & Maren, S. (2015) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2015.00170 · Cited by 313 · see citing works
“Contextual retrieval is also critical for organizing defensive behaviors related to emotional memories (Bouton, 2002; Maren and Quirk, 2004; Maren et al., 2013).”
BackgroundSelf-citation
Organization of valence-encoding and projection-defined neurons in the basolateral amygdala
Beyeler, A., Chang, C.-J., Silvestre, M., Lévêque, C., Namburi, P., Wildes, C. P., & Tye, K. M. (2018) · Cell Reports · doi:10.1016/j.celrep.2017.12.097 · Cited by 306 · see citing works
“This may synthesize apparently conflicting studies reporting the role of the CeA in freezing and avoidance (Ciocchi et al., 2010; Davis and Shi, 1999; Duvarci and Pare, 2014; Fadok et al., 2017; Goosens and Maren, 2001; Haubensak et al., 2010; Jimenez and Maren, 2009; Li et al., 2013; Maren and Quirk, 2004; Penzo et a…”
BackgroundInfluential
Fear-Conditioning Mechanisms Associated with Trait Vulnerability to Anxiety in Humans
Indovina, I., Robbins, T. W., Núñez-Elizalde, A. O., Dunn, B. D., & Bishop, S. J. (2011) · Neuron · doi:10.1016/j.neuron.2010.12.034 · Cited by 310 · see citing works
Optical activation of lateral amygdala pyramidal cells instructs associative fear learning
Johansen, J. P., Hamanaka, H., Monfils, M. H., Behnia, R., Deisseroth, K., Blair, H. T., & LeDoux, J. E. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1002418107 · Cited by 308 · see citing works
The Persistence and Transience of Memory
Richards, B. A., & Frankland, P. W. (2017) · Neuron · doi:10.1016/j.neuron.2017.04.037 · Cited by 304 · see citing works
Fear and safety engage competing patterns of theta-gamma coupling in the basolateral amygdala
Stujenske, J. M., Likhtik, E., Topiwala, M. A., & Gordon, J. A. (2014) · Neuron · doi:10.1016/j.neuron.2014.07.026 · Cited by 303 · see citing works
Synaptic tagging during memory allocation
Rogerson, T., Cai, D. J., Frank, A. C., Sano, Y., Shobe, J. L., López‐Aranda, M. F., & Silva, A. J. (2014) · Nature reviews. Neuroscience · doi:10.1038/nrn3667 · Cited by 305 · 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
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
Plasticity of amygdala neurons underlying fear learning and extinction
Morozov, A., & Ito, W. (2020) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-815134-1.00006-4 · Cited by 4 · see citing works
Computational Modeling of Lateral Amygdala Neurons During Acquisition and Extinction of Conditioned Fear, Using Hebbian Learning
Li, G., Cheng, S. H., Ko, F. C., Raunch, S. L., Quirk, G. J., & Nair, S. S. (2006) · doi:10.1115/imece2006-15078
Self-citation
Encoding of fear learning and memory in distributed neuronal circuits
Herry, C., & Johansen, J. P. (2014) · Nature Neuroscience · doi:10.1038/nn.3869 · Cited by 474 · 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

Authors: Maren, S., & Quirk, G. J.
Affiliations: University of Michigan (US)
Ponce Health Sciences University (PR)
ORCID: Maren, Stephen
Quirk, Gregory J.
Venue: Nature Reviews Neuroscience
Publisher: Springer Science and Business Media LLC
Published: 2004-11
Volume: 5
Issue: 11
Pages: 844-852
ISSN: 1471-003X (ISSN-L)
1471-0048
DOI: 10.1038/nrn1535
OpenAlex: W1967887989
Cited by: 1,428
References: 109
Citations by year: 2026: 32 · 2025: 45 · 2024: 49 · 2023: 41 · 2022: 61 · 2021: 50 · 2020: 96 · 2019: 59 · 2018: 58 · 2017: 70 · 2016: 74 · 2015: 83 · 2014: 76 · 2013: 90 · 2012: 85
FWCI: 4.78
Type: journal article
Language: en
Open access: green
hdl.handle.net
Licence: www.springer.com/tdm (tdm)
Locations: Nature reviews. Neuroscience (publishedVersion)
PubMed (publishedVersion)
Deep Blue (University of Michigan) (submittedVersion)
Funders: National Institutes of Health
National Institute of Mental Health
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 memory, lateral amygdala, fear conditioning, fear extinction, neural coding, aversive memory, associative plasticity, hippocampus, prefrontal cortex
MeSH terms: Amygdala, Animals, Extinction, Psychological, Fear, Humans, Memory, Neural Inhibition, Neuronal Plasticity, Neurons, Signal Transduction

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

Neuronal signalling of fear memory

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks