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Neuronal signalling of fear memory
Open accessAbstract
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.
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“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
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
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“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
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“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
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“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
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“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
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“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
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“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]
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“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]
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“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]
In the citing paper
“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]
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“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]
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“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]
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Intrinsic circuitry of the amygdaloid complex: common principles of organization in rats and cats
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Lateral amygdala unit activity: II. Habituating and non-habituating neurons
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Short-latency discriminative unit response: Engram or bias?
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Experimental procedures affecting evoked responses recorded from auditory cortex
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Modification of unit discharges in the medial geniculate nucleus by click-shock pairing
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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
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
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
Cognitive neuroscience of emotional memory
LaBar, K. S., & Cabeza, R. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1825 · Cited by 1,834
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
Metadata
- Authors
- Maren, S., & Quirk, G. J.
- Affiliations
- University of Michigan (US)
- Ponce Health Sciences University (PR)
- Venue
- Nature Reviews Neuroscience
- Published
- 2004-11
- Volume
- 5
- Issue
- 11
- Pages
- 844-852
- ISSN
- 1471-003X (ISSN-L)
- 1471-0048
- 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.
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