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Experience-dependent modification of a central amygdala fear circuit
Open accessAbstract
The amygdala is essential for fear learning and expression. The central amygdala (CeA), once viewed as a passive relay between the amygdala complex and downstream fear effectors, has emerged as an active participant in fear conditioning. However, the mechanism by which CeA contributes to the learning and expression of fear is unclear. We found that fear conditioning in mice induced robust plasticity of excitatory synapses onto inhibitory neurons in the lateral subdivision of the CeA (CeL). This experience-dependent plasticity was cell specific, bidirectional and expressed presynaptically by inputs from the lateral amygdala. In particular, preventing synaptic potentiation onto somatostatin-positive neurons impaired fear memory formation. Furthermore, activation of these neurons was necessary for fear memory recall and was sufficient to drive fear responses. Our findings support a model in which fear conditioning-induced synaptic modifications in CeL favor the activation of somatostatin-positive neurons, which inhibit CeL output, thereby disinhibiting the medial subdivision of CeA and releasing fear expression.
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“In this circuit, glutamatergic signals from the BLA are conducted onward to the CeL, where they impinge on two populations of mutually inhibitory GABAergic neurons, the protein kinase C-δ (PKCδ)-negative CeLON cells and the PKCδ-positive CeLOFF cells72,75.”
From Resolving the neural circuits of anxiety (2015) · cites this paper as [75]
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“Activation of somatostatin (SOM)-positive CeL neurons by the lateral amygdala75 and paraventricular nucleus of the thalamus76,77 has also been shown to drive fear learning through an overall increase in inhibition in the CeL.”
From Resolving the neural circuits of anxiety (2015) · cites this paper as [75]
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InfluentialBrain circuit dysfunction in post-traumatic stress disorder: from mouse to man
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InfluentialContributions of the central extended amygdala to fear and anxiety
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Central amygdala circuits modulate food consumption through a positive-valence mechanism
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New perspectives on central amygdala function
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MethodInfluentialSelf-citationDual and Opposing Functions of the Central Amygdala in the Modulation of Pain
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“Previous studies have shown, however, that CeA-PKCδ and CeA-Som neurons are synaptically interconnected and can inhibit each other (Ciocchi et al., 2010; Haubensak et al., 2010; Hunt et al., 2017; Li et al., 2013).”
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A Neural Circuit for the Suppression of Pain by a Competing Need State
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MethodFunctional heterogeneity in the bed nucleus of the stria terminalis
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“Indeed, different subsets of CeL neurons reciprocally inhibit each other and form different connections with CeM (Ciocchi et al., 2010; Haubensak et al., 2010; Viviani et al., 2011; Li et al., 2013).”
BackgroundNPY signaling inhibits extended amygdala CRF neurons to suppress binge alcohol drinking
Pleil, K. E., Rinker, J. A., Lowery-Gionta, E. G., Mazzone, C. M., McCall, N. M., Kendra, A. M., Olson, D. P., Lowell, B. B., Grant, K. A., Thiele, T. E., et al. (2015) · Nature Neuroscience · doi:10.1038/nn.3972 · Cited by 195
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BackgroundA Central Amygdala CRF Circuit Facilitates Learning about Weak Threats
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MethodInfluentialPathological circuit function underlying addiction and anxiety disorders
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Regulating anxiety with extrasynaptic inhibition
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“Fear learning also induces preLTP of lateral amygdala excitatory inputs onto somatostatin inhibitory interneurons in the central amygdala, and activation of these interneurons was sufficient to drive fear responses (Li et al. 2013).”
BackgroundHtr2a-Expressing Cells in the Central Amygdala Control the Hierarchy between Innate and Learned Fear
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The central amygdala controls learning in the lateral amygdala
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“1D) – an effect that is consistent with our previous findings (Li et al., 2013; Penzo et al., 2015).”
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Left and right hemispheric lateralization of the amygdala in pain
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“The CeA has been implicated in modulating emotional processes and it is known to have a role in fear and threat-conditioning (Baker and Kim, 2004; Haubensak et al., 2010; Li et al., 2013).”
BackgroundNovel designer receptors to probe GPCR signaling and physiology
Wess, J., Nakajima, K., & Jain, S. (2013) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2013.04.006 · Cited by 169
Central Amygdala Somatostatin Neurons Gate Passive and Active Defensive Behaviors
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“To this end, we implanted optical fibers bilaterally above the CeL of Som-Cre;Ai32 mice (Madisen et al., 2012), in which the light-sensitive cation channel channelrhodopsin-2 (ChR2; Zhang et al., 2006) is specifically expressed in SOM cells (Li et al., 2013; Fig.”
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Bonilla-Jaime, H., Sánchez-Salcedo, J. A., Estevez-Cabrera, M. M., Molina‐Jiménez, T., Cortes-Altamirano, J. L., & Alfaro-Rodríguez, A. (2021) · Current Neuropharmacology · doi:10.2174/1570159x19666210609161447 · Cited by 162
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“Li et al. (2013) showed an increase of synaptic strength from BLA inputs onto these SOM+ neurons, concomitant with decreased synaptic input onto SOM neurons after passive threat conditioning, i.e., following a conditioning protocol that did not allow for escape from the threat.”
BackgroundInfluentialA Central Extended Amygdala Circuit That Modulates Anxiety
Ahrens, S., Wu, M. V., Furlan, A., Hwang, G., Paik, R., Li, H., Penzo, M. A., Tollkühn, J., & Li, B. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.0705-18.2018 · Cited by 157
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MethodInfluentialSelf-citationNeuroimaging of fear-associated learning
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“…neurons are nearly exclusively GABAergic (Swanson and Petrovich 1998), and additionally express various neuropeptides, especially within the CEAl (e.g., Cassell et al. 1986; Day et al. 1999; Haubensak et al. 2010; Li et al. 2013; Marchant et al. 2007; Roberts et al. 1982; Wray and Hoffman 1983).”
InfluentialA Fear Memory Engram and Its Plasticity in the Hypothalamic Oxytocin System
Hasan, M. T., Althammer, F., Gouveia, M. D. S., Goyon, S., Eliava, M., Lefèvre, A., Kerspern, D., Schimmer, J., Raftogianni, A., Wahis, J., et al. (2019) · Neuron · doi:10.1016/j.neuron.2019.04.029 · Cited by 146
“We further found that, upon fear exposure, OT neurons show enhanced glutamatergic over OT-ergic transmission in the CeM (Figure 3D1) with increased membrane capacitance (Figure 5C2) and elevated vGluT2-levels in OT axons terminating in the CeA (Figure 5C3), consistent with previous studies (Ciocchi et al., 2010; Li et…”
Quantified Coexpression Analysis of Central Amygdala Subpopulations
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“2018 1–12 (Herry et al., 2008; Haubensak et al., 2010; Li et al., 2013a; Kim et al., 2017).”
BackgroundInfluentialSomatostatin and Somatostatin-Containing Neurons in Shaping Neuronal Activity and Plasticity
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“Synaptic potentiation onto SOM neurons in amygdala is required for the expression of conditioned fear (Li et al., 2013; Penzo et al., 2014).”
BackgroundBasolateral amygdala circuitry in positive and negative valence
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eIF2α controls memory consolidation via excitatory and somatostatin neurons
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Genetically identified amygdala–striatal circuits for valence-specific behaviors
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Self-citationSynaptic encoding of fear memories in the amygdala
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Central Amygdala Prepronociceptin-Expressing Neurons Mediate Palatable Food Consumption and Reward
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The Physiology of Fear: Reconceptualizing the Role of the Central Amygdala in Fear Learning
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“(81) studied another subset of CEl neurons, those that express the neuropeptide somatostatin (SOM), which are largely distinct from the PKC-" population.”
BackgroundPomrenze, M. B., Millan, E. Z., Hopf, F. W., Keiflin, R., Maiya, R., Blasio, A., Dadgar, J., Kharazia, V., de Guglielmo, G., Crawford, E. F., et al. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00487 · Cited by 130
“We determined that approximately 44.2 ± 0.7% of CeL CRF neurons co-localize with SOM+ neurons.”
BackgroundMethodInfluentialSerotonin in fear conditioning processes
Bauer, E. P. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.07.028 · Cited by 136
Sex differences in fear extinction
Velasco, E. R., Florido, A., Milad, M. R., & Andero, R. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.05.020 · Cited by 132
“Besides this, the CeA is also involved in plasticity, nociception and the hierarchical organization of defensive behaviors (Balleine and Killcross, 2006; Cardinal et al., 2002; Ehrlich et al., 2009; Fadok et al., 2017; Isosaka et al., 2015; Li et al., 2013).”
BackgroundErbB4 regulation of a thalamic reticular nucleus circuit for sensory selection
Ahrens, S., Jaramillo, S., Yu, K., Ghosh, S., Hwang, G., Paik, R., Lai, C., He, M., Huang, Z. J., & Li, B. (2014) · Nature Neuroscience · doi:10.1038/nn.3897 · Cited by 129
Self-citationA feedback neural circuit for calibrating aversive memory strength
Ozawa, T., Ycu, E. A., Kumar, A., Yeh, L.-F., Ahmed, T., Koivumaa, J., & Johansen, J. P. (2016) · Nature Neuroscience · doi:10.1038/nn.4439 · Cited by 129
Chen, Y.-H., Wu, J., Hu, N.-Y., Zhuang, J.-P., Li, W., Zhang, S.-R., Li, X.-W., Yang, J., & Gao, T. (2021) · Journal of Clinical Investigation · doi:10.1172/jci145692 · Cited by 126
“(F–H) CeM-ChR2–projecting mice showed increased open-arm exploration [F, Finteraction (4,38) = 15.”
BackgroundInfluentialSynaptic Modifications in the Medial Prefrontal Cortex in Susceptibility and Resilience to Stress
Wang, M., Perova, Z., Arenkiel, B. R., & Li, B. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.5294-13.2014 · Cited by 116
“Viral injections were performed using previously described procedures (Li et al., 2011, 2013).”
MethodSelf-citationAugur, I. F., Wyckoff, A. R., Aston-Jones, G., Kalivas, P. W., & Peters, J. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.0773-16.2016 · Cited by 111
“CNO was administered at a dose of 10 mg/ml/kg (i.p.) based on reports indicating that this may be a minimal effective dose in some systems (Li et al., 2013; Chiarlone et al., 2014; Mahler et al., 2014).”
BackgroundDéjean, C., Courtin, J., Rozeske, R. R., Bonnet, M. C., Dousset, V., Michelet, T., & Herry, C. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.03.017 · Cited by 130
“Interestingly, about 65% of PKC-δ1 CEl neurons express the OR, suggesting that the oxytocinmediated suppression of fear is mediated by inhibition of PKC-δ1 CEl neurons, which, consequently, may disinhibit PAG-projecting CEm neurons (68–70).”
BackgroundInfluentialDorsal tegmental dopamine neurons gate associative learning of fear
Groessl, F., Munsch, T., Meis, S., Griessner, J., Kaczanowska, J., Pliota, P., Kargl, D., Badurek, S., Kraitsy, K., Rassoulpour, A., et al. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0174-5 · Cited by 118
Perova, Z., Delevich, K. M., & Li, B. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.2670-14.2015 · Cited by 117
Self-citationInception of a false memory by optogenetic manipulation of a hippocampal memory engram
Liu, X., Ramirez, S., & Tonegawa, S. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0142 · Cited by 124
The promise and perils of causal circuit manipulations
Wolff, S. B. E., & Ölveczky, B. P. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.01.004 · Cited by 121
De Bundel, D., Zussy, C., Espallergues, J., Gerfen, C. R., Girault, J.-A., & Valjent, E. (2016) · Molecular Psychiatry · doi:10.1038/mp.2015.210 · Cited by 112
“The CEA has a well-established role in the acquisition, consolidation and expression of fear responses towards auditory threat-predicting cues (CS+) (3, 42, 43) but was also found to be involved in generalization of fear responses towards non-predictive auditory cues (CS−) (3, 5).”
BackgroundMoscarello, J. M., & Penzo, M. A. (2022) · Nature Neuroscience · doi:10.1038/s41593-022-01130-5 · Cited by 112
Self-citationLiu, X., & Carter, A. G. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.0378-18.2018 · Cited by 117
“…including during repetitive activity with intact feedforward inhibition. their locations in specific subregions and layers of the PFC, these projection neurons can sample distinct synaptic inputs (Little and Carter, 2012; McGarry and Carter, 2016; Anastasiades et al., 2018; Collins et al., 2018).”
BackgroundZhou, M., Liu, Z., Melin, M. D., Ng, Y. H., Xu, W., & Südhof, T. C. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0248-4 · Cited by 112
Valence coding in amygdala circuits
Pignatelli, M., & Beyeler, A. (2018) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2018.10.010 · Cited by 133
“Consistent with this finding, activation of SOM+ neurons can decrease conditioned flight responses [41] but can also initiate passive freezing [41,42].”
BackgroundAmygdala-Midbrain Connections Modulate Appetitive and Aversive Learning
Steinberg, E. E., Gore, F., Heifets, B. D., Taylor, M. D., Norville, Z. C., Beier, K. T., Földy, C., Lerner, T. N., Luo, L., Deisseroth, K. A., et al. (2020) · Neuron · doi:10.1016/j.neuron.2020.03.016 · Cited by 120
“Sst proved to be the best genetic marker for CeA/ SNL neurons, and our results comport with studies demonstrating Sst+ neurons are necessary for fear conditioning (Li et al., 2013), promote passive defensive behaviors (Yu et al.”
ResultGrogans, S. E., Bliss‐Moreau, E., Buss, K. A., Clark, L. A., Fox, A. S., Keltner, D. J., Cowen, A., Kim, J. J., Kragel, P. A., MacLeod, C., et al. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105237 · Cited by 135
“…is insufficient, as research in rodents has identified subsets of neurons in threat-relevant regions, such as the amygdala, that have a distinct impact on the behavioral and physiological responses to threat (Fadok et al., 2017; Haubensak et al., 2010; Li et al., 2013; Viviani et al., 2011).”
BackgroundThe lateral parabrachial nucleus is actively involved in the acquisition of fear memory in mice
Satô, M., Ito, M., Nagase, M., Sugimura, Y. K., Takahashi, Y., Watabe, A. M., & Kato, F. (2015) · Molecular Brain · doi:10.1186/s13041-015-0108-z · Cited by 111
Translating Across Circuits and Genetics Toward Progress in Fear- and Anxiety-Related Disorders
Ressler, K. J. (2020) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2020.20010055 · Cited by 104
The Brain-Gut Axis in Health and Disease
Omran, Y. A., & Aziz, Q. (2014) · Advances in experimental medicine and biology · doi:10.1007/978-1-4939-0897-4_6 · Cited by 109
Cortico-Limbic Interactions Mediate Adaptive and Maladaptive Responses Relevant to Psychopathology
Kovner, R., Oler, J. A., & Kalin, N. H. (2019) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2019.19101064 · Cited by 111
Asok, A., Draper, A., Hoffman, A. F., Schulkin, J. A., Lupica, C. R., & Rosen, J. B. (2017) · Molecular Psychiatry · doi:10.1038/mp.2017.79 · Cited by 103
Asede, D., Bosch, D., Lüthi, A., Ferraguti, F., & Ehrlich, I. (2015) · Neuron · doi:10.1016/j.neuron.2015.03.008 · Cited by 109
Rodent models of impaired fear extinction
Singewald, N., & Holmes, A. (2018) · Psychopharmacology · doi:10.1007/s00213-018-5054-x · Cited by 110
Burghardt, N. S., & Bauer, E. P. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.05.050 · Cited by 109
An Insula–Central Amygdala Circuit for Guiding Tastant-Reinforced Choice Behavior
Schiff, H. C., Bouhuis, A. L., Yu, K., Penzo, M. A., Li, H., He, M., & Li, B. (2018) · The Journal of Neuroscience · doi:10.1523/jneurosci.1773-17.2017 · Cited by 100
“Briefly, the Som-cre; Rosa26-stopflox-tTA mice and the Prkcd-cre;Rosa26-stopflox-tTA mice, which express tetracycline transactivator (tTA) in SOM cells and PKC- cells, respectively, were injected into the CeL with the AAVTRE-hGFP-TVA-G (0.2– 0.3 l) that expresses the following components in a tTA-dependent manner: a f…”
MethodInfluentialSelf-citationA neural substrate of compulsive alcohol use
Domi, E., Xu, L. X., Toivainen, S., Nordeman, A., Gobbo, F., Vènniro, M., Shaham, Y., Messing, R. O., Visser, E., van den Oever, M. C., et al. (2021) · Science Advances · doi:10.1126/sciadv.abg9045 · Cited by 100
Benarroch, E. E. (2014) · Neurology · doi:10.1212/wnl.0000000000001171 · Cited by 103
Sleep Regulation by Neurotensinergic Neurons in a Thalamo-Amygdala Circuit
Ma, C., Zhong, P., Liu, D., Barger, Z., Zhou, L., Chang, W.-C., Kim, B., & Dan, Y. (2019) · Neuron · doi:10.1016/j.neuron.2019.05.015 · Cited by 97
“NTS Is a Marker for CeA Candidate Sleep Neurons The CeA is known to contain multiple subtypes of GABAergic neurons with distinct molecular markers, projection targets, and functional properties (Cai et al., 2014; Carter et al., 2013; Ciocchi et al., 2010; Douglass et al., 2017; Fadok et al., 2017; Haubensak et al., 20…”
BackgroundRetrieving fear memories, as time goes by…
Monte, F. H. D., Quirk, G. J., Li, B., & Penzo, M. A. (2016) · Molecular Psychiatry · doi:10.1038/mp.2016.78 · Cited by 98
Self-citationNew learning and unlearning: strangers or accomplices in threat memory attenuation?
Clem, R. L., & Schiller, D. (2016) · Trends in Neurosciences · doi:10.1016/j.tins.2016.03.003 · Cited by 90
Cerebellar modulation of synaptic input to freezing-related neurons in the periaqueductal gray
Vaaga, C. E., Brown, S. T., & Raman, I. M. (2020) · eLife · doi:10.7554/elife.54302 · Cited by 89
“These TH neurons may act either locally or via projections to regions such as the central amygdala and bed nucleus of the stria terminalis (Li et al., 2013; Matthews et al., 2016; Li et al., 2016; Groessl et al., 2018).”
BackgroundYamauchi, N., Sato, K., Sato, K., Murakawa, S., Hamasaki, Y., Nomura, H., Amano, T., & Minami, M. (2022) · Science Advances · doi:10.1126/sciadv.abj5586 · Cited by 90
Metadata
- Authors
- Li, H., Penzo, M. A., Taniguchi, H., Kopec, C. D., Huang, Z. J., & Li, B.
- Affiliations
- Cold Spring Harbor Laboratory (US)
- Princeton University (US)
- Corresponding author
- Li, Bo
- Venue
- Nature Neuroscience
- Published
- 2013-01-27
- Volume
- 16
- Issue
- 3
- Pages
- 332-339
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC3581751
- OpenAlex
- W2003870213
- Cited by
- 497
- References
- 49
- Citations by year
- 2026: 15 · 2025: 25 · 2024: 49 · 2023: 35 · 2022: 42 · 2021: 46 · 2020: 50 · 2019: 40 · 2018: 49 · 2017: 33 · 2016: 34 · 2015: 43 · 2014: 23 · 2013: 13
- FWCI
- 20.58
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Cold Spring Harbor Laboratory Institutional Repository (Cold Spring Harbor Laboratory) (acceptedVersion)
- Funders
- National Institute of Mental Health (U01MH078844, R01MH091903)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Keywords
- central amygdala, fear conditioning, fear memory, inhibitory interneurons, synaptic potentiation, experience-dependent plasticity, lateral amygdala, disinhibition, fear expression
- MeSH terms
- Amygdala, Animals, Conditioning, Psychological, Fear, Nerve Net, Neuronal Plasticity, Neurons, Somatostatin, Synapses, Mice
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