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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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BackgroundSelf-citationAmygdaloid and non-amygdaloid fear both influence avoidance of risky foraging in hungry rats
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BackgroundA model of amygdala function following plastic changes at specific synapses during extinction
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“It is well known that PKC-δ - and SOM-positive neurons constitute two major non-overlapping cell subtypes in the CeL (Li et al., 2013; Moscarello et al., 2022).”
Self-citationRyazantseva, M., Liiwand, M., Shteinikov, V., Kunnari, A.-J., Sulku, J., & Lauri, S. E. (2025) · Molecular Psychiatry · doi:10.1038/s41380-025-03093-y · Cited by 11
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“Many previous studies have used foot shocks for fear-conditioning acquisition and have investigated the functional roles of the CeA in the process (Haubensak et al., 2010; Li et al, 2013; Han et al., 2015; Tovote et al., 2015; Fadok et al., 2018).”
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“Indeed, there is evidence of increased activation of the CeA (Baker and Kim, 2004; Li et al., 2013) and rapid CRF translation during stress (Jurek et al., 2015), especially when the stressor is novel (Aguilera and Liu, 2012).”
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“The functional segregation of the central amygdala as a command module gained momentum when fear-on (CeLon) and fear-off (CeLoff) cell pools were identified to trigger or block, respectively, fear conditioning driven by the engagement of a local inhibitory microcircuit that gates CeM output to control the level of con…”
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“28 Subtypes of central amygdala neurons regulate specific behaviors through mutual inhibition.”
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“S6) revealed projections to multiple brain regions, including the CeA, basomedial amygdalar nucleus, parasubthalamic nucleus, posterior thalamic regions, and PAG—key areas in emotional regulation and learning ( 39 , 67 – 70 ).”
Inhibitory Fear Memory Engram in the Mouse Central Lateral Amygdala
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Ethanol Untangles the Amygdala‐Anxiety Circuit Through Tonic GABA Inhibition
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“The studies of Herman and colleagues (2013) noted that the majority of the CRF1+ were located in the CeM and restricted their studies to this region.”
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Studying Integrative Processing and Prospected Plasticity in Cholinergic Interneurons
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“…of the striatal DA circuits we inhibited, as fear learning and expression are usually attributed to circuits relevant for fast and timely behavioral responses such as freezing or escaping (Fadok et al., 2017; Li et al., 2013) which are less relevant for other innate behaviors such as grooming.”
Holford, T. W., Letourneau, K. N., Von-Walter, C., Moncaleano, D., Loomis, C. L., & Bolton, M. M. (2025) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2025.1597131 · Cited by 5
“Likewise, chemogenetic inhibition of PKC δ + neurons promotes freezing (Haubensak et al., 2010) whereas optogenetic activation of SOM+ induces freezing (Li et al., 2013).”
Jo, Y. S., Kong, M.-S., Sethi, E., Pyeon, G. H., & Zweifel, L. S. (2026) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2522768123 · Cited by 7
“Sst - expressing neurons are activated by fear - associated (42) as well as reward - associated cues (47), we find that dopamine increases to both CS Fear + and CS Rew + in the CeA suggesting that these signals may facilitate plasticity within the Sst neurons following conditioning.”
The central amygdala as a pathological hub: A multi-level review of pain–emotion comorbidity
Xu, X., Hu, J., Wang, Y., Zhu, Y., Cao, Y., Li, M., & Peng, P. (2026) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2026.111756 · Cited by 4
Divergent input patterns to the central lateral amygdala play a duet in fear memory formation
Gao, J.-H., Liu, Y.-Y., Xu, H.-X., Wu, K., Zhang, L., Peng, C., Peng, X., Cao, J., Hua, R., & Zhang, Y.-M. (2024) · iScience · doi:10.1016/j.isci.2024.110886 · Cited by 4
“9,10,27 In addition, CRF + GABA neurons are thought to promote flight responses during FC. 54,56 Furthermore, SOM + GABA neurons has been reported to form connections with other neuron subtypes in the CeL, engaging in the modulation of intra-CeL microcircuits, thereby participating in associative…”
InfluentialSelf Regulation of Memory Processing Centers of the Brain
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Valence and salience encoding in the central amygdalaPreprint
Kong, M.-S., Ancell, E., Witten, D., & Zweifel, L. S. (2024) · eLife · doi:10.7554/elife.101980 · Cited by 4
“…cells in the CeA encode conditioned and/or unconditioned fear stimulus information (Ciocchi et al., 2010; Duvarci et al., 2011; Fadok et al., 2017; Li et al., 2013; Sanford et al., 2017; Yang et al., 2023; Yu et al., 2017), as well as appetitive information (Douglass et al., 2017; Hardaway et…”
InfluentialGeneration and Characterization of a NovelPrkcd-Cre Rat Model
Toivainen, S., Petrella, M., Li, X., Visser, E., Weiss, T., Vellere, S., Zeier, Z. R., Wahlestedt, C., Barbier, E., Domi, E., et al. (2024) · Journal of Neuroscience · doi:10.1523/jneurosci.0528-24.2024 · Cited by 3
“…between sensory input nuclei of the amygdala and behavioral output centers in the brainstem (LeDoux, 2000), to one of an active node of information processing (Balleine and Killcross, 2006; Ciocchi et al., 2010; H. Li et al., 2013; Robinson et al., 2014; Janak and Tye, 2015; K. Yu et al., 2017).”
BackgroundTezanos, P., & Trejo, J. L. (2025) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2025.106145 · Cited by 3
“Yang et al. (2023) thoroughly described the role of somatostatin-positive (Sst + ) neurons in the central amygdala (CeA), previously characterized as "fear-on" neurons (Li et al., 2013), in encoding the aversive versus appetitive content of experience.”
Nisbett, K. E., & Koob, G. F. (2025) · eNeuro · doi:10.1523/eneuro.0059-25.2025 · Cited by 3
“The other population instead expresses somatostatin, which can be later fi ring or regular spiking (Li et al., 2013).”
Serotonin and the CNS - New Developments in Pharmacology and Therapeutics
Olivier, B. (2021) · IntechOpen eBooks · doi:10.5772/intechopen.90962 · Cited by 6
Dorofeikova, M., Stelly, C. E., Duong, A., Basavanhalli, S., Bean, E., Weissmuller, K., Sifnugel, N., Resendez, A., Corey, D. M., Tasker, J. G., et al. (2023) · eNeuro · doi:10.1523/eneuro.0319-22.2023 · Cited by 3
“Threatening cues activate CeA SOM1 neurons, and stimulating this population promotes freezing behavior (Li et al., 2013; Yu et al., 2016; Fadok et al., 2017).”
InfluentialCui, L.-L., Wang, X., Han, L., Luo, F., & Li, C. (2024) · Molecular Pain · doi:10.1177/17448069241226960 · Cited by 3
“CeLC contains two distinct subpopulations of GABAergic neurons that express somatostatin (SOM+) or protein kinase C δ (PKC δ +) 66 – 68 and they have distinct functions in pain modulation.”
BackgroundGreiner, E. M., & Petrovich, G. D. (2024) · Brain Structure and Function · doi:10.1007/s00429-024-02791-7 · Cited by 3
Koita, O., Lebowitz, J. J., & Williams, J. T. (2025) · eNeuro · doi:10.1523/eneuro.0249-24.2025 · Cited by 4
“For example, the PVT to central AM pathway drives conditioned freezing responses, whereas the PVT to NAc pathway signals active avoidance events (Choi et al., 2010; Oleson et al., 2012; Li et al., 2013; Bravo-Rivera et al., 2014; Penzo et al., 2015; Ramirez et al., 2015; Fadok et al., 2017).”
Саульская, Н. Б. (2018) · Успехи физиологических наук · doi:10.7868/s0301179818040021 · Cited by 3
Defining circuit-specific roles for G protein-coupled receptors in aversive learning
Gowrishankar, R., & Bruchas, M. R. (2019) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2019.01.002 · Cited by 3
Roles of the Serotoninergic System in Coping with Traumatic Stress
Vitalis, T., & Verney, C. (2021) · IntechOpen eBooks · doi:10.5772/intechopen.97221 · Cited by 4
“Following fear conditioning, SOM+ GABAergic projection neurons disinhibiting the medial part of the CE (CEM) allowed a range of defensive behaviour as freezing [105–107] and fear recall [108].”
BackgroundYang, L. C., Chen, M., & Zheng, P. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/133090 · Cited by 3
“PPR, measured as the ratio of EPSC amplitude in response to two successive stimulation pulses, reflects presynaptic release probability; a lower PPR correlates with higher release probability (Zucker and Regehr, 2002, Li et al., 2013).”
BackgroundMethodInfluentialPoli, A., Viglione, A., Mazziotti, R. M., Morea, S., Melani, R., Silingardi, D., Putignano, E., Berardi, N., & Pizzorusso, T. (2022) · Research Square · doi:10.21203/rs.3.rs-2089271/v1 · Cited by 3
A dopamine-dependent mechanism for reward-induced modification of fear memoriesPreprint
Kong, M.-S., Jo, Y. S., Sethi, E., Pyeon, G. H., & Zweifel, L. S. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.09.05.611495 · Cited by 3
“…of genetically distinct CeA neurons are activated (Fear-On) or inhibited (Fear-Off) by conditioned threat stimuli and contribute to associative fear learning ( 20, 21, 29-32 ), but how these neurons respond during generalized fear or the impact of dopamine on this encoding is not known.”
Baudon, A., Grelot, V., Althammer, F., Wang, K., Denis, C., Ali, S. A., Yan, Y., Díaz, F. C., Piacentini, F., Creusot, E. C., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.10.07.617014 · Cited by 3
“4e-f ), similarly to 30 .”
Motivation as Neural Context for Adaptive Learning and Memory Formation
Poh, J.-H., & Adcock, R. A. (2025) · Annual Review of Psychology · doi:10.1146/annurev-psych-032525-031744 · Cited by 4
Le, Q.-S. E., Lardant, E., Siddiqui, Y., Alam, T., Evans, K., & Fadok, J. P. (2026) · Journal of Neuroscience · doi:10.1523/jneurosci.1049-25.2026 · Cited by 2
Ontogeny of the Corticolimbic System and the Risk of Anxiety Disorders in Adolescence
Дыгало, Н. Н. (2022) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-022-01235-1 · Cited by 2
Associative Memory Cells in Memory Trace
Wang, J. (2019) · Springer eBooks · doi:10.1007/978-981-13-9501-7_5 · Cited by 2
Wright, K. M., Cieslewski, S., Chu, A., & McDannald, M. A. (2023) · Behavioral Neuroscience · doi:10.1037/bne0000568 · Cited by 2
Rajbhandari, A. K., Tribble, J. E., & Fanselow, M. S. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.21100-0 · Cited by 2
Delevich, K. M., Jaaro-Peled, H., Penzo, M. A., Sawa, A., & Li, B. (2016) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/054759 · Cited by 2
Self-citationPresence of a remote fear memory engram in the central amygdala.Preprint
Hammack, R. J., Fischer, V. E., Andrade, M. A., & Toney, G. M. (2023) · PubMed Central · doi:10.1101/lm.053833.123 · Cited by 2
“…including induction of synaptic plasticity among output projections that contribute to multiple fear learning-associated processes ranging from memory acquisition (Li et al. 2013; Penzo et al. 2014) to memoryexpression (Ciocchi et al. 2010; Kim et al. 2016) and extinction (Whittle et al. 2021).”
BackgroundInfluentialAshby, D. M., Dias, C., Aleksandrova, L. R., Lapish, C. C., Wang, Y. T., & Phillips, A. G. (2021) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyab011 · Cited by 2
Khormi, I. M., Fazlollahi, A., Al‐iedani, O., Vidyasagar, R., Ayton, S., Alshehri, A., Paton, B. K., Ramadan, S. A., & Lechner‐Scott, J. (2024) · The Neuroradiology Journal · doi:10.1177/19714009241303123 · Cited by 2
Tohyama, S., Nagashima, T., Higashino, I., Arima‐Yoshida, F., Hiyoshi, K., Nagase, M., Yada, Y., Naoki, H., & Watabe, A. M. (2025) · Communications Biology · doi:10.1038/s42003-025-08367-3 · Cited by 1
“Moreover, SOM + and SOM − neurons show distinct modi fi cations in a US experience-dependent manner 68 , and repeated US experience enhances CeC/L SOM + responses 69 .”
A posterior hypothalamic to midbrain circuit orchestrating nociceptive behaviours in male mice
Ma, Y., Liu, H., Zhao, W.-N., Li, Q., Gao, P., Han, X., Chaudhury, D., Wang, F., Liu, H., Yu, W., et al. (2025) · British Journal of Pharmacology · doi:10.1111/bph.70227 · Cited by 1
“2.9 | Slice preparation for electrophysiology release probability, while a lower PPR correlates with a higher release probability (Li et al., 2013).”
InfluentialThe central amygdala gates exogenous glucagon-like peptide 1 signals
Duran, M., Zeng, N., Cutts, E. J., POLAMARASETTY, A., Rodríguez, M., Habegger, K. M., & Hardaway, J. A. (2026) · Molecular Metabolism · doi:10.1016/j.molmet.2026.102403 · Cited by 2
“In support of this notion, Prkcd CeA and Sst CeA neurons inhibit one another to regulate fear learning [78].”
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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