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Genetic dissection of an amygdala microcircuit that gates conditioned fear
Open accessAbstract
The role of different amygdala nuclei (neuroanatomical subdivisions) in processing Pavlovian conditioned fear has been studied extensively, but the function of the heterogeneous neuronal subtypes within these nuclei remains poorly understood. Here we use molecular genetic approaches to map the functional connectivity of a subpopulation of GABA-containing neurons, located in the lateral subdivision of the central amygdala (CEl), which express protein kinase C-δ (PKC-δ). Channelrhodopsin-2-assisted circuit mapping in amygdala slices and cell-specific viral tracing indicate that PKC-δ(+) neurons inhibit output neurons in the medial central amygdala (CEm), and also make reciprocal inhibitory synapses with PKC-δ(-) neurons in CEl. Electrical silencing of PKC-δ(+) neurons in vivo suggests that they correspond to physiologically identified units that are inhibited by the conditioned stimulus, called CEl(off) units. This correspondence, together with behavioural data, defines an inhibitory microcircuit in CEl that gates CEm output to control the level of conditioned freezing.
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“The amygdala plays a key role in defensive behaviour and switching between defensive modes in rodents [39–42].”
From Freeze for action: neurobiological mechanisms in animal and human freezing (2017) · cites this paper as [42]
Experimental — accuracy not yet measuredIn the citing paper
“since BLA neurons excite GABAergic CeL neurons26 that provide feed-forward inhibition onto CeM “output” neurons6,18,19”
From Amygdala circuitry mediating reversible and bidirectional control of anxiety (2011) · cites this paper as [19]
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“For instance, a population of GABAergic neurons in the CeL which express protein kinase C-delta (PKC-delta+ neurons) increase their spontaneous activity following fear conditioning [34], and are involved in fear generalization and anxiety (Fig. 1D) [4].”
From An emerging circuit pharmacology of GABAA receptors (2018) · cites this paper as [34]
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“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.”
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Parrilla-Carrero, J., Kaigler, K. F., Hartshorn, G. H., Fadel, J. R., & Wilson, M. A. (2019) · Neurobiology of Stress · doi:10.1016/j.ynstr.2019.100197 · Cited by 9
“The CeA is comprised of several neurochemically-distinct cell populations, which are differentially responsive to both stress and MOR activation (Day et al., 1999; Zhu and Pan, 2005; Haubensak et al., 2010; Poulin et al., 2013a).”
Natural Products Altering GABAergic Transmission
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Stress peptides sensitize fear circuitry to promote passive coping
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“Theoretically, PKC δ neurons are a subset of GABAergic neurons in the CeC/CeL, 48,49 and nociTRAPed neurons are a subset of PKC δ neurons, as discussed earlier.”
Inhibitory Fear Memory Engram in the Mouse Central Lateral Amygdala
Hou, W., Jariwala, M., Wang, K., Seewald, A., Lin, Y. Q., Liou, Y.-C., Ricci, A., Ferraguti, F., Lien, C., & Capogna, M. (2022) · Cell Reports · doi:10.1016/j.celrep.2024.114468 · Cited by 8
Afferent Projections to the Calca /CGRP‐Expressing Parabrachial Neurons in Mice
Korkutata, M., Luca, R. D., Fitzgerald, B., Khanday, M. A., Arrigoni, E., & Scammell, T. E. (2025) · The Journal of Comparative Neurology · doi:10.1002/cne.70018 · Cited by 6
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A Role for Neuropeptide S in Alcohol and Cocaine Seeking
Cannella, N., Borruto, A. M., Petrella, M., Bonaventura, M. V. M. D., Soverchia, L., Cifani, C., Carlo, S. D., Domi, E., & Ubaldi, M. (2022) · Pharmaceuticals · doi:10.3390/ph15070800 · Cited by 7
“Similarly, a GABAergic neuronal ensemble in the CeA, identified as protein kinase C δ (PKCδ + neurons) GABAergic positive neurons, was found to be crucial in driving compulsive drinking in a subset of rats and regulating the fear response through their brainstem projections [26,27].”
BackgroundHerry, C., & Jercog, D. (2022) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2022.102600 · Cited by 8
HE, F., & Ai, H. ‐. (2016) · Physiological Research · doi:10.33549/physiolres.933125 · Cited by 8
Gilman, T. L., Dutta, S., Adkins, J. M., Cecil, C. A., & Jasnow, A. M. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.09.010 · Cited by 7
“For example, activation of CeL neurons classified as PKCδ-expressing (Haubensak et al., 2010) or oxytocin receptor-expressing (Knobloch et al.”
Dehghani, N. (2018) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2018.00081 · Cited by 10
“, 2009) or fear-conditioning (Haubensak et al., 2010), as well as targeting deep structures (brainstem) (Lin et al.”
BackgroundPavlovian Fear Conditioning Function, Cause, and Treatment
Fanselow, M. S., & Sterlace, S. R. (2014) · eScholarship (California Digital Library) · Cited by 7
Self-citationSeewald, A., Schönherr, S., Hörtnagl, H., Ehrlich, I., Schmuckermair, C., & Ferraguti, F. (2021) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2021.634558 · Cited by 7
How Brain Arousal Mechanisms Work: Paths Toward Consciousness
Pfaff, D. W. (2018) · Cited by 9
Curbing Fear by Axonal Oxytocin Release in the Amygdala
Tovote, P., & Lüthi, A. (2012) · Neuron · doi:10.1016/j.neuron.2012.01.016 · Cited by 7
“…targeting and interfering with selected circuit elements to not only characterize anatomy and connectivity, but also to investigate their specific function (Haubensak et al., 2010; Letzkus et al., 2011) and thus to dissect neuronal circuitry underlying complex behavior with unprecedented precision.”
BackgroundSelf-citationLei, S., & Hu, B. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108714 · Cited by 5
Shelkar, G. P., Gakare, S. G., Narasimhan, K. K. S., Chettiar, P. B., Asati, D. G., Thakur, S. S., & Dravid, S. M. (2025) · Scientific Reports · doi:10.1038/s41598-025-06073-y · Cited by 9
“CeA neurons are entirely GABAergic, with PKCδ and SOM being the two major inhibitory neurons in the CeA characterized by different firing patterns 18,50,51 .”
A cholinergic spinal pathway for the adaptive control of breathing
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Recent Developments in Optical Neuromodulation Technologies
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Neurotechnologies, Ethics, and the Limits of Free Will
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“This is achieved by genetically modifying the neuron cells that are involved in the circuits by adding photosensitive features to it (Haubensak et al., 2010; Jasnow et al., 2013; Johansen et al., 2010).”
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Yummy or yucky? Ask your central amygdala
Livneh, Y., & Andermann, M. L. (2017) · Nature Neuroscience · doi:10.1038/nn.4639 · Cited by 6
A Data Structure for Real-Time Aggregation Queries of Big Brain Networks
Ganglberger, F., Kaczanowska, J., Haubensak, W. E., & Bühler, K. (2019) · Neuroinformatics · doi:10.1007/s12021-019-09428-9 · Cited by 6
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Experience-dependent changes in affective valence of taste in male mice
Hamada, S., Mikami, K., Ueda, S., Nagase, M., Nagashima, T., Yamamoto, M., Bito, H., Takemoto‐Kimura, S., Ohtsuka, T., & Watabe, A. M. (2023) · Molecular Brain · doi:10.1186/s13041-023-01017-x · Cited by 6
“inhibitory neurons and form reciprocally connected microcircuits in the CeA [39, 40], one possible underlying mechanism is that Sst- and Prkcd-positive neurons are plastically regulated in a different manner via mutual inhibition, resulting in opposite plastic changes.”
BackgroundOn and Off switches in the brain
Moustafa, A. A. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00114 · Cited by 7
Cell types in the mouse amygdala and their transcriptional response to fear conditioningPreprint
Hochgerner, H., Tibi, M., Netser, S., Ophir, O., Reinhardt, N., Singh, S., Lin, Z.-H., Wagner, S., & Zeisel, A. (2022) · bioRxiv · doi:10.1101/2022.10.25.513733 · Cited by 2
Neuronal physiology of amygdala neurons in the context of injury and pain
Paul, B. K., Nunez-Ordaz, M. I., Samuel, J. R., & Kolber, B. J. (2025) · Neurobiology of Pain · doi:10.1016/j.ynpai.2025.100190 · Cited by 6
“…of the CeA, there are three major distinct classes of neuronal populations as defined by spiking patterns in adult male rats and mice – 1) Early spiking (ES) cells, 2) late spiking (LS) cells and 3) low-threshold bursting neurons (Chieng et al. 2006; Haubensak et al. 2010; Adke et al. 2021).”
Bohnsack, J. P., Zhang, H., & Pandey, S. C. (2024) · Translational Psychiatry · doi:10.1038/s41398-024-02906-y · Cited by 5
“Up regulation of EZH2 expression on PKC-δ positive GABAergic neurons after adolescent alcohol exposure in adulthood The CeA contains two major nuclei referred to as medial (CeM) and lateral (CeL) CeA which have been shown to interact in emotional processing, such as fear and anxiety [22, 59, 60].”
BackgroundCentral amygdala NPBWR1 neurons facilitate social novelty seeking and new social interactions
Soya, S., Toda, K., Sakurai, K., Chérasse, Y., Saito, Y. C., Abe, M., Sakimura, K., & Sakurai, T. (2025) · Science Advances · doi:10.1126/sciadv.adn1335 · Cited by 6
“The expression of Pkc δ and Som suggests that CeA Npbwr1 neurons could function as a part of the mutual disinhibitory circuit in the CeA, regulating fear behavior ( 14 , 15 ).”
Protein Kinase C promotes peroxisome biogenesis and peroxisome–endoplasmic reticulum interaction
Borisyuk, A., Howman, C. M., Pattabiraman, S., Kaganovich, D., & Amen, T. (2025) · The Journal of Cell Biology · doi:10.1083/jcb.202505040 · Cited by 8
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Light-Controlled Modulation and Analysis of Neuronal Functions
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“It has become possible to control the behaviour of organisms [13,14], as well as to explore new ways of treating certain diseases [15–17].”
BackgroundCentral Amygdala Neuroplasticity in Alcohol Dependence
Roberto, M., & Gilpin, N. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-405941-2.00011-0 · Cited by 9
Auditory Fear Circuits in the Amygdala – Insights from Computational Models
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“The output nucleus Ce also has distinct sub-circuits with different functions in fear learning (Coicci et al., 2010; Haubensak et al., 2010).”
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“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
“Off neurons (inhibited by CS Fear +) (41), and we find significantly fewer CeA inhibited cells following Th mutagenesis in the VTA, suggesting that dopamine acting on D2 receptors may be a key mediator of these observed inhibitions.”
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
Morphological heterogeneity of neurons in the human central amygdaloid nucleus
Vásquez, C. E., Guerra, K. T. K., Renner, J., & Rasia‐Filho, A. A. (2024) · Journal of Neuroscience Research · doi:10.1002/jnr.25319 · Cited by 7
“…no current data for the human CeA wiring at a fine-grained cellular level as described in other animals (for data in rodents, see Cassell et al., 1999; Schiess et al., 1999; Ciocchi et al., 2010; Haubensak et al., 2010; Janak & Tye, 2015; Beyeler & Dabrowska, 2020; Hájos, 2021; Wang et al., 2023).”
BackgroundDivergent 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
“10,55,69 SOM + neurons in the CeL, acted as fear-on neurons, are partially co-labeled with CeL Calcrl + neurons as well.”
Fanselow, M. S., Zelikowsky, M., Perusini, J. N., Barrera, V. R., & Hersman, S. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.10.021 · Cited by 4
“Fear conditioning again holds promise because the underlying circuitry has been fairly well characterized (Fendt & Fanselow, 1999; Haubensak et al., 2010; Paré, Quirk, & LeDoux, 2004).”
Self-citationSelf Regulation of Memory Processing Centers of the Brain
Mizumori, S. J. Y. (2015) · Springer eBooks · doi:10.1007/978-3-319-15759-7_9 · Cited by 5
Phenotyping neurons activated in the mouse brain during restoration of salt debt
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Cell-type Specific Optogenetic Mice for Dissecting Neural Circuitry Function
Zhao, S., Ting, J. T., Atallah, H., Qiu, L., Tan, J., Gloss, B. R., Augustine, G. J., Deisseroth, K. A., Luo, M., Graybiel, A. M., et al. (2011) · PubMed Central · Cited by 4
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“BEHAVIORAL NEUROSCIENCE ORIGINAL RESEARCH ARTICLE published: 30 September 2014 doi: 10.3389/fnbeh.2014.00324 Fear memory formation can affect a different memory: fear conditioning affects the extinction, but not retrieval, of conditioned taste aversion (CTA) memory”
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The Brain, Explained: A Comprehensive Theory of Brain FunctionPreprint
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The parabrachial to central amygdala circuit is a key mediator of injury-induced pain sensitizationPreprint
Torres-Rodriguez, J. M., Wilson, T. D., Singh, S., Chaudhry, S., Adke, A. P., Becker, J. J., Lin, J. J., González, S. M., Soler‐Cedeño, O., & Carrasquillo, Y. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.02.08.527340 · Cited by 4
“Consistent with previous reports, firing phenotypes 115 in PKCδ+ and Som+ CeA neurons were heterogeneous (33-35) (Figure 1D).”
ResultValence 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
“…cell types that contribute to both appetitive and aversive processes (Cai et al., 2014; Douglass et al., 2017; Fadok et al., 2018; Hardaway et al., 2019; Haubensak et al., 2010; Isosaka et al., 2015; Kim et al., 2017; Li et al., 2013; McCullough et al., 2018; Warlow et al., 2020; Yu et al., 2017).”
Generation 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
“However, CeA PKC δ + neurons also synapse onto PAG-projecting CeM neurons and control their activity (Haubensak et al., 2010), and it is therefore likely that modulation of vlPAG neuronal function from CeA PKC δ + is primarily mediated by a multisynaptic mechanism.”
BackgroundResultInfluentialNisbett, K. E., & Koob, G. F. (2025) · eNeuro · doi:10.1523/eneuro.0059-25.2025 · Cited by 3
“For example, Haubensak et al. showed that 65% of CeL OFF neurons express oxytocin receptors (Haubensak et al., 2010), and we found that a majority (94.0 ± 0.9”
InfluentialDorofeikova, 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
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“73,74 One study found that activation of ERK in CeA mostly occurred in PKC δ + neurons after formalin injection.”
BackgroundWang, X., Zhang, H., Zhou, W. P., Li, X., Ibáñez, C. F., & Xie, M. (2025) · BMC Biology · doi:10.1186/s12915-025-02230-x · Cited by 3
“These GABAergic neurons have been reported to suppress food intake [27] and reduce conditioned fear [28], which may account for the tendency to reduced body weight in animals fed with inulin-rich diet, as well as the enrichment in the sub-population of metabolism-related astrocytes in the same…”
Central amygdalar PKCδ neurons mediate fentanyl withdrawal
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Bed Nucleus of Stria Terminalis (BNST) circuits
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The Neurobehavioral State hypothesis
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Self-citationCocaine-Induced Changes in Low-Dimensional Attractors of Local Field Potentials in Optogenetic Mice
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“, 2013; Chen and Knight, 2016), fear conditioning (Haubensak et al., 2010; Do Monte et al., 2016), and aggression (Lin et al.”
BackgroundMethodGABA A receptors and inhibitory neurotransmission in the amygdalar complex
Perumal, M. B., Lynch, J. W., & Sah, P. (2018) · Current Opinion in Physiology · doi:10.1016/j.cophys.2018.01.003 · Cited by 3
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“In behavioral studies, optogentics proved invaluable in studying feeding [57–60], fear conditioning [61, 62], and Dopamine receptor antagonists effects on neural activity”
BackgroundLa inversión socialmente responsable
Izquierdo, M. Á. F., & Torres, M. J. M. (2009) · LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) · Cited by 3
Nodal Structures in Anxiety-Like and Panic-Like Responses
Maximino, C. (2012) · SpringerBriefs in neuroscience · doi:10.1007/978-1-4614-4048-2_3 · Cited by 3
Neuropeptide Y and amygdala circuitry: Modulation of stress-related behavior
Urban, J. H. (2020) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-815134-1.00007-6 · Cited by 3
Central amygdala CRF pathways in alcohol dependencePreprint
de Guglielmo, G., Kallupi, M., Pomrenze, M. B., Crawford, E. F., Simpson, S., Schweitzer, P., Koob, G. F., Messing, R. O., & George, O. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/134759 · Cited by 3
“In six neurons that showed fluorescence that were held at -52.9 ± 0.4 mV, activation of a green laser (532 nm) using a 6.5 s train at 15 Hz (Haubensak et al , 2010) elicited hyperpolarization of 6.5 ± 1.0 mV, concomitantly suppressing the firing of action potentials (Fig.”
MethodInfluentialMedrihan, L., Knudsen, M. G., Ferraro, T., Vasques, P. D. C., Romin, Y., Fujisawa, S., Greengard, P., & Milosevic, A. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.04.20.488950 · Cited by 3
“Therefore, while this study used the approach in experimental design and rigorous analysis of virally labeled projection neurons, previously design by others 21, 22, 42 , these circuitries will need further confirmation by other methods, such as electrophysiology.”
BackgroundMethodIntra-amygdala circuits of sleep disruption-induced anxiety in female micePreprint
Peng, B., Foilb, A. R., Manasian, Y., Li, Y., Deng, X., Meloni, E. G., Ressler, K. J., Carlezon, W. A., & Bolshakov, V. Y. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.05.19.594863 · Cited by 2
“Notably, the CeL contains two distinct subpopulations of GABAergic neurons, termed CeL on /PKC-d - (fear-on) and CeL off /PKC-d + (fear-off) neurons (Ciocchi et al., 2010; Haubensak et al., 2010), with CRF positive cells constituting a fraction of PKC-d - cells.”
BackgroundA 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
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
Protect and harm: Effects of stress on the amygdala
(2020) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-815134-1.00011-8 · Cited by 2
Velica, A., & Kullander, K. (2024) · BMC Neuroscience · doi:10.1186/s12868-024-00848-1 · Cited by 2
Ueda, S., & Takemoto‐Kimura, S. (2024) · Folia Pharmacologica Japonica · doi:10.1254/fpj.23052 · Cited by 2
Sex Differences in Neural Circuits Underlying Fear Processing
Romero, L. R., Acharya, N., Nabás, J. F., Marin‐Blasco, I., & Andero, R. (2024) · Current topics in behavioral neurosciences · doi:10.1007/7854_2024_543 · Cited by 2
Tong, S., Chen, Y., Wu, Z., Wang, L., Wei, Y., Wang, X., & Wu, Y. (2025) · PLoS ONE · doi:10.1371/journal.pone.0323203 · Cited by 2
Mechanisms of alcohol influence on fear conditioning: A computational model
Lonnberg, A., Logrip, M. L., & Kuznetsov, A. S. (2025) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.70071 · Cited by 4
“We use a current-frequency relationship for CeA neurons (Haubensak et al., 2010 ) to calibrate the neural response function FIGURE 2 Design of the simulated trial structure.”
Hernández, V. S., Segura‐Chama, P., & Zhang, L. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms262311405 · Cited by 1
Oxytocin promotes socially triggered cataplexy
Mahoney, C. E., Luca, R. D., Joyal, A. A., Woods, C., Zhao, W., Coffey, A. A., Kurimoto, E., Kroeger, D., Zhu, L., Fenselau, H., et al. (2026) · Nature Neuroscience · doi:10.1038/s41593-026-02352-7 · Cited by 3
“CeA OTR neurons make up about 65% of the broader population of CeA neurons expressing protein kinase C-δ 48 , a cell group known to reduce freezing behavior in response to oxytocin signaling 11,47 .”
Connectivity and Circuit Architecture Using Transsynaptic Tracing in Vertebrates
Miyamichi, K., & Schwarz, L. A. (2017) · Springer eBooks · doi:10.1007/978-3-319-57363-2_4 · Cited by 2
Albaugh, D. L., & Stuber, G. D. (2012) · Springer eBooks · doi:10.1007/978-3-642-30991-5_22 · Cited by 2
Multi-scale Neural Circuit Analysis with Rabies Viral Vectors
Kamaguchi, R., & Osakada, F. (2023) · The Brain & Neural Networks · doi:10.3902/jnns.30.56 · 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
Self-citationPhotochromic Modulation of Cys-loop Ligand-gated Ion Channels
Bregestovski, P. D., & Ponomareva, D. (2021) · Journal of Evolutionary Biochemistry and Physiology · doi:10.1134/s0022093021020162 · Cited by 2
“tive oxygen species [23, 24], as well as to control the behavior of organisms [25, 26].”
BackgroundAsymmetric representation of aversive prediction errors in Pavlovian threat conditioningPreprint
Ojala, K. E., Tzovara, A., Poser, B. A., Lutti, A., & Bach, D. R. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.07.10.197665 · Cited by 2
Central extended amygdala neurons in the development of activity-based anorexiaPreprint
Schnapp, W. I., Kim, J., Wang, Y., Timilsena, S., Fang, C., & Cai, H. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.11.10.515977 · Cited by 2
Self-citationAcute and chronic alcohol modulation of extended amygdala calcium dynamicsPreprint
Roland, A. V., Chao, T.-H. H., Hon, O. J., Machinski, S. N., Sides, T. R., Lee, S. I., Shih, Y. I., & Kash, T. L. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.10.10.561741 · Cited by 2
“PKCδ neurons, which are active in BNST during approach behavior in anxiogenic contexts (45,46) and play a role in fear behavior in CeA (47).”
Zhang, L., Hernández, V. S., Giraldo‐Gómez, D. M., Jiang, S. Z., León‐Contreras, J. C., Ye, R., Zhang, S., Schäfer, M., Barrio, R. A., Hernández‐Pando, R., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.04.03.647119 · Cited by 2
Ashby, 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
“Consideration should also be given to a subpopulation of PKC+ GABAergic cells within the lateral region of the CeA as a possible target of these inputs, as these neurons cease to display action potentials during acquisition of conditioned fear (Haubensak et al., 2010).”
BackgroundChronic inflammatory pain and chronic THC vapor inhalation alter midbrain neuronal activity
Kelley, L. K., Gilpin, N. W., & Middleton, J. W. (2025) · Journal of Neurophysiology · doi:10.1152/jn.00456.2024 · Cited by 1
Second-order threat conditioning in the amygdala-posterior piriform cortex network
Sepahvand, T., Qin, T., Hasan, Z., Power, K. D., Carew, S. J., Nazari, N., Janes, A. M., Salman, A., Xia, Y., Benoukraf, T., et al. (2025) · Communications Biology · doi:10.1038/s42003-025-08287-2 · Cited by 1
“We thank the reviewer for their strong support of our work.”
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
Yi, X., Zhang, Y., Yu, T.-Z., Yang, X., He, P., Li, H.-L., & Li, W.-G. (2026) · Molecular Psychiatry · doi:10.1038/s41380-026-03458-x · Cited by 1
“…basolateral amygdala; BLA) interact bidirectionally with medial prefrontal cortex (mPFC; prelimbic [PL] and infralimbic [IL]) and ventral hippocampus (vHPC) to integrate cue-context information, while the central amygdala (CeA) organizes downstream autonomic and motor output [36, 38 – 40].”
Identification of somatostatin + inhibitory engrams for extinction in the basolateral amygdala
Zhang, X., Lan, Z., Huang, Y. X., Yuting, L. I., Wang, Z., Sun, J., Zhou, Y., Bao, H., Fan, X., Yang, J., et al. (2026) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2511528123 · Cited by 3
Endocannabinoid modulation of a reciprocal fronto-coerulear connection in contextual discrimination
Locarno, A., Nava, L., Barsotti, N., Caltabiano, A., Misevičiūtė, I., Pelloux, Y., Boi, F., Vincenzi, M., Ribeiro, J. F., Angotzi, G. N., et al. (2026) · Cell Reports · doi:10.1016/j.celrep.2026.117141 · Cited by 1
Metadata
- Authors
- Haubensak, W., Kunwar, P. S., Cai, H., Ciocchi, S., Wall, N. R., Ponnusamy, R., Biag, J., Dong, H.-W., Deisseroth, K., Callaway, E. M., Fanselow, M. S., Lüthi, A., & Anderson, D. J.
- Affiliations
- California Institute of Technology (US)
- Salk Institute for Biological Studies (US)
- University of California, Los Angeles (US)
- Stanford University (US)
- Friedrich Miescher Institute (CH)
- Corresponding author
- Anderson, David J.
- ORCID
- Venue
- Nature
- Published
- 2010-11
- Volume
- 468
- Issue
- 7321
- Pages
- 270-276
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC3597095
- OpenAlex
- W1981044491
- Cited by
- 840
- References
- 55
- Citations by year
- 2026: 24 · 2025: 35 · 2024: 50 · 2023: 45 · 2022: 64 · 2021: 62 · 2020: 50 · 2019: 55 · 2018: 84 · 2017: 51 · 2016: 50 · 2015: 68 · 2014: 50 · 2013: 58 · 2012: 46
- FWCI
- 29.09
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institute of Mental Health (R01MH063912, R01MH085082)
- National Institute of Neurological Disorders and Stroke (RC2NS069464)
- 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, protein kinase C delta, GABAergic neurons, inhibitory microcircuits, disinhibition, conditioned freezing, fear memory, neuronal cell types
- MeSH terms
- Amygdala, Animals, Axonal Transport, Cells, Cultured, Conditioning, Classical, Fear, Female, gamma-Aminobutyric Acid, Genetic Techniques, Humans, Male, Mice, Transgenic, Neural Inhibition, Neural Pathways, Neurons, Synapses, Freezing Reaction, Cataleptic, Mice, Protein Kinase C-delta
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