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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]
In the citing paper
“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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“The CEl contains two functionally distinct subpopulations of neurons, which are excited (CElon) and inhibited (CEloff) upon presentation of fear-conditioned stimuli and which are largely overlapping with the genetically defined PKC -positive and -negative neuronal subtypes (Ciocchi et al. 2010; Haubensak et al. 2010).”
BackgroundInfluentialDissociation of Appetitive Overexpectation and Extinction in the Infralimbic Cortex
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“…(Pape and Pare, 2010), following two pathways: the first through BA units (Stefanacci et al., 1992; Pitkänen et al., 1995; Savander et al., 1997), and the second through two types of interneurons in CeL, called CeL-ON and CeL-OFF (Ciocchi et al., 2010; Haubensak et al., 2010; Li et al., 2013).”
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“Recent research has defined the detailed inhibitory microcircuits for the fear conditioning through combined use of in vivo eletrophysiological, optogenetic and pharmacological approaches (Ciocchi et al., 2010; Haubensak et al., 2010).”
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“, 2014), and inspected an AAV tracing case targeting the BNSTov (a part of alBNST) with a Cre-dependent, EGFP-expressing AAV in a PKC-δ-Cre mouse (Haubensak et al., 2010).”
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“Once released therein, OT acts on OTR expressed in the lateral subdivision of CeA (CeL) [20, 21], where it increases the activity of ‘fear off’ cells that send inhibitory projections to fear-promoting neurons located in the medial division of the CeA (CeM) [19, 20, 22].”
BackgroundHighly unstable heterogeneous representations in VIP interneurons of the anterior cingulate cortex
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“This AAV contained genes to express EGFP, the avian sarcoma/leukosis virus subtype A receptor (TVA, which confers infection capability to rabies virus pseudotyped with the avian sarcoma leucosis virus glycoprotein (EnvA)), and the rabies virus glycoprotein (G or Glyco) [47, 48] (which is necessary for trans-synaptic t…”
BackgroundInfluentialControl of Behavioral Arousal and Defense by a Glutamatergic Midbrain-Amygdala Pathway in Mice
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“Although CeA circuits consist of complex inhibitory and disinhibitory loops (Ciocchi and others 2010; Haubensak and others 2010), these findings indicate that information about an auditory stimulus, arriving from thalamic and cortical sources, can gain access to the CeA by way of plastic changes at…”
BackgroundLay, B. P. P., Koya, E., Hope, B. T., Esber, G. R., & Iordanova, M. D. (2022) · Biological Psychiatry · doi:10.1016/j.biopsych.2022.07.021 · Cited by 16
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“The CeA is a very heterogeneous structure with a rich diversity of cell types and complex circuitry (Ciocchi et al., 2010; Haubensak et al., 2010; Ahrens et al., 2018; McCullough et al., 2018), and the PACAP neurocircuit mechanisms in the CeA are so far not well understood.”
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Molecular diversity and functional dynamics in the central amygdala
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“We thus examined juvenile mice (P14) where BNSTov neurons can be identified by the expression of protein kinase C delta (Pkcd, Figure 5c–g; Bodnar, 2013; Cai et al., 2014; Haubensak et al., 2010).”
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“These type A and type B intrinsic phenotypes have been described previously in the CeL (Amano et al., 2012; Haubensak et al., 2010; Li and Sheets, 2018) including within CeL Sst populations (Hunt et al.”
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“The majority of CeAl neurons are GABAergic cells (Ehrlich et al. 2009; Haubensak et al. 2010), which could contribute to an enhanced ambient GABA concentration.”
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De novo designed voltage-gated anion channels suppress neuron firing
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“This hypothesized pattern of activity is consistent with recent work characterizing CeA circuits in freezing expression (Haubensak et al., 2010; Duvarci et al., 2011), although its role in directing other types of behaviors is unknown.”
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“The central lateral amygdala has long been known as a key region of fear processing [48] and fear memory [49], and has recently been shown to play an important role in nociceptive modulation [50,51].”
BackgroundPrefrontal circuits encode both general danger and specific threat representations
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“These behavioral approaches have been complemented by recording techniques to probe neuronal activity during defensive behaviors 3,4,6–10 Consistently with previous studies 11 , mice also displayed stereotyped behaviors during error trials with an initial decrease in speed behavior independent of…”
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“…via direct projections to the medial subnucleus of the CeA (CeAm) as well through an indirect pathway that leads to negative feedback for the medial subdivision of the CeA via activation of GABAergic neurons in the lateral subdivision of the CeA (CeAl) (Haubensak et al., 2010; Tye et al., 2011).”
A model of amygdala function following plastic changes at specific synapses during extinction
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“Finally, LA neurons project to inhibitory neurons in the lateral central nucleus (CEL), namely CELon neurons characterized by PKCδ (lacking PKCδ) which in turn inhibit CELoff neurons characterized by PKCδ (cells possessing PKCδ and lack somatostatin expression (Ciocchi et al., 2010; Haubensak et al., 2010; Li et al.,…”
Behavioural effects of extracellular matrix protein Fras1 depletion in the mouse
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“…animals or pharmacological or optogenetic means, perturbed structure and/or function of amygdala correlates with disrupted fear conditioning memory (Haubensak et al., 2010; Johansen, Wolff, Luthi, & LeDoux, 2012; Ko, Zhao, Toyoda, Qiu, & Zhuo, 2005; Martel, Hevi, Friebely, Baybutt, &…”
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“G ), consistent with previous findings (49).”
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“Then the defensive responses such as freezing are elicited by the CS [2,4,5].”
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“, fear (LeDoux, 2000; Haubensak et al., 2010; Tovote et al., 2015) and reward-related states (Everitt et al.”
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Neural circuits regulation of satiation
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“Interestingly, unlike VSNs and the neurons in NTS and LPB, almost all neurons in the CEA are GABAergic inhibitory neurons (Haubensak et al., 2010; Sun et al., 1993), making it difficult to identify the brain regions downstream of CEA for satiation.”
BackgroundSelf-citationCentral amygdala‐to‐pre‐Bötzinger complex neurotransmission is direct and inhibitory
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“Neurons expressing PKC δ have been shown to play specific roles in the network associated with fear and threat learning, appetite suppression, anxiety and nociceptive signalling (Botta et al., 2015; Cai et al., 2014; Ciocchi et al., 2010; Haubensak et al., 2010;Wilson et al., 2019).”
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Astrocyte-mediated central amygdala microcircuit gates comorbid anxiety symptoms in chronic pain
Zan, G., Yao, S.-Y., Deng, Y.-Z., Jiang, Y., Ye, R.-F., Chen, Y., Long, J.-D., Cheng, Y.-J., Chai, J., Xu, C., et al. (2025) · Neuron · doi:10.1016/j.neuron.2025.09.004 · Cited by 12
Tsukioka, K., Yamanaka, K., & Waki, H. (2022) · Neuroscience · doi:10.1016/j.neuroscience.2022.06.005 · Cited by 10
“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).”
General anesthesia activates a central anxiolytic center in the BNST
Lu, D., Lavergne, C. G. U., Choi, S., Park, J. H., Kim, J., Zhao, S., Desimone, Q., Lendaro, E., Chen, B., Han, B.-X., et al. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114909 · Cited by 8
Optogenetic dissection of cortical information processing-shining light on schizophrenia
Wang, X., & Carlén, M. (2012) · Brain Research · doi:10.1016/j.brainres.2012.04.015 · Cited by 10
Amygdala: Neuroanatomy and neurophysiology of fear
Tsvetkov, E., Ивановна, К. Е., Vesselkin, N. P., & Kharazova, A. (2015) · Journal of Evolutionary Biochemistry and Physiology · doi:10.1134/s0022093015060022 · Cited by 11
“This can be well exemplified by inhibitory neurons in the CeA nucleus among which two subpopulations with mutually antithetic functions were singled out [7, 63, 64].”
BackgroundFrancesconi, W., Szűcs, A. L., Berton, F., Koob, G. F., Vendruscolo, L. F., & Sanna, P. P. (2017) · Psychopharmacology · doi:10.1007/s00213-017-4732-4 · Cited by 10
“In particular, the jcBNST has direct projections to the medial part of the central nucleus of the amygdala (CeAm), like other cell groups of the anterolateral BNST (Dong et al., 2000).”
Stamatakis, A., Diamantopoulou, A., Panagiotaropoulos, T. I., Raftogianni, A., & Stylianopoulou, F. (2014) · Developmental Psychobiology · doi:10.1002/dev.21248 · Cited by 10
Diamantopoulou, A., Raftogianni, A., Stamatakis, A., Tzanoulinou, S., Oitzl, M. S., & Stylianopoulou, F. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.02.012 · Cited by 10
“Even within the CeA it has been shown that there are two distinct populations, one of which elicits freezing while the other inhibits it (Haubensak et al., 2010).”
BackgroundViral Vectors for Optogenetics of Hypothalamic Neuropeptides
Knobloch, H. S., Charlet, A., Stoop, R., & Grinevich, V. (2013) · Neuromethods · doi:10.1007/978-1-62703-610-8_16 · Cited by 9
Optogenetics 2.0: challenges and solutions towards a quantitative probing of neural circuits
Altahini, S., Arnoux, I., & Stroh, A. (2023) · Biological Chemistry · doi:10.1515/hsz-2023-0194 · Cited by 11
Impaired oxytocin signalling in the central amygdala in rats with chronic heart failure
Althammer, F., Roy, R. K., Kirchner, M. K., Campos‐Lira, E., Schimmer, J., Charlet, A., Grinevich, V., & Stern, J. E. (2024) · The Journal of Physiology · doi:10.1113/jp286297 · Cited by 8
“…demonstrated multiple times before, and the CeL → CeM circuit has been shown to contribute to anxiety-like behaviour or depression in several studies, including work from our lab (Hasan et al., 2019; Knobloch et al., 2012; Wahis et al., 2021) and others (Haubensak et al., 2010; Massi et al., 2023).”
Liu, Y. K., Kelly, M. A., Sexton, T. J., & Neumaier, J. F. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.04.032 · Cited by 10
“The amygdala is a brain area that receives strong serotonergic projections and is heavily implicated in fear and anxiety behaviors (Davis, 1992; Ebner et al., 2004; Lowry et al., 2005; Ciocchi et al., 2010; Haubensak et al., 2010; Herry et al., 2010; Johansen et al., 2010).”
BackgroundLepousez, G., Alonso, M., Wagner, S., Gallarda, B. W., & Lledo, P. (2011) · Journal of Visualized Experiments · doi:10.3791/3380 · Cited by 9
Subregional Differences in Alcohol Modulation of Central Amygdala Neurocircuitry
Melkumyan, M., & Silberman, Y. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.888345 · Cited by 9
Hao, L., Yang, Z., Gong, P., & Lei, J. (2018) · Cognitive Neurodynamics · doi:10.1007/s11571-018-9479-z · Cited by 9
“control the level of conditioned freezing (Ciocchi et al. 2010; Haubensak et al. 2010).”
Secretagogin marks amygdaloid PKCδ interneurons and modulates NMDA receptor availability
Hevesi, Z., Zelena, D., Romanov, R. A., Hanics, J., Ignácz, A., Zambon, A., Pollak, D. D., Lendvai, D., Schlett, K., Palkovits, M., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1921123118 · Cited by 9
“Previously, PKCδ CeL neurons were classified as late-firing cells (10).”
BackgroundResultInfluentialOptogenetics in neuroscience: what we gain from studies in mammals
Chen, Q., Zeng, Z., & Hu, Z. (2012) · Neuroscience Bulletin · doi:10.1007/s12264-012-1250-6 · Cited by 9
“Thus, functional connectivity exists between CEl PKC-δ or PKC-δ neurons and neurons projecting to the CEm-PAG, which play an important role in associative fear learning([62]).”
Characterization of McDonald's intermediate part of the Central nucleus of the amygdala in the rat
Barbier, M., FELLMANN, D., & Risold, P. (2018) · The Journal of Comparative Neurology · doi:10.1002/cne.24470 · Cited by 10
Zhu, T., Yan, Y., Deng, S., Liu, Y., Fan, H.-R., Ma, B., Meng, B., Mei, B., Li, W., & Li, F. R. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.08.034 · Cited by 9
“To distinguish the neuron type specificity to ME, PKC-δCre mice (Cai et al., 2014; Haubensak et al., 2010) were injected with an AAV-DIO-EGFP virus allowing the specific identification of PKC-δpositive neurons in the CeL (Fig.”
InfluentialBoyle, C. A., & Lei, S. (2023) · Journal of Cellular Physiology · doi:10.1002/jcp.31020 · Cited by 8
“The microcircuits of the CeA are involved in fear processing (Ciocchi et al., 2010; Haubensak et al., 2010; Viviani et al., 2011) and send projections to brainstem nuclei involved in fear expression and cardiovascular responses (Viviani et al., 2011).”
BackgroundDou, Y., Liu, Y., Ding, W.-Q., Li, Q., Zhou, H., Li, L., Zhao, M., Li, Z.-Y.-Q., Yuan, J., Wang, X., et al. (2024) · National Science Review · doi:10.1093/nsr/nwae195 · Cited by 8
“Most previous studies on the neural mechanisms of the CEA in different physiological processes (i.e. fear, pain modulation) were mostly based on molecularly defined subtypes of CEA neurons [17 ,66 ,67 ].”
MethodGABAergic Neurons in the Central Amygdala Promote Emergence from Isoflurane Anesthesia in Mice
Zhang, J., Yao, W., Zhang, L., Li, Z.-S., Gong, X.-T., Duan, L.-L., Huang, Z.-X., Chen, T., Huang, J.-C., Yang, S.-X., et al. (2024) · Anesthesiology · doi:10.1097/aln.0000000000005279 · Cited by 9
“29 For example, in a study on conditioned fear, Haubensak et al. 30 found that PKC-δ –positive central amygdala neurons inhibited neuronal output in the central medial amygdala and produced mutual inhibition with PKC-δ –negative neurons in the lateral central amygdala.”
Coordinated excitatory and inhibitory circuits governing unpredictable threat-induced anxiety
Teng, S.-W., Wang, X., Yao, Z.-X., He, T., Gao, M.-Y., Che, Y.-Y., Wei, X.-Y., Chen, X.-L., Liu, C., & Chen, Z.-Y. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.115146 · Cited by 9
Li, J., Li, Z.-A., Tian, H.-M., Tao, S.-S., Zhang, Q., Li, F. Y., & Li, Y.-Q. (2025) · Brain Research · doi:10.1016/j.brainres.2025.149753 · Cited by 8
Crofton, E. J., O’Buckley, T. K., Bohnsack, J. P., Morrow, A. L., & Herman, M. A. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.0717-23.2023 · Cited by 8
Acute and chronic alcohol modulation of extended amygdala calcium dynamics
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. (2024) · Alcohol · doi:10.1016/j.alcohol.2024.02.004 · Cited by 9
Schnapp, W. I., Kim, J., Wang, Y., Timilsena, S., Fang, C., & Cai, H. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.113933 · Cited by 9
“We crossed PKC-δ -Cre C57BL/6 mice (generated by David Anderson’s lab 57 ) with wildtype (WT) C57BL/6 mice from the Charles River Laboratory to get PKC-δ -Cre and WT littermate mice; the same mouse line as was used in previous studies from our lab.”
MethodSelf-citationChen, W., Guo, H., Zhou, N., Mai, Y., Hu, T., Xu, X., He, T., Wen, J., Qin, S., Liu, C., et al. (2024) · Theranostics · doi:10.7150/thno.95383 · Cited by 8
“The lCeA predominantly consists of PKCδ + neurons [43, 44], and optogenetic activation of lCeA PKCδ was anxiolytic [45].”
BackgroundGrossmann, C. P., Sommer, C., Fahliogullari, I. B., Neumann, I. D., & Menon, R. (2024) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2024.107083 · Cited by 8
“…OXT release within the LS and the amygdala – regions, where the neuropeptide robustly facilitates either social fear extinction (LS) (Menon et al., 2018; Zoicas et al., 2014) or non-social fear expression and anxiety (amygdala) (Haubensak et al., 2010; Huber et al., 2005; Knobloch et al., 2012).”
Comyn, T., Préat, T., Pavlowsky, A., & Plaçais, P.-Y. (2024) · eLife · doi:10.7554/elife.92085.3 · Cited by 20
“In mammals, this non-canonical D1-like receptor/Gq coupling was notably found in the hippocampus and amygdala ( Jin et al., 2001 ; Ming et al., 2006 ), two brain areas that are enriched in PKC δ +neurons ( Haubensak et al., 2010 ; Zafiri and Duvarci, 2022 ).”
BackgroundInfluentialKamboj, S., Carlson, E. L., Ander, B. P., Hanson, K. L., Murray, K. D., Fudge, J. L., Bauman, M. D., Schumann, C. M., & Fox, A. S. (2024) · American Journal of Psychiatry · doi:10.1176/appi.ajp.20230602 · Cited by 8
Amygdalostriatal transition zone neurons encode sustained cue responses to guide defensive behaviors
Mills, F., Lee, C. R., Howe, J. R., Li, H., Keisler, M. N., Shao, S., Taschbach, F., Lemieux, M., Aloboudi, F., White, J., et al. (2026) · Neuron · doi:10.1016/j.neuron.2026.08.012 · Cited by 10
He, T., Chen, W., Fan, Y., Xu, X., Wang, Z., Li, N., Guo, H., Lu, X., Ge, F., & Guan, X. (2022) · Brain Communications · doi:10.1093/braincomms/fcac219 · Cited by 9
“its two types of non-over-lapping but mutually suppresses GABA neurons, expressed with protein kinase C-δ (PKCδ) or somatostatin (SOM), respectively.(51,52) The lCeA and lCeA neurons have opposite effects on the output neurons in the medial region of the CeA (mCeA): The lCeA neurons inhibit these output neurons that p…”
BackgroundShi, P., Zhang, M., Liu, A., Yang, C.-L., Yue, J.-Y., Hu, R., Mao, Y., Zhang, Z., Wang, W., Jin, Y., et al. (2023) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.1006125 · Cited by 9
“Immunofluorescence staining showed that the tdTomato-labeled neurons in the CeA were colocalized with the GABA-specific antibody (Figures 1I,J), which is consistent with previous research, suggesting that the CeA contains 95% GABA neurons (Haubensak et al., 2010; Janak and Tye, 2015; MartinFernandez et al., 2017).”
BackgroundResultOptogenetics: Perspectives in Biomedical Research (Review)
Bregestovski, P. D., & Mukhtarov, M. R. (2016) · Современные технологии в медицине · doi:10.17691/stm2016.8.4.26 · Cited by 8
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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