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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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Whittle, N., Fadok, J. P., MacPherson, K. P., Nguyen, R., Botta, P., Wolff, S. B. E., Müller, C. R., Herry, C., Tovote, P., Holmes, A., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-24068-x · Cited by 87
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“…both to and within the central nucleus of the amygdala (CeA) (Paré et al. 2004; Wilensky et al. 2006; Ciocchi et al. 2010; Duvarci et al. 2011; Li et al. 2013a), at synapses onto interneurons in the LA and basolateral amygdala (BLA) (Mahanty and Sah 1998; Bauer and LeDoux 2004), and the…”
GABAergic interneurons: The orchestra or the conductor in fear learning and memory?
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“A third, smaller population of low-threshold bursting neurons has also been described (Dumont et al., 2002; Lopez de Armentia and Sah, 2004; Haubensak et al., 2010; Li et al., 2013; Hou et al., 2016).”
BackgroundMethodInfluentialMetastable dynamics of neural circuits and networks
Brinkman, B. A. W., Yan, H., Maffei, A., Park, I. M., Fontanini, A., Wang, J., & La Camera, G. (2022) · Applied Physics Reviews · doi:10.1063/5.0062603 · Cited by 64
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A Central Amygdala Input to the Parafascicular Nucleus Controls Comorbid Pain in Depression
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“The amygdaloid complex is well known to be relevant to fear learning, anxiety, reward, and pain (Duvarci and Pare, 2014; Li et al., 2013; Tovote et al., 2015; Tye et al., 2011; Zhuo, 2008).”
BackgroundResultA novel cortico-intrathalamic circuit for flight behavior
Dong, P., Wang, H., Shen, X., Jiang, P., Zhu, X., Li, Y., Gao, J., Lin, S., Huang, Y., He, X., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0391-6 · Cited by 71
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“The lateral CeA sends GABAergic to the medial CeA in cell type and projection-specific manner to gate behavior (Ciocchi et al. 2010; Haubensak et al. 2010; Li et al. 2013; Tye et al. 2011).”
BackgroundSugimura, Y. K., Takahashi, Y., Watabe, A. M., & Kato, F. (2016) · Journal of Neurophysiology · doi:10.1152/jn.00946.2015 · Cited by 69
“The authors declare no conflict of interest regarding the contents of this study.”
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“Activation of SOM neurons, on the other hand, is sufficient to induce freezing in naïve freely moving mice (Li et al., 2013).”
BackgroundIntegration of Descending Command Systems for the Generation of Context-Specific Locomotor Behaviors
Kim, L. H., Sharma, S., Sharples, S. A., Mayr, K. A., Kwok, C. H. T., & Whelan, P. J. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00581 · Cited by 75
“…in part by both the CeA and BLA of the amygdala (LeDoux, 2000; Medina et al., 2002; Wilensky et al., 2006; Ciocchi et al., 2010; Duvarci et al., 2011; Frontiers in Neuroscience | www.frontiersin.org 10 October 2017 | Volume 11 | Article 581 Li et al., 2013; Han et al., 2015; Sato et al., 2015).”
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Hartley, N. D., Gaulden, A. D., Báldi, R., Winters, N. D., Salimando, G. J., Rosas-Vidal, L. E., Jameson, A. N., Winder, D. G., & Patel, S. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0528-7 · Cited by 72
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Regulation of Hippocampal Memory by mTORC1 in Somatostatin Interneurons
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“Fear conditioning strongly relies on amygdala function where SOM-INs play 168 crucial roles (22, 23).”
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Botta, P., Fushiki, A., Vicente, A. M., Hammond, L. A., Mosberger, A. C., Gerfen, C. R., Peterka, D. S., & Costa, R. M. (2020) · Cell · doi:10.1016/j.cell.2020.09.023 · Cited by 66
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“Two of these markers, somatostatin (Sst; Cassell and Gray, 1989) and protein kinase C-d (PKC-d ; Haubensak et al., 2010), label two major populations that are largely nonoverlapping in the CeA (Haubensak et al., 2010; Li et al., 2013; Li, 2019).”
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Abstinence-dependent dissociable central amygdala microcircuits control drug craving
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Central amygdala cells for learning and expressing aversive emotional memories
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Self-citationAmygdala inhibitory neurons as loci for translation in emotional memories
Shrestha, P., Shan, Z., Mamcarz, M., Ruiz, K. S. A., Zerihoun, A. T., Juan, C.-Y., Herrero-Vidal, P., Pelletier, J., Heintz, N., & Klann, E. (2020) · Nature · doi:10.1038/s41586-020-2793-8 · Cited by 61
Amygdala Circuits for Fear Memory: A Key Role for Dopamine Regulation
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A Central Amygdala-Substantia Innominata Neural Circuitry Encodes Aversive Reinforcement Signals
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“There are two major subpopulations of GABAergic neurons found in the CeL, one expressing the neuropeptide somatostatin (SOM) and the other expressing protein kinase C-delta (PKC-d) (Haubensak et al., 2010; Li et al., 2013).”
BackgroundSelf-citationIn vivo sub-millisecond two-photon optogenetics with temporally focused patterned light
Chen, I.-W., Ronzitti, E., Lee, B. R., Daigle, T. L., Dalkara, D., Zeng, H., Emiliani, V., & Papagiakoumou, E. I. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.1785-18.2018 · Cited by 71
“Here, we extended these investigations to three efficient ChR variants: ReaChR, CoChR, and ChrimsonR (Lin et al., 2013; Klapoetke et al., 2014).”
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“The central nucleus of the amygdala (CEA) is not only the major output station of the amygdala but consists itself of a highly complex micro-network capable of diverse types of plasticity (Ciocchi et al. 2010; Haubensak et al. 2010; Li et al. 2013; Wilensky et al. 2006).”
A brainstem-central amygdala circuit underlies defensive responses to learned threats
Gu, Y., Piper, W. T., Branigan, L., Vazey, E. M., Aston‐Jones, G., Lin, L., LeDoux, J. E., & Sears, R. M. (2019) · Molecular Psychiatry · doi:10.1038/s41380-019-0599-6 · Cited by 65
Central amygdala circuit dynamics underlying the benzodiazepine anxiolytic effect
Griessner, J., Pasieka, M., Böhm, V., Groessl, F., Kaczanowska, J., Pliota, P., Kargl, D., Werner, B., Kaouane, N., Strobelt, S., et al. (2018) · Molecular Psychiatry · doi:10.1038/s41380-018-0310-3 · Cited by 64
“However, CEAl PKCδ neurons are under inhibitory control of CEAl SST (largely identical to PKCδ) [23] neurons, the other major class of antagonistically wired GABA-ergic neuronal populations (Supplementary Fig.”
BackgroundGüngör, N. Z., Yamamoto, R., & Paré, D. (2015) · Journal of Neurophysiology · doi:10.1152/jn.00677.2015 · Cited by 64
“A possible solution to this conundrum comes from recent reports indicating that different subsets of CeL neurons reciprocally inhibit each other and form contrasting connections with CeM (Ciocchi et al. 2010; Haubensak et al. 2010; Li et al. 2013; Viviani et al. 2011).”
BackgroundSynaptic potentiation in the nociceptive amygdala following fear learning in mice
Watabe, A. M., Ochiai, T., Nagase, M., Takahashi, Y., Satô, M., & Kato, F. (2013) · Molecular Brain · doi:10.1186/1756-6606-6-11 · Cited by 61
Cell-Type Specificity of Neuronal Excitability and Morphology in the Central Amygdala
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“In all these studies, however, glutamatergic inputs to Som- cells are stronger than those to Som+ neurons in the CeC (Li and Sheets, 2019, Li et al., 2013).”
BackgroundResultInfluentialThe modulation of emotional and social behaviors by oxytocin signaling in limbic network
Triana-Del Rio, R., Ranade, S., Guardado, J., LeDoux, J., Klann, E., & Shrestha, P. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.1002846 · Cited by 58
Behavioral and brain mechanisms mediating conditioned flight behavior in rats
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Stress peptides sensitize fear circuitry to promote passive coping
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“In contrast, Pavlovian fear evokes long-term synaptic plasticity, that relies in part on postsynaptic effects at BLA-CE synapses (7), which are gated also by CRH (9).”
InfluentialRajbhandari, A. K., Octeau, C. J., Gonzalez, S. T., Pennington, Z. T., Mohamed, F., Trott, J. M., Chavez, J., Ngyuen, E., Keces, N., Hong, W., et al. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.2564-20.2021 · Cited by 59
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“The stimulus to any of these areas in neural circuits can evoke conditioned reflex (Ehrlich et al., 2009; Pape and Pare, 2010; Liu et al., 2012; Li et al., 2013; Xu and Südhof, 2013).”
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Convergence on reduced stress behavior in the Mexican blind cavefish
Chin, J. S. R., Gassant, C. E., Amaral, P. M., Lloyd, E., Stahl, B. A., Jaggard, J. B., Keene, A. C., & Duboué, E. R. (2018) · Developmental Biology · doi:10.1016/j.ydbio.2018.05.009 · Cited by 51
“In mammals, the central nucleus of the amygdala has both stressinducing and stress-suppressing neuronal populations (Ciocchi et al., 2010; Li et al., 2013; Tye et al., 2011; Wilensky et al., 2006).”
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The center of the emotional universe: Alcohol, stress, and CRF1 amygdala circuitry
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Endocannabinoid Modulation of Predator Stress-Induced Long-Term Anxiety in Rats
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Somatostatin neurons control an alcohol binge drinking prelimbic microcircuit in mice
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Prelimbic cortex drives discrimination of non-aversion via amygdala somatostatin interneurons
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“For silencing genetically defined interneuron populations, 3-5 month old male C57/B6 mice expressing cre-recombinase in either SOM+ cells (SOM-IRES-cre) (Taniguchi et al., 2011) or PV+ cells (PV-IRES-cre) (Hippenmeyer et al., 2005) were utilized.”
InfluentialA PCR-Based Method for RNA Probes and Applications in Neuroscience
Hua, R., Yu, S., Liu, M., & Li, H. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00266 · Cited by 55
“Previous studies show that the central lateral amygdala (CeL) contains three types of neurons expressing SST, PKC-δ, or CRH (Li et al., 2013; Wang et al., 2016).”
BackgroundSelf-citationNeural circuits for the adaptive regulation of fear and extinction memory
Plas, S. L., Tuna, T., Bayer, H., Juliano, V. A. L., Sweck, S. O., Pérez, A. D. A., Hassell, J. E., & Maren, S. (2024) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2024.1352797 · Cited by 55
GABA Cells in the Central Nucleus of the Amygdala Promote Cataplexy
Snow, M. B., Fraigne, J. J., Thibault‐Messier, G., Chuen, V. L., Thomasian, A., Horner, R. L., & Peever, J. H. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.4070-15.2017 · Cited by 47
Top-down control of conditioned overconsumption is mediated by insular cortex Nos1 neurons
Stern, S. A., Azevedo, E. P., Pomeranz, L. E., Doerig, K. R., Ivan, V. J., & Friedman, J. M. (2021) · Cell Metabolism · doi:10.1016/j.cmet.2021.03.001 · Cited by 47
Sex differences in behavioral responses during a conditioned flight paradigm
Borkar, C. D., Dorofeikova, M., Le, Q.-S. E., Vutukuri, R., Vo, C., Hereford, D., Resendez, A., Basavanhalli, S., Sifnugel, N., & Fadok, J. P. (2020) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.112623 · Cited by 49
Associative memory cells and their working principle in the brain
Wang, J., & Cui, S. (2018) · F1000Research · doi:10.12688/f1000research.13665.1 · Cited by 45
Organizational principles of amygdalar input-output neuronal circuits
Huang, L., Chen, Y., Jin, S., Lin, L., Duan, S., Si, K., Gong, W., & Zhu, J. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01262-3 · Cited by 49
Top-down control of flight by a non-canonical cortico-amygdala pathway
Borkar, C. D., Stelly, C. E., Fu, X., Dorofeikova, M., Le, Q.-S. E., Vutukuri, R., Vo, C., Walker, A. B., Basavanhalli, S., Duong, A., et al. (2024) · Nature · doi:10.1038/s41586-023-06912-w · Cited by 45
“It has been demonstrated that CeL circuit activity is regulated by local recurrent inhibitory interactions 2,34,35 , and this mutual inhibition motif is important for rapid action selection.”
McCullough, K. M., Morrison, F. G., & Ressler, K. J. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.07.025 · Cited by 50
Danger and distress: Parabrachial-extended amygdala circuits
Jaramillo, A. A., Brown, J. A., & Winder, D. G. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108757 · Cited by 46
The Insula Cortex Contacts Distinct Output Streams of the Central Amygdala
Ponserre, M., Peters, C., Fermani, F., Conzelmann, K., & Klein, R. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.0567-20.2020 · Cited by 45
Scheich, B., Csekő, K., Borbély, É., Ábrahám, I. M., CSERNUS, V. J., Gaszner, B., & Helyes, Z. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.01.039 · Cited by 47
“In particular, a crucial role of somatostatin-expressing neurons has been demonstrated (Li et al., 2013).”
BackgroundSchipper, P., Hiemstra, M., Bosch, K., Nieuwenhuis, D., Adinolfi, A., Glotzbach, S., Borghans, B., Lopresto, D., Fernández, G., Klumpers, F., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1904843116 · Cited by 44
Nentwig, T. B., Obray, J. D., Vaughan, D. T., & Chandler, L. J. (2022) · Scientific Reports · doi:10.1038/s41598-022-10668-0 · Cited by 41
“…with CNO in slice electrophysiology applications typically monitored changes in membrane potential, action potential firing, rheobase, etc., and reported near-maximal inhibitory responses with 5 or 10 uM CNO (Anderson et al., 2019; Buchta et al., 2017; H. Li et al., 2013; M. M. Li et al., 2019).”
BackgroundMouse models of fear-related disorders: Cell-type-specific manipulations in amygdala
Gafford, G. M., & Ressler, K. J. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.06.019 · Cited by 46
“A study by Li and colleagues (71) investigated how a specific subset of CeL neurons respond to fear conditioning and contribute to both the learning and expression of fear.”
The bed nucleus of the stria terminalis regulates ethanol-seeking behavior in mice
Pina, M. M., Young, E. A., Ryabinin, A. E., & Cunningham, C. L. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2015.08.033 · Cited by 42
“Moreover, these doses were based on previously published studies showing that CNO alone produced no physiological or behavioral response in rodents at doses of 10 mg/kg and above (Li et al., 2013; Mahler et al., 2014; Ray et al., 2011, 2013; Vazey and Aston-Jones, 2014).”
BackgroundPrefrontal dopamine regulates fear reinstatement through the downregulation of extinction circuits
HitoraーImamura, N., Miura, Y., Teshirogi, C., Ikegaya, Y., Matsuki, N., & Nomura, H. (2015) · eLife · doi:10.7554/elife.08274 · Cited by 43
“…from the IL and contains two functionally distinct subpopulations of neurons (CElon or somatostatin-expressing neurons, and CEloff or protein kinase C-δ-expressing neurons) forming local inhibitory circuits to inhibit CeM activity (Ciocchi et al., 2010; Haubensak et al., 2010; Li et al., 2013).”
BackgroundVasuta, C., Artinian, J., Laplante, I., Hébert-Seropian, S., Elayoubi, K., & Lacaille, J. (2015) · eNeuro · doi:10.1523/eneuro.0051-15.2015 · Cited by 40
“Furthermore, SOMINs have been shown to specifically and dynamically regulate input-output transformations and to gate burst firing in pyramidal cells (Lovett-Barron et al., 2012).”
BackgroundYan, F., Gao, Z., Pin, C., Huang, L. T., Wang, D., Chen, N., Wu, R., Feng, J., Cui, S., Lü, W., et al. (2016) · Neural Plasticity · doi:10.1155/2016/5648390 · Cited by 40
“This hypothesis is granted by the facts that stimulating any of these areas triggers memory retrieval [75–79] and the responses to the associated signals are detected in sensory cortices [28] and their downstream brain areas [30, 31, 80].”
McCullough, K. M., Daskalakis, N. P., Gafford, G. M., Morrison, F. G., & Ressler, K. J. (2018) · Translational Psychiatry · doi:10.1038/s41398-018-0190-y · Cited by 40
Berret, E., Kintscher, M., Palchaudhuri, S., Tang, W., Osypenko, D., Kochubey, O., & Schneggenburger, R. (2019) · Science · doi:10.1126/science.aaw0474 · Cited by 42
RetractedBruzsik, B., Bíró, L., Zelena, D., Sipos, E., Szebik, H., Sarosdi, K. R., Horváth, O., Farkas, I., Csillag, V., Finszter, C. K., et al. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.1944-20.2020 · Cited by 40
Neuronal cell types, projections, and spatial organization of the central amygdala
O’Leary, T. P., Kendrick, R. M., Bristow, B. N., Sullivan, K. E., Wang, L., Clements, J., Lemire, A. L., & Cembrowski, M. S. (2022) · iScience · doi:10.1016/j.isci.2022.105497 · Cited by 42
“focused on two marker genes, Prkcd and Sst, which are virtually non-overlapping in expression(11,13,18,39,40) with associated cells differing in electrophysiology,(18,39,41) local CEA circuitry(19,39,42) and function.(6,18,19,42) Beyond these classical CEA cell types, cell types defined by other marker genes (e.”
Homeostatic regulation of memory systems and adaptive decisions
Mizumori, S. J. Y., & Jo, Y. S. (2013) · Hippocampus · doi:10.1002/hipo.22176 · Cited by 43
“neural activity in response to fear (Ciocchi et al., 2010; Haubensak et al., 2010; Li et al., 2013).”
BackgroundGlucocorticoid Induces Incoordination between Glutamatergic and GABAergic Neurons in the Amygdala
Wang, G.-Y., Zhao-ming, Z., Cui, S., & Wang, J. (2016) · PLoS ONE · doi:10.1371/journal.pone.0166535 · Cited by 40
Neuropeptide signalling in the central nucleus of the amygdala
van den Burg, E. H., & Stoop, R. (2018) · Cell and Tissue Research · doi:10.1007/s00441-018-2862-6 · Cited by 42
Sun, Y., Qian, L., Xu, L., Hunt, S., & Sah, P. (2020) · Molecular Psychiatry · doi:10.1038/s41380-020-00894-1 · Cited by 41
Functional organization of the midbrain periaqueductal gray for regulating aversive memory formation
Yeh, L.-F., Ozawa, T., & Johansen, J. P. (2021) · Molecular Brain · doi:10.1186/s13041-021-00844-0 · Cited by 35
Meloni, E. G., Venkataraman, A., Donahue, R. J., & Carlezon, W. A. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.11.003 · Cited by 36
“The increase in c-Fos in the CeA is consistent with a role for this structure in the acquisition of fear conditioning (Li et al., 2013) and of enhanced synaptic plasticity in CeA neurons after PACAP application (Cho et al., 2012).”
BackgroundInfluentialMultiple Memory Subsystems: Reconsidering Memory in the Mind and Brain
Sherman, B. E., Turk‐Browne, N. B., & Goldfarb, E. V. (2023) · Perspectives on Psychological Science · doi:10.1177/17456916231179146 · Cited by 48
“BLA lesions decreased selection of a “rapid escape” behavior and facilitated autonomic reactions (human startle potential and rodent freezing) associated with CeA (Fadok et al., 2017; Li et al., 2013).”
BackgroundBurnett, C. J., & Krashes, M. J. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.1333-16.2016 · Cited by 40
“Chemogenetic inhibition of CeA SST cells during conditioning, however, prevented the development of fear-conditioned responses, implicating their necessity for fear learning (H. Li et al., 2013).”
BackgroundSerine Racemase and D-serine in the Amygdala Are Dynamically Involved in Fear Learning
Balu, D. T., Presti, K. T., Huang, C. C., Muszynski, K., Radzishevsky, I. S., Wolosker, H., Guffanti, G., Ressler, K. J., & Coyle, J. T. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.08.012 · Cited by 38
“Protein kinase C delta (PKCδ) neurons are referred to as CeLOFF because they inhibit output CeM neurons (47).”
BackgroundInfluentialWalker, L. C. (2021) · Journal of Neurochemistry · doi:10.1111/jnc.15301 · Cited by 38
“Optogenetic manipulations suggest these populations may have opposing roles in fear and anxiety- like behaviours (Botta et al., 2015; Cai et al., 2014; Fadok et al., 2017; Li et al., 2013).”
BackgroundSilencing of amygdala circuits during sepsis prevents the development of anxiety-related behaviours
Bourhy, L., Mazeraud, A., Costa, L. H. A., Levy, J., Rei, D., Hecquet, E., Gabanyi, I., Bozza, F. A., Chrétien, F., Lledo, P.-M., et al. (2022) · Brain · doi:10.1093/brain/awab475 · Cited by 37
Associative memory cells: Formation, function and perspective
Wang, J., & Cui, S. (2017) · F1000Research · doi:10.12688/f1000research.11096.1 · Cited by 37
An active inference perspective for the amygdala complex
Sladky, R., Kargl, D., Haubensak, W. E., & Lamm, C. (2023) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2023.11.004 · Cited by 41
Gastrointestinal hormones and the gut connectome
Ye, L., & Liddle, R. A. (2016) · Current Opinion in Endocrinology Diabetes and Obesity · doi:10.1097/med.0000000000000299 · Cited by 37
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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