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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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Nonhuman Primate Models to Explore Mechanisms Underlying Early-Life Temperamental Anxiety
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BackgroundInfluentialCannabinoids: Revealing their complexity and role in central networks of fear and anxiety
Murkar, A., Koninck, J. D., & Merali, Z. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.09.002 · Cited by 35
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“…densitometry identified a higher expression of Crh, Pdyn, Prkcd, and Sst in the CeL compared to the CeM, which is in agreement with previous studies in mice and rats (Veinante et al., 1997; Day et al., 1999; Marchant et al., 2007; Li et al., 2013; Kim et al., 2017; McCullough et al., 2018).”
BackgroundResultIntensity of anxiety is modified via complex integrative stress circuitries
Smith, J. P., Prince, M. A., Achua, J. K., Robertson, J. M., Anderson, R. T., Ronan, P. J., & Summers, C. H. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.10.016 · Cited by 34
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“Within the CeA there are several molecularly distinct neuronal populations which mediate speci fi c elements of fear conditioning (FC) and extinction (EXT) learning processes 23 – 33 .”
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“Besides the PV+ and CRH+ neurons in the CeA, there are also a large amount of somatostatin-positive interneurons (Li et al., 2013), PKC-δ+ neurons (Haubensak et al.”
BackgroundTinbergen’s challenge for the neuroscience of behavior
Pfaff, D. W., Tabansky, I., & Haubensak, W. E. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1903589116 · Cited by 33
Grin1 Receptor Deletion within CRF Neurons Enhances Fear Memory
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Transcriptomics reveals amygdala neuron regulation by fasting and ghrelin thereby promoting feeding
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Emotion in action: When emotions meet motor circuits
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“The involvement of individual cell–types (PKCδ, SOM, CRF; see Introduction) in pain–related amygdala neuroplasticity has not been fully explored and is currently an area of extensive research (Wilson et al., 2019; Li and Sheets, 2020; Adke et al., 2021).”
BackgroundJüngling, K., Lange, M. D., Szkudlarek, H. J., Lesting, J., Erdmann, F. S., Doengi, M., Kügler, S., & Pape, H. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.125 · Cited by 32
“A similar increase of the expression of the immediate early gene c-fos was observed in SOMpositive CeL neurons of fear-conditioned mice (Li et al, 2013).”
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NPY Y2 receptors in the central amygdala reduce cued but not contextual fear
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Serotonergic neuromodulation of synaptic plasticity
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Visual Sequences Drive Experience-Dependent Plasticity in Mouse Anterior Cingulate Cortex
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“Anatomical circuit mapping with viral vectors and CTB—Adeno-associated virus (AAV) vectors (~1012 viral molecules per mL), AAV5-CaMKII-GFP, and AAV5-CaMKIIhChR2-EYFP, were produced by the University of North Carolina Vector Core Facilities (Chapel Hill, NC) and have been described previously (Li et al., 2013; Miyamich…”
MethodBaird, M. A., Hsu, T. Y., Wang, R., Juarez, B., & Zweifel, L. S. (2020) · eNeuro · doi:10.1523/eneuro.0370-20.2020 · Cited by 29
“…heterogeneous and interconnected structure that has emerged as an important central regulator for the acquisition, consolidation, and expression of conditioned threat (Ciocchi et al., 2010; Haubensak et al., 2010; Li et al., 2013) and anxiety-related behavior (Tye et al., 2011; Botta et al., 2015).”
BackgroundInhibitory circuits in fear memory and fear-related disorders
Singh, S. P., & Topolnik, L. (2023) · Frontiers in Neural Circuits · doi:10.3389/fncir.2023.1122314 · Cited by 29
“Furthermore, optogenetic activation of these cells elicited freezing behavior whereas their silencing impaired fear learning (Li et al., 2013).”
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“…by the facts that the stimulations to any of these areas can trigger memory retrievals (Ehrlich et al., 2009; Pape and Pare, 2010; Liu et al., 2012; Li et al., 2013; Xu and Südhof, 2013; Otis et al., 2017; Yokose et al., 2017) as well as the responses to associated signals can be recorded in…”
BackgroundCGRP-dependent sensitization of PKC-δ positive neurons in central amygdala mediates chronic migraine
Chou, T.-M., Lee, Z.-F., Wang, S., Lien, C., & Chen, S. (2022) · The Journal of Headache and Pain · doi:10.1186/s10194-022-01531-8 · Cited by 27
“As the CeA primarily comprises heterogeneous GABAergic subpopulations of interneurons [44–46], we further investigated whether these pERK positive neurons were protein kinase C-delta (PKC-δ) or somatostatin (SOM) positive neurons, two major non-overlapping cell types in the CeA [44, 46, 47], with immunofluorescent co-…”
BackgroundEstradiol and progesterone in female reward-learning, addiction, and therapeutic interventions
Hilz, E. N., & Lee, H. J. (2022) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2022.101043 · Cited by 29
Wiring Specificity and Synaptic Diversity in the Mouse Lateral Central Amygdala
Hou, W., Kuo, N., Fang, G.-W., Huang, H., Wu, K.-P., Zimmer, A., Cheng, J., & Lien, C. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.3309-15.2016 · Cited by 28
“SOM neurons display heterogeneous intrinsic excitability (Li et al., 2013).”
BackgroundResultInfluentialAn NTS-CeA projection modulates depression-like behaviors in a mouse model of chronic pain
He, S., Huang, X., Zheng, J., Zhang, Y., & Ruan, X. (2022) · Neurobiology of Disease · doi:10.1016/j.nbd.2022.105893 · Cited by 27
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Somatostatin receptors (SSTR1-5) on inhibitory interneurons in the barrel cortex
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Disynaptic specificity of serial information flow for conditioned fear
Massi, L., Hagihara, K. M., Courtin, J., Hinz, J., Müller, C. R., Fustiñana, M. S., Xu, C., Karalis, N., & Lüthi, A. (2023) · Science Advances · doi:10.1126/sciadv.abq1637 · Cited by 25
“Previous work identified so-matostatin-expressing CeA neurons (SST + ) as a major subpopulation projecting to the vlPAG ( 8 , 13 ), and stimulation of SST + CeA neurons elicits freezing behavior in naïve and conditioned animals ( 19 , 20 ) [but see ( 13 )].”
BackgroundRío, R. T.-D., van den Burg, E. H., Stoop, R., & Hegoburu, C. (2018) · Psychopharmacology · doi:10.1007/s00213-018-5030-5 · Cited by 26
Kovner, R., Souaiaia, T., Fox, A. S., French, D. A., Goss, C. E., Roseboom, P. H., Oler, J. A., Riedel, M. K., Fekete, E. M., Fudge, J. L., et al. (2020) · Biological Psychiatry · doi:10.1016/j.biopsych.2020.05.009 · Cited by 25
The amygdala instructs insular feedback for affective learning
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“As the CE serves as a major gate for conditioned behavior (Goosens and Maren, 2001; Haubensak et al., 2010; Li et al., 2013), the IC and CE may constitute components of a dedicated cortico-limbic network for affective decision-making and Pavlovian learning.”
BackgroundTopographic representation of current and future threats in the mouse nociceptive amygdala
Bowen, A. J., Huang, Y. W., Chen, J., Pauli, J. L., Campos, C., & Palmiter, R. D. (2023) · Nature Communications · doi:10.1038/s41467-023-35826-4 · Cited by 26
PACAP Controls Endocrine and Behavioral Stress Responses via Separate Brain Circuits
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“Unilateral viral injections were performed using previously described procedures (Li et al., 2013) at the following stereotaxic coordinates: MD: –1.58 mm from bregma, 0.44 mm lateral from midline, and 3.20 mm ventral from cortical surface; dorsal mPFC: 1.94 mm from bregma, 0.34 mm lateral from…”
MethodInfluentialSelf-citationMesolimbic neuropeptide W coordinates stress responses under novel environments
Motoike, T., Long, J. M., Tanaka, H., Sinton, C. M., Skach, A., Williams, S. C., Hammer, R. E., Sakurai, T., & Yanagisawa, M. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1518658113 · Cited by 24
Searching basic units in memory traces: associative memory cells
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A systems-neuroscience model of phasic dopamine.
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“Although the BLA is not strongly topographically organized, we assume a similar opponency between subsets of neurons, as is more clearly demonstrated in the central amygdala CElON vs. CElOFF cells (Ciocchi et al., 2010; Li et al., 2013).”
BackgroundResultSerotonin modulates an inhibitory input to the central amygdala from the ventral periaqueductal gray
Hon, O. J., DiBerto, J. F., Mazzone, C. M., Sugam, J. A., Bloodgood, D. W., Hardaway, J. A., Husain, M., Kendra, A. M., McCall, N. M., López, A. J., et al. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-022-01392-4 · Cited by 23
Synaptic plasticity in two cell types of central amygdala for regulation of emotion and pain
Ge, J., Cai, Y., & Pan, Z. Z. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.997360 · Cited by 22
“These markers include SOM, PKCδ, CRF, neurotensin and tachykinin (Li et al., 2013; Hunt et al., 2017; McCullough et al., 2018; Wilson et al., 2019; Li and Sheets, 2020; Miller Neilan et al., 2021).”
BackgroundResultInfluentialDemaestri, C., Pisciotta, M., Altunkeser, N., Berry, G., Hyland, H., Breton, J., Darling, A., Williams, B. L., & Bath, K. G. (2024) · Nature Communications · doi:10.1038/s41467-024-49828-3 · Cited by 23
PACAP increases Arc/Arg 3.1 expression within the extended amygdala after fear conditioning in rats
Meloni, E. G., Kaye, K. T., Venkataraman, A., & Carlezon, W. A. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.11.011 · Cited by 21
“More exhaustive future analyses may reveal that the remainder (and majority) of Arcpositive cells in the CeA and BNST co-express other neuropeptides such as enkephalin, neurotensin or somatostatin, which are also found in high densities in these areas (Day et al., 1999; Li et al., 2013).”
Neural Circuit Mechanism Underlying the Feeding Controlled by Insula-Central Amygdala Pathway
Zhang-Molina, C., Schmit, M. B., & Cai, H. (2020) · iScience · doi:10.1016/j.isci.2020.101033 · Cited by 24
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“…& Roberto, 2013), CRF-tomato (Silberman, Matthews, & Winder, 2013), PKC-d::GluCla-iCre (Haubensak et al., 2010), and the somatostatin-IRES-Cre (Li et al., 2013) lines, is likely to play an important role in gaining a better understanding of the general architecture of CeA neurocircuitry and…”
BackgroundMethodGABAergic microcircuitry of fear memory encoding
Cummings, K. A., Lacagnina, A. F., & Clem, R. L. (2021) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2021.107504 · Cited by 23
“Similar plasticity has been observed in GABAergic projection cells of the central amygdala (Li et al. 2013, Penzo et al. 2014, Penzo et al. 2015), which underlines the importance of GABAergic plasticity in fear conditioning, but is beyond the scope of the present review.”
BackgroundGrowth Hormone Action in Somatostatin Neurons Regulates Anxiety and Fear Memory
dos Santos, W. O., Juliano, V. A. L., Chaves, F. M., Vieira, H. R., Frazão, R., List, E. O., Kopchick, J. J., Munhoz, C. D., & Donato, J. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.0254-23.2023 · Cited by 22
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“As suggested for the mouse CeL [Bupesh et al., 2011a], it is likely that the Std-derived Pax6 neurons of the chicken pINP contain ENK, while the Stv-derived Islet1 neurons may contain CRF and/or other neuropep- (For figure see next page.)”
BackgroundInfluentialBiologically based neural circuit modelling for the study of fear learning and extinction
Nair, S. S., Paré, D., & Vicentic, A. (2016) · npj Science of Learning · doi:10.1038/npjscilearn.2016.15 · Cited by 20
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MeCP2 in cholinergic interneurons of nucleus accumbens regulates fear learning
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“The amygdala has been emphasized as an essential component in the network that encodes fear (Adolphs, 2013; Johansen et al., 2010; Maren and Quirk, 2004; Paton et al., 2006; Reijmers et al., 2007; Janak and Tye, 2015; Yu et al., 2017; Li et al., 2013).”
BackgroundA Glitch in the Matrix: The Role of Extracellular Matrix Remodeling in Opioid Use Disorder
Ray, M. H., Williams, B. R., Kuppe, M. K., Bryant, C. D., & Logan, R. W. (2022) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2022.899637 · Cited by 20
“In human and rodent brain, chondroitin sulfate glycosaminoglycans (CS-GAGs) accumulate around the synapse in response to inflammation (Li et al., 2013) and may be increased following chronic opioid use in human brain (Seney et al., 2021).”
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Salience processing by glutamatergic neurons in the ventral pallidum
Wang, F., Zhang, J., Yuan, Y., Chen, M., Gao, Z., Zhan, S., Fan, C., Sun, W., & Hu, J. (2019) · 中国科学通报：英文版 · doi:10.1016/j.scib.2019.11.029 · Cited by 18
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“1 3 dense glutamatergic synapses onto CeA, with the LA projecting only to its lateral sector (CeL) [47], and the BLA projecting to both the lateral and the medial (CeM) sectors [48–50].”
BackgroundReichard, R. A., Subramanian, S., Desta, M. T., Sura, T. A., Becker, M. L., Ghobadi, C. W., Parsley, K. P., & Zahm, D. S. (2016) · Brain Structure and Function · doi:10.1007/s00429-016-1321-y · Cited by 23
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BackgroundRessler, R. L., Goode, T. D., Evemy, C. G., & Maren, S. (2020) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2020.107281 · Cited by 20
Cellular mechanisms underlying central sensitization in a mouse model of chronic muscle pain
Lin, Y., Yang, Z.-S., Wong, W.-Y., Lin, S.-C., Wang, S., Chen, S., Cheng, J., Lü, H., & Lien, C. (2022) · eLife · doi:10.7554/elife.78610 · Cited by 24
“Nevertheless, the neural mechanisms by which the CeASST neurons and their downstream targets regulate negative affect have been characterized (Ahrens et al., 2018; Haubensak et al., 2010; Li et al., 2013; Zhou et al., 2019).”
BackgroundAntolasic, E. J., Jaehne, E. J., & van den Buuse, M. (2023) · Current Neuropharmacology · doi:10.2174/1570159x21666230724101321 · Cited by 22
“…that PTSD is moderately inheritable, although the *Address correspondence to this author at the School of Psychology and Public Health, La Trobe University, Melbourne, Victoria 3086, Australia; Tel: +61394795257; E-mail: m.vandenbuuse@latrobe.edu.au specific genes implicated remain unclear [7, 8].”
BackgroundDelaney, A., Crane, J. W., Holmes, N. M., Fam, J. P., & Westbrook, R. F. (2018) · Scientific Reports · doi:10.1038/s41598-018-28321-0 · Cited by 18
Encoding of Environmental Cues in Central Amygdala Neurons during Foraging
Ponserre, M., Fermani, F., Gaitanos, L., & Klein, R. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.1791-21.2022 · Cited by 18
Learning rules for aversive associative memory formation
Ozawa, T., & Johansen, J. P. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.02.010 · Cited by 25
Somatostatin Gene and Protein Expression in the Non-human Primate Central Extended Amygdala
Kovner, R., Fox, A. S., French, D. A., Roseboom, P. H., Oler, J. A., Fudge, J. L., & Kalin, N. H. (2019) · Neuroscience · doi:10.1016/j.neuroscience.2018.12.035 · Cited by 19
“The peptide somatostatin (SST) is of particular interest as studies in mice demonstrate a role for CeL SST neurons in modulating threat-related responses [16, 17, 22-25].”
InfluentialDiverse Effects of Conditioned Threat Stimuli on BehaviorPreprint
Moscarello, J. M., & LeDoux, J. E. (2014) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2014.79.024968 · Cited by 24
“Inactivation of the lateral subdivision of CeA, which receives direct projections from LA (Pitkänen et al. 1997; Li et al. 2013), prevents the acquisition of aversive Pavlovian memory.”
BackgroundInfluentialPrice, M. E., & McCool, B. A. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.857550 · Cited by 20
“Fear conditioning reverses the relative strength of these synapses by increasing glutamate release from the BLA onto CeASOM+ neurons and decreasing glutamate release onto CeASOM- neurons (Li et al., 2013).”
BackgroundAlteration of the Centromedial Amygdala Glutamatergic Synapses by the BDNF Val66Met Polymorphism
Galvin, C., Lee, F. S., & Ninan, I. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.76 · Cited by 19
Mapping the estrous cycle to context-specific extinction memory.
Hilz, E. N., Smith, R. W., Hong, Y. J., Monfils, M., & Lee, H. J. (2019) · Behavioral Neuroscience · doi:10.1037/bne0000343 · Cited by 17
Butler, C., Wilson, Y. M., Gunnersen, J. M., & Murphy, M. (2015) · Learning & Memory · doi:10.1101/lm.037663.114 · Cited by 20
“The CeA has long been associated as an output site of fearful behavior (Johansen et al. 2011), but has recently been found to be directly involved in the fear-conditioning process (Ciocchi et al. 2010; Haubensak et al. 2010; Li et al. 2013).”
BackgroundInfluentialGao, Z., Wu, R., Chen, C., Wen, B., Liu, Y., Lü, W., Chen, N., Feng, J., Fan, R., Wang, D., et al. (2019) · Brain Research · doi:10.1016/j.brainres.2019.146333 · Cited by 17
Yang, L., Chen, M., Ma, Q., Huan, S., Cui, D., Shao, D., Lai, B., & Zheng, P. (2020) · Neuropharmacology · doi:10.1016/j.neuropharm.2020.108217 · Cited by 17
Douceau, S., Lemarchand, E., Hommet, Y., Lebouvier, L., Joséphine, C., Bemelmans, A., Maubert, E., Agin, V., & Vivien, D. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01455-4 · Cited by 17
The Amygdala – A Hub of the Social Auditory Brain
Wenstrup, J. J., Ghasemahmad, Z., Hazlett, E., & Shanbhag, S. J. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.24194-1 · Cited by 16
Ueda, S., Hosokawa, M., Arikawa, K., Takahashi, K., Fujiwara, M., Kakita, M., Fukada, T., Koyama, H., Horigane, S., Itoi, K., et al. (2021) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2021.741895 · Cited by 17
Liu, Y., Ge, R., Zhao, X. C., Guo, R., Huang, L. T., Zhao, S., Guan, S., Lü, W., Cui, S., Wang, S. D., et al. (2017) · Oncotarget · doi:10.18632/oncotarget.19918 · Cited by 15
Behavioral outputs and overlapping circuits between conditional fear and active avoidance
Diehl, M. M., Moscarello, J. M., & Trask, S. (2024) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2024.107943 · Cited by 16
Diminishing fear: Optogenetic approach toward understanding neural circuits of fear control
Luchkina, N. V., & Bolshakov, V. Y. (2017) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2017.05.005 · Cited by 16
“SOM+ cells do not directly inhibit CeM (15% of CeM-projecting cells are SOM+; Li et al., 2013) and promote freezing via their long-range projections to PAG (Penzo et al., 2014).”
InfluentialKondev, V., Morgan, A., Najeed, M., Winters, N. D., Kingsley, P. J., Marnett, L. J., & Patel, S. (2022) · Biological Psychiatry · doi:10.1016/j.biopsych.2022.05.012 · Cited by 17
Bonnan, A., Zhang, K., Gaffield, M. A., & Christie, J. M. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.0731-22.2022 · Cited by 16
Sosulina, L., Strippel, C., Parra, H. R., Walter, A. L., Kanyshkova, T. G., Sartori, S. B., Lange, M. D., Singewald, N., & Pape, H. (2015) · Journal of Neurophysiology · doi:10.1152/jn.00883.2014 · Cited by 16
“…(CEl) and medial (CEm) subnuclei, and subpopulations of CEl GABAergic neurons characterized by the absence or presence of protein kinase C (PKC ) connect to CEm GABAergic neurons to gate fear expression and regulate fear generalization (Ciocchi et al. 2010; Haubensak et al. 2010; Li et al. 2013).”
BackgroundDiagnostic potential of multimodal neuroimaging in posttraumatic stress disorder
Im, J. J., Kim, B., Hwang, J., Kim, J. E., Kim, J., Rhie, S. J., Namgung, E., Kang, I., Moon, S., Lyoo, I. K., et al. (2017) · PLoS ONE · doi:10.1371/journal.pone.0177847 · Cited by 17
Mattera, A., Pagani, M., & Baldassarre, G. (2020) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2020.569108 · Cited by 15
Locomotor suppression by a monosynaptic amygdala to brainstem circuitPreprint
Roseberry, T. K., Lalive, A. L., Margolin, B. D., & Kreitzer, A. C. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/724252 · Cited by 13
“…in this output projection to MLR may appear surprising in light of evidence for a functional opposition between CeL and CeM, in which CeL neurons inhibit projection neurons in the neighboring CeM (Ciocchi et al., 2010; Fadok et al., 2017; Huber et al., 2005; Li et al., 2013; Viviani et al., 2011).”
BackgroundInfluentialNausea-induced suppression of feeding is mediated by central amygdala Dlk1-expressing neurons
Ding, W., Weltzien, H., Peters, C., & Klein, R. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.113990 · Cited by 14
Control of Behavioral Arousal and Defense by a Glutamatergic Midbrain-Amygdala Pathway in Mice
Chen, S.-Y., Yao, J., Hu, Y., Chen, H., Liu, P.-C., Wang, W., Zeng, Y.-H., Zhuang, C.-W., Zeng, S.-X., Li, Y., et al. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.850193 · Cited by 14
Self-citationFear Learning: An Evolving Picture for Plasticity at Synaptic Afferents to the Amygdala
Palchaudhuri, S., Osypenko, D., & Schneggenburger, R. (2022) · The Neuroscientist · doi:10.1177/10738584221108083 · Cited by 15
Lay, 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
Longitudinal Assessment of Amygdala Activity in Mice Susceptible to Trauma
Dirven, B. C. J., Botan, A., van der Geugten, D., Kraakman, B., van Melis, L. V. J., Merjenburgh, S., van Rijn, R., Waajen, L., Homberg, J. R., Kozicz, T., et al. (2022) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2022.105912 · Cited by 14
Sengupta, A., & McNally, G. P. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00148 · Cited by 14
“ORIGINAL RESEARCH ARTICLE published: 01 May 2014 doi: 10.3389/fnbeh.2014.00148”
BackgroundInfluentialMolecular basis for and chemogenetic modulation of comorbidities in GABRG 2‐deficient epilepsies
Zhang, C., McMahon, B., Dong, H., Warner, T. A., Shen, W., Gallagher, M. J., Macdonald, R. L., & Kang, J. (2019) · Epilepsia · doi:10.1111/epi.15160 · Cited by 15
Li, J., Chen, K. M., & Sheets, P. L. (2022) · The Journal of Comparative Neurology · doi:10.1002/cne.25332 · Cited by 11
“∗P< .05; ∗∗P< .01; ∗∗∗P< .001 This firing property has been denoted previously as a “late-firing” phenotype (Hunt et al., 2017; Li et al., 2013; Li & Sheets, 2018).”
BackgroundResultMolecular diversity and functional dynamics in the central amygdala
Yeh, L.-F., Zuo, S., & Liu, P.-W. (2024) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2024.1364268 · Cited by 15
“Together, these two distinct populations make up over 80% of CeL neurons (Haubensak et al., 2010; Li et al., 2013).”
BackgroundAmygdala intercalated cells form an evolutionarily conserved system orchestrating brain networks
Aksoy‐Aksel, A., Ferraguti, F., Holmes, A., Lüthi, A., & Ehrlich, I. (2024) · Nature Neuroscience · doi:10.1038/s41593-024-01836-8 · Cited by 16
Valence and salience encoding in the central amygdala
Kong, M.-S., Ancell, E., Witten, D., & Zweifel, L. S. (2024) · eLife · doi:10.7554/elife.101980.3 · Cited by 16
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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