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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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“Projections from the BLA enter the CeA at the level of the lateral division and unit studies have shown that following fear conditioning, the CS activates ‘ON neurons’ in the lateral CeA, and these cells inhibit a different population of tonically active ‘OFF neurons’ (Ciocchi et al. 2010; Haubensak et al. 2010).”
BackgroundInfluentialPlacing prediction into the fear circuit
McNally, G. P., Johansen, J. P., & Blair, H. T. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.03.005 · Cited by 298
Organization of valence-encoding and projection-defined neurons in the basolateral amygdala
Beyeler, A., Chang, C.-J., Silvestre, M., Lévêque, C., Namburi, P., Wildes, C. P., & Tye, K. M. (2018) · Cell Reports · doi:10.1016/j.celrep.2017.12.097 · Cited by 306
“…the CeA in freezing and avoidance (Ciocchi et al., 2010; Davis and Shi, 1999; Duvarci and Pare, 2014; Fadok et al., 2017; Goosens and Maren, 2001; Haubensak et al., 2010; Jimenez and Maren, 2009; Li et al., 2013; Maren and Quirk, 2004; Penzo et al., 2014; Sanford et al., 2017; Viviani et al.,…”
BackgroundRemote Control of Neuronal Signaling
Rogan, S. C., & Roth, B. L. (2011) · Pharmacological Reviews · doi:10.1124/pr.110.003020 · Cited by 339
“Ideally, researchers will soon begin to combine multiple approaches to modulating signaling to determine the interplay between the targeted pathways.”
BackgroundCommon brain mechanisms of chronic pain and addiction
Elman, I., & Borsook, D. (2016) · Neuron · doi:10.1016/j.neuron.2015.11.027 · Cited by 303
Inhibition in the amygdala anxiety circuitry
Babaev, O., Chatain, C. P., & Krueger‐Burg, D. (2018) · Experimental & Molecular Medicine · doi:10.1038/s12276-018-0063-8 · Cited by 334
Whole-brain mapping of the direct inputs and axonal projections of POMC and AgRP neurons
Wang, D., He, X., Zhao, Z., Feng, Q., Lin, R., Sun, Y., Ding, T., Xu, F., Luo, M., & Zhan, C. (2015) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2015.00040 · Cited by 298
Design and generation of recombinant rabies virus vectors
Osakada, F., & Callaway, E. M. (2013) · Nature Protocols · doi:10.1038/nprot.2013.094 · Cited by 298
Self-citationThe Neuropeptide Tac2 Controls a Distributed Brain State Induced by Chronic Social Isolation Stress
Zelikowsky, M., Hui, M., Karigo, T., Choe, A., Yang, B., Blanco, M. R., Beadle, K., Gradinaru, V., Deverman, B. E., & Anderson, D. J. (2018) · Cell · doi:10.1016/j.cell.2018.03.037 · Cited by 290
“Tone fear conditioning and shock reactivity The protocol for tone trace fear conditioning occurred as previously described (Cushman et al., 2014) in fear conditioning boxes previously described in detail (Haubensak et al., 2010; Kunwar et al., 2015).”
BackgroundMethodSelf-citationActive Avoidance Learning Requires Prefrontal Suppression of Amygdala-Mediated Defensive Reactions
Moscarello, J. M., & LeDoux, J. E. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.2596-12.2013 · Cited by 277
Distinct Ventral Pallidal Neural Populations Mediate Separate Symptoms of Depression
Knowland, D., Lilascharoen, V., Pacia, C. P., Shin, S., Wang, E. H.-J., & Lim, B. K. (2017) · Cell · doi:10.1016/j.cell.2017.06.015 · Cited by 273
“Scale bars, 200 mm. (D) Molecular characterization of CeA inputs to PVVP/VTA neurons via FISH assay.”
InfluentialBocchio, M., Nabavi, S., & Capogna, M. (2017) · Neuron · doi:10.1016/j.neuron.2017.03.022 · Cited by 265
“group expresses protein kinase C- (PKC-) but predominantly lacks somatostatin (SOM) expression (Ciocchi et al., 2010; Haubensak et al., 2010; Li et al, 2013).”
InfluentialBruchas, M. R., Schindler, A. G., Shankar, H., Messinger, D. I., Miyatake, M., Land, B. B., Lemos, J. C., Hagan, C. E., Neumaier, J. F., Quintana, A., et al. (2011) · Neuron · doi:10.1016/j.neuron.2011.06.011 · Cited by 273
“In addition, differences in functional roles are consistent with isoform differences in other signaling kinases including the various PKC isoforms (Haubensak et al., 2010; Sajikumar and Korte, 2011).”
Seeking a Spotless Mind: Extinction, Deconsolidation, and Erasure of Fear Memory
Maren, S. (2011) · Neuron · doi:10.1016/j.neuron.2011.04.023 · Cited by 259
“…that mediate fear responses, such as freezing, tachycardia, and stress hormone release, and axonal projections from BLA to CE are critical for the expression of these responses after fear conditioning (Ciocchi et al., 2010; Haubensak et al., 2010; Jimenez and Maren, 2009; Paré et al., 2004).”
BackgroundRadley, J., Morilak, D., Viau, V., & Campeau, S. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.06.018 · Cited by 339
“Moreover, both BLA and CeA contain heterogeneous intrinsic subpopulations of interneurons that differentially modulate adaptive behavioral responses (Ciocchi et al., 2010; Haubensak et al., 2010; Wolff et al., 2014).”
BackgroundCentral amygdala circuits modulate food consumption through a positive-valence mechanism
Douglass, A. M., Kucukdereli, H., Ponserre, M., Marković, M., Gründemann, J., Strobel, C., Morales, P. L. A., Conzelmann, K., Lüthi, A., & Klein, R. (2017) · Nature Neuroscience · doi:10.1038/nn.4623 · Cited by 264
Self-citationExtending the amygdala in theories of threat processing
Fox, A. S., Oler, J. A., Tromp, D., Fudge, J. L., & Kalin, N. H. (2015) · Trends in Neurosciences · doi:10.1016/j.tins.2015.03.002 · Cited by 267
New perspectives on central amygdala function
Fadok, J. P., Marković, M., Tovote, P., & Lüthi, A. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.02.009 · Cited by 275
Self-citationPrefrontal cortical control of a brainstem social behavior circuit
Franklin, T. B., Silva, B. A., Perova, Z., Marrone, L., Masferrer, M. E., Zhan, Y., Kaplan, A., Greetham, L., Verrechia, V., Halman, A., et al. (2017) · Nature Neuroscience · doi:10.1038/nn.4470 · Cited by 231
Lo, L., & Anderson, D. J. (2011) · Neuron · doi:10.1016/j.neuron.2011.12.002 · Cited by 251
“While conditional trans-synaptic tracer viruses are available to map the synaptic inputs to genetically marked neuronal subpopulations (DeFalco et al., 2001; Haubensak et al., 2010; Wall et al., 2010; Weible et al., 2010; Wickersham et al., 2007), an analogous anterogradespecific trans-synaptic viral tracer for mappin…”
Self-citationNeural Circuit Motifs in Valence Processing
Tye, K. M. (2018) · Neuron · doi:10.1016/j.neuron.2018.10.001 · Cited by 268
“For examples of innate valence, the initial application of optogenetic-mediated projection-specific manipulation identified the BLA-CeA projection as anxiolytic (Tye et al., 2011), specifically biased toward the lateral aspect of the CeA (CeL), which in turn produced feedforward inhibition on neurons in the medial asp…”
InfluentialDual and Opposing Functions of the Central Amygdala in the Modulation of Pain
Wilson, T. D., Valdivia, S., Khan, A., Ahn, H., Adke, A. P., González, S. M., Sugimura, Y. K., & Carrasquillo, Y. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.09.011 · Cited by 238
“To determine which neurons, among this highly heterogeneous group of cells, modulate painrelated behaviors, we took a genetic approach in which we fluorescently labeled molecularly distinct CeA neurons (Figure 1C) (Han et al., 2015; Haubensak et al., 2010; Li et al., 2013) and combined this with optogenetically assist…”
BackgroundMethodThe emergence and influence of internal states
Flavell, S. W., Gogolla, N., Lovett-Barron, M., & Zelikowsky, M. (2022) · Neuron · doi:10.1016/j.neuron.2022.04.030 · Cited by 246
Thompson, J. M., & Neugebauer, V. (2017) · Pain Research and Management · doi:10.1155/2017/8296501 · Cited by 238
An emerging circuit pharmacology of GABAA receptors
Engin, E., Benham, R. S., & Rudolph, U. (2018) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2018.04.003 · Cited by 225
“For instance, a population of GABAergic neurons in the CeL which express protein kinase Cd (PKCd neurons) increase their spontaneous activity following fear conditioning [34], and are involved in fear generalization and anxiety (Figure 1D) [4].”
BackgroundRepetition suppression: a means to index neural representations using BOLD?
Barron, H. C., Garvert, M. M., & Behrens, T. E. J. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0355 · Cited by 229
GABAergic RIP-Cre Neurons in the Arcuate Nucleus Selectively Regulate Energy Expenditure
Kong, D., Tong, Q., Ye, C., Koda, S., Fuller, P. M., Krashes, M. J., Vong, L., Ray, R. S., Olson, D. P., & Lowell, B. B. (2012) · Cell · doi:10.1016/j.cell.2012.09.020 · Cited by 215
“ChR2 and CRACM Viral Channelrhodopsin-2 expression and activation were similarly performed as previously described (Atasoy et al., 2008; Haubensak et al., 2010; Higley et al., 2011; Zhang et al., 2007).”
Amygdala, neuropeptides, and chronic pain-related affective behaviors
Neugebauer, V., Mazzitelli, M., Cragg, B., Ji, G., Navratilova, E., & Porreca, F. (2020) · Neuropharmacology · doi:10.1016/j.neuropharm.2020.108052 · Cited by 220
Functional heterogeneity in the bed nucleus of the stria terminalis
Gungor, N. Z., & Pare, D. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.0856-16.2016 · Cited by 214
“Central in the Walker et al. (2009a) model is the notion that BNST activation is delayed relative to that of CeM.”
BackgroundInfluentialLoss of O -GlcNAc glycosylation in forebrain excitatory neurons induces neurodegeneration
Wang, A. C., Jensen, E. H., Rexach, J. E., Vinters, H. V., & Hsieh-Wilson, L. C. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1606899113 · Cited by 211
A VTA GABAergic Neural Circuit Mediates Visually Evoked Innate Defensive Responses
Zhou, Z., Liu, X., Chen, S., Zhang, Z., Liu, Y., Montardy, Q., Tang, Y., Wei, P., Liu, N., Li, L., et al. (2019) · Neuron · doi:10.1016/j.neuron.2019.05.027 · Cited by 221
Genetically encoded optical indicators for the analysis of neuronal circuits
Knöpfel, T. (2012) · Nature reviews. Neuroscience · doi:10.1038/nrn3293 · Cited by 205
Stress Modulation of Opposing Circuits in the Bed Nucleus of the Stria Terminalis
Daniel, S., & Rainnie, D. G. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.178 · Cited by 224
“The CRF neurons in the CeAL are a distinct population from neurons expressing the neuronal marker, PKC-δ (Haubensak et al, 2010).”
BackgroundMethodInfluentialBiag, J., Huang, Y., Gou, L., Hintiryan, H., Askarinam, A., Hahn, J. D., Toga, A. W., & Dong, H. (2012) · Journal of Comparative Neurology · doi:10.1002/cne.22698 · Cited by 205
“…using either traditional tract tracing method (see, e.g., Wang and Burkhalter, 2007; Hashimoto et al., 2009; Qin and Luo, 2009) or genetically modified virus tracing (see, e.g., Campbell and Herbison, 2007; Wickersham et al., 2007; Atasoy et al., 2008; Braz et al., 2009; Haubensak et al., 2010).”
MethodSelf-citationA Central Amygdala CRF Circuit Facilitates Learning about Weak Threats
Sanford, C. A., Soden, M. E., Baird, M. A., Miller, S. M., Schulkin, J. A., Palmiter, R. D., Clark, M., & Zweifel, L. S. (2016) · Neuron · doi:10.1016/j.neuron.2016.11.034 · Cited by 206
“CRF Neurons Are Largely Distinct from Other Populations within the CeAL Electrophysiological recordings in the CeAL during presentations of threat-associated stimuli have revealed two primary response profiles: ‘‘fear-on’’ and ‘‘fear-off’’ neurons (Haubensak et al., 2010).”
InfluentialAmygdala microcircuits mediating fear expression and extinction
Pare, D., & Duvarci, S. (2012) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2012.02.014 · Cited by 193
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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