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.
“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]
The Abstract reports that a central-amygdala microcircuit controls conditioned freezing in mice, supporting a role in defensive behaviour. It does not establish that the amygdala switches rodents between different defensive modes; the behaviour studied here is conditioned freezing. (LLM, conf=0.84)
Experimental — accuracy not yet measuredBLA neurons excite GABAergic CeL neurons that provide feed-forward inhibition onto CeM output neurons.
“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]
A population of GABAergic neurons in CeL expressing PKC-delta increase spontaneous activity following fear conditioning and are involved in fear generalization and anxiety.
“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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The paraventricular thalamus controls a central amygdala fear circuit
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Experience-dependent modification of a central amygdala fear circuit
Li, H., Penzo, M. A., Taniguchi, H., Kopec, C. D., Huang, Z. J., & Li, B. (2013) · Nature Neuroscience · doi:10.1038/nn.3322 · Cited by 497 · see citing works
Differential Innervation of Direct- and Indirect-Pathway Striatal Projection Neurons
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“We utilized a two-virus system, in combination with Creexpressing mouse lines (Gong et al., 2007), to target genetically specified projection neuron subtypes in the striatum and specifically label their monosynaptic inputs (Haubensak et al., 2010; Wall et al., 2010).”
Self-citationScalable control of mounting and attack by Esr1+ neurons in the ventromedial hypothalamus
Lee, H., Kim, D.-W., Remedios, R., Anthony, T. E., Chang, A., Madisen, L., Zeng, H., & Anderson, D. J. (2014) · Nature · doi:10.1038/nature13169 · Cited by 479 · see citing works
Self-citationImplications of memory modulation for post-traumatic stress and fear disorders
Parsons, R. G., & Ressler, K. J. (2013) · Nature Neuroscience · doi:10.1038/nn.3296 · Cited by 476 · see citing works
Encoding of fear learning and memory in distributed neuronal circuits
Herry, C., & Johansen, J. P. (2014) · Nature Neuroscience · doi:10.1038/nn.3869 · Cited by 474 · see citing works
A competitive inhibitory circuit for selection of active and passive fear responses
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Self-citationBasolateral to Central Amygdala Neural Circuits for Appetitive Behaviors
Kim, J., Zhang, X., Muralidhar, S., LeBlanc, S., & Tonegawa, S. (2017) · Neuron · doi:10.1016/j.neuron.2017.02.034 · Cited by 460 · see citing works
“Cell-type-specific studies have shown evidence for the involvement of several genetically defined CeA neurons in aversive behaviors such as defensive responses and anxiogenesis (Andero et al., 2014; Han et al., 2015; Haubensak et al., 2010; Isosaka et al., 2015; Li et al., 2013;McCall et al., 2015; Pomrenze et al., 20…”
BackgroundResultInfluentialThe Central Amygdala as an Integrative Hub for Anxiety and Alcohol Use Disorders
Gilpin, N. W., Herman, M. A., & Roberto, M. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.09.008 · Cited by 457 · see citing works
“Acute alcohol decreases firing of CRF1-negative neurons but increases firing of CRF1-positive neurons, suggesting a local CeAM inhibitory microcircuit whose constituent neurons are differentially regulated by alcohol, similar to the CeAL inhibitory microcircuit described in the behavioral expression of conditioned fea…”
BackgroundElucidating an Affective Pain Circuit that Creates a Threat Memory
Han, S., Soleiman, M. T., Soden, M. E., Zweifel, L. S., & Palmiter, R. D. (2015) · Cell · doi:10.1016/j.cell.2015.05.057 · Cited by 447 · see citing works
“, 2010); PKC-d neurons decrease their firing rate in response to the CS (CeAloff) (Haubensak et al., 2010), whereas SOM neurons increase their firing rate in response to the CS (CeAlon) (Li et al.”
InfluentialIzquierdo, I., Furini, C. R. G., & Myskiw, J. C. (2016) · Physiological Reviews · doi:10.1152/physrev.00018.2015 · Cited by 453 · see citing works
Neural and cellular mechanisms of fear and extinction memory formation
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Monosynaptic Circuit Tracing with Glycoprotein-Deleted Rabies Viruses
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“…with particular cell-surface receptors (Choi and Callaway, 2011), and to genetically identified cell types in Cre- or tTA-expressing mouse lines (Haubensak et al., 2010; Wall et al., 2010; Weible et al., 2010; Miyamichi et al., 2011; Watabe-Uchida et al., 2012; Wall et al., 2013; Fu et al.,…”
BackgroundSelf-citationSingewald, N., Schmuckermair, C., Whittle, N., Holmes, A., & Ressler, K. J. (2015) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2014.12.004 · Cited by 390 · see citing works
“CeL-OFF neurons (PKCδ+ phenotype) inhibit fear-promoting CeM neurons, while CeL-ON (PKCδ- phenotype) cells stimulate fear-promoting CeM neurons (Ciocchi et al., 2010; Haubensak et al., 2010).”
BackgroundLeDoux, J. E., & Daw, N. D. (2018) · Nature reviews. Neuroscience · doi:10.1038/nrn.2018.22 · Cited by 391 · see citing works
Oxytocin Selectively Gates Fear Responses Through Distinct Outputs from the Central Amygdala
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Central amygdala PKC-δ+ neurons mediate the influence of multiple anorexigenic signals
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Self-citationSynapse-specific astrocyte gating of amygdala-related behavior
Martin-Fernandez, M., Jamison, S., Robin, L. M., Zhao, Z., Martin, E. D., Aguilar, J., Benneyworth, M. A., Marsicano, G., & Araque, A. (2017) · Nature Neuroscience · doi:10.1038/nn.4649 · Cited by 345 · see citing works
The birth, death and resurrection of avoidance: a reconceptualization of a troubled paradigm
LeDoux, J. E., Moscarello, J., Sears, R., & Campese, V (2017) · Molecular Psychiatry · doi:10.1038/mp.2016.166 · Cited by 348 · see citing works
Neurobehavioral perspectives on the distinction between fear and anxietyPreprint
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“Specifically, lateral nucleus neurons project to the lateral subdivision of central nucleus (CeL), which sends GABAergic projections to the medial subdivision of the central nucleus (CeM) (Haubensak et al. 2010).”
Self-citationA neural circuit for comorbid depressive symptoms in chronic pain
Zhou, W., Jin, Y., Meng, Q., Zhu, X., Bai, T., Tian, Y., Mao, Y., Wang, L., Xie, W., Zhong, H., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0468-2 · Cited by 343 · see citing works
Presynaptic partners of dorsal raphe serotonergic and GABAergic neurons
Weissbourd, B., Ren, J., DeLoach, K. E., Guenthner, C. J., Miyamichi, K., & Luo, L. (2014) · Neuron · doi:10.1016/j.neuron.2014.06.024 · Cited by 337 · see citing works
“It has been established in many systems that rabies virus spreads effectively across known synaptic connections (Haubensak et al., 2010; Miyamichi et al., 2011, 2013; Stepien et al., 2010; Takatoh et al., 2013; Ugolini, 1995; Watabe-Uchida et al., 2012; Wickersham et al., 2007) and does not infect axons in passage (e.”
BackgroundInfluentialTwo-photon optogenetic toolbox for fast inhibition, excitation and bistable modulation
Prakash, R., Yizhar, O., Grewe, B. F., Ramakrishnan, C., Wang, N. N., Goshen, I., Packer, A. M., Peterka, D. S., Yuste, R., Schnitzer, M. J., et al. (2012) · Nature Methods · doi:10.1038/nmeth.2215 · Cited by 328 · see citing works
Self-citationLocus coeruleus to basolateral amygdala noradrenergic projections promote anxiety-like behavior
McCall, J. G., Siuda, E. R., Bhatti, D. L., Lawson, L. A., McElligott, Z. A., Stuber, G. D., & Bruchas, M. R. (2017) · eLife · doi:10.7554/elife.18247 · Cited by 322 · see citing works
“It is also possible that the neuromodulatory effects on this circuit require a long-term associative memory component compared to fast-acting, acute activation of similar pathways (Kim et al., 2013; Namburi et al., 2015; Haubensak et al., 2010).”
BackgroundTools for Probing Local Circuits: High-Density Silicon Probes Combined with Optogenetics
Buzsáki, G., Stark, E., Berényi, A., Khodagholy, D., Kipke, D. R., Yoon, E., & Wise, K. D. (2015) · Neuron · doi:10.1016/j.neuron.2015.01.028 · Cited by 328 · see citing works
Myers, B., McKlveen, J. M., & Herman, J. P. (2014) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2013.12.003 · Cited by 318 · see citing works
“However, recent studies have defined an amygdala microcircuit wherein BLA projections activate inhibitory neurons within the CeA that gate behavioral output (Ciocchi et al., 2010; Haubensak et al., 2010; Tye et al., 2011), suggesting the amygdala has the ability to both facilitate and inhibit behaviors indicative of f…”
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The amygdala between sensation and affect: a role in pain
Veinante, P., Yalçın, İ., & Barrot, M. (2013) · Journal of Molecular Psychiatry · doi:10.1186/2049-9256-1-9 · Cited by 321 · see citing works
“While most studies focused on the BLA, recent researches on the fear circuit disclosed a part of the CeA microcircuitry involved in fear conditioning [104,105].”
BackgroundOsakada, F., Mori, T., Cetin, A. H., Marshel, J. H., Virgen, B., & Callaway, E. M. (2011) · Neuron · doi:10.1016/j.neuron.2011.07.005 · Cited by 314 · see citing works
“…SADΔG-GFP rabies viruses can be used to selectively label the direct inputs to a targeted neuronal population or even a single neuron (Haubensak et al., 2010; Marshel et al., 2010; Miyamichi et al., 2011; Rancz et al., 2011; Stepien et al., 2010; Wall et al., 2010; Wickersham et…”
InfluentialSelf-citationThe age of anxiety: role of animal models of anxiolytic action in drug discovery
Cryan, J. F., & Sweeney, F. F. (2011) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2011.01362.x · Cited by 313 · see citing works
“…amygdala-dependent fear memory (Phelps and LeDoux, 2005; Sigurdsson et al., 2007; Herry et al., 2008; Ehrlich et al., 2009; Davis et al., 2010; Haubensak et al., 2010; Pape and Pare, 2010; Parsons and Davis, 2011; Sierra-Mercado et al., 2011), which are already being paralleled with imaging…”
BackgroundResultHypothalamic Survival Circuits: Blueprints for Purposive Behaviors
Sternson, S. M. (2013) · Neuron · doi:10.1016/j.neuron.2013.02.018 · Cited by 313 · see citing works
“…2008, 2012; Kong et al., 2012; Schöne et al., 2012) and other brain regions (Arenkiel et al., 2007; Callaway and Katz, 1993; English et al., 2012; Frick et al., 2008; Haubensak et al., 2010; Luo et al., 2008; Mao et al., 2011; Shepherd and Svoboda, 2005; Stuber et al., 2011; Tye et al., 2011).”
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“Diminishing this inhibitory tone through aversive stimuli leads to a disinhibition of the CEm output neurons, triggering the execution of fear and anxiety responses (77, 78).”
BackgroundThe amygdala and medial prefrontal cortex: partners in the fear circuit
Marek, R., Strobel, C., Bredy, T. W., & Sah, P. (2013) · The Journal of Physiology · doi:10.1113/jphysiol.2012.248575 · Cited by 304 · see citing works
“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 · see citing works
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 · see citing works
“…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 · see citing works
“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 · see citing works
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 312 · see citing works
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 · see citing works
Design and generation of recombinant rabies virus vectors
Osakada, F., & Callaway, E. M. (2013) · Nature Protocols · doi:10.1038/nprot.2013.094 · Cited by 296 · see citing works
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 282 · see citing works
“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 · see citing works
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 · see citing works
“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 260 · see citing works
“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 266 · see citing works
“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 · see citing works
“…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 · see citing works
“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 257 · see citing works
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 251 · see citing works
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 255 · see citing works
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 · see citing works
Lo, L., & Anderson, D. J. (2011) · Neuron · doi:10.1016/j.neuron.2011.12.002 · Cited by 251 · see citing works
“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 247 · see citing works
“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 232 · see citing works
“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 234 · see citing works
Thompson, J. M., & Neugebauer, V. (2017) · Pain Research and Management · doi:10.1155/2017/8296501 · Cited by 231 · see citing works
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 · see citing works
“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 219 · see citing works
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 · see citing works
“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 216 · see citing works
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 · see citing works
“Central in the Walker et al. (2009a) model is the notion that BNST activation is delayed relative to that of CeM.”
BackgroundInfluentialLoss of <i>O</i> -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 · see citing works
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 211 · see citing works
Genetically encoded optical indicators for the analysis of neuronal circuits
Knöpfel, T. (2012) · Nature reviews. Neuroscience · doi:10.1038/nrn3293 · Cited by 205 · see citing works
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 213 · see citing works
“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 · see citing works
“…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 199 · see citing works
“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 · see citing works
- 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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