Organization of valence-encoding and projection-defined neurons in the basolateral amygdala
Open accessAbstract
The basolateral amygdala (BLA) mediates associative learning for both fear and reward. Accumulating evidence supports the notion that different BLA projections distinctly alter motivated behavior, including projections to the nucleus accumbens (NAc), medial aspect of the central amygdala (CeM), and ventral hippocampus (vHPC). Although there is consensus regarding the existence of distinct subsets of BLA neurons encoding positive or negative valence, controversy remains regarding the anatomical arrangement of these populations. First, we map the location of more than 1,000 neurons distributed across the BLA and recorded during a Pavlovian discrimination task. Next, we determine the location of projection-defined neurons labeled with retrograde tracers and use CLARITY to reveal the axonal path in 3-dimensional space. Finally, we examine the local influence of each projection-defined populations within the BLA. Understanding the functional and topographical organization of circuits underlying valence assignment could reveal fundamental principles about emotional processing.
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Projections from the medial amygdala to basolateral amygdala may integrate valence with social cues.
“Projections from the medial amygdala to basolateral amygdala may integrate valence with social cues [20].”
From Translational opportunities for circuit-based social neuroscience: advancing 21st century psychiatry (2021) · cites this paper as [20]
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“Here, we defined the BLA from the Paxinos and Franklin (2004) mouse atlas, including the posterior medial BLA (BLP) and excluding the anterior and posterior parts of the basomedial amygdaloid nucleus (BMA and BMP, respectively).”
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Paxinos, G. (2001) · Cited by 12,859 · see citing works
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Chung, K., Wallace, J., Kim, S.-Y., Kalyanasundaram, S., Andalman, A. S., Davidson, T. J., Mirzabekov, J. J., Zalocusky, K. A., Mattis, J., Denisin, A. K., et al. (2013) · Nature · doi:10.1038/nature12107 · Cited by 2,008 · cited 4× · see citing works
“We thank K. Chung and his lab for advice regarding CLARITY.”
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BackgroundInfluentialAmygdala circuitry mediating reversible and bidirectional control of anxiety
Tye, K. M., Prakash, R., Kim, S.-Y., Fenno, L. E., Grosenick, L., Zarabi, H., Thompson, K. R., Gradinaru, V., Ramakrishnan, C., & Deisseroth, K. (2011) · Nature · doi:10.1038/nature09820 · Cited by 1,289 · cited 3× · see citing works
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“…(LA) and the basal amygdala (BA), receives dense sensory inputs and is necessary for the acquisition of fear conditioning (Fanselow and Kim, 1994; LeDoux et al., 1990; Maren and Quirk, 2004; Miserendino et al., 1990; Wilensky et al., 1999) and reward associations (Baxter and Murray, 2002; Cador…”
BackgroundEncoding of conditioned fear in central amygdala inhibitory circuits
Ciocchi, S., Herry, C., Grenier, F., Wolff, S. B. E., Letzkus, J. J., Vlachos, I., Ehrlich, I., Sprengel, R., Deisseroth, K., Stadler, M. B., et al. (2010) · Nature · doi:10.1038/nature09559 · Cited by 924 · cited 2× · see citing works
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“Defining BLA populations by projection target has revealed functional divergences in valence coding (Beyeler et al., 2016;Burgos-Robles et al., 2017; Felix-Ortiz et al., 2013, 2016; Namburi et al., 2015; Stuber et al., 2011; Tye et al., 2011).”
BackgroundSelf-citationGenetic dissection of an amygdala microcircuit that gates conditioned fear
Haubensak, W., Kunwar, P. S., Cai, H., Ciocchi, S., Wall, N. R., Ponnusamy, R., Biag, J., Dong, H.-W., Deisseroth, K., Callaway, E. M., et al. (2010) · Nature · doi:10.1038/nature09553 · Cited by 840 · cited 2× · see citing works
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“…dense sensory inputs and is necessary for the acquisition of fear conditioning (Fanselow and Kim, 1994; LeDoux et al., 1990; Maren and Quirk, 2004; Miserendino et al., 1990; Wilensky et al., 1999) and reward associations (Baxter and Murray, 2002; Cador et al., 1989; Cardinal et al., 2002; Tye et…”
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Duvarci, S., & Pare, D. (2014) · Neuron · doi:10.1016/j.neuron.2014.04.042 · Cited by 751 · cited 2× · see citing works
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“Our results are in agreement with prior evidence that projections are heterogeneous in terms of the location and/or cell type they contact within the downstream target, because anterior BLA-NAc projectors preferentially target the anterolateral NAc, whereas the posterior BLA-NAc neurons preferentially target the poste…”
BackgroundResultSynaptic and Behavioral Profile of Multiple Glutamatergic Inputs to the Nucleus Accumbens
Britt, J. P., Benaliouad, F., McDevitt, R. A., Stuber, G. D., Wise, R. A., & Bonci, A. (2012) · Neuron · doi:10.1016/j.neuron.2012.09.040 · Cited by 716 · cited 1× · see citing works
“The accumulation of evidence surrounding the BLA-NAc projection has consistently supported the role of this projection in mediating positive valence and appetitive behavior (Beyeler et al., 2016; Britt et al., 2012; Namburi et al., 2015; Ramirez et al., 2015; Stuber et al., 2011).”
BackgroundInvolvement of the amygdala in stimulus-reward associations: interaction with the ventral striatum
Cador, M., Robbins, T. W., & Everitt, B. J. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90354-0 · Cited by 652 · cited 1× · see citing works
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BackgroundA circuit mechanism for differentiating positive and negative associations
Namburi, P., Beyeler, A., Yorozu, S., Calhoon, G. G., Halbert, S. A., Wichmann, R., Holden, S. S., Mertens, K. L., Anahtar, M., Felix-Ortiz, A. C., et al. (2015) · Nature · doi:10.1038/nature14366 · Cited by 614 · cited 8× · see citing works
“, 2016), and the synaptic strength of their inputs increased after fear conditioning (Namburi et al., 2015).”
BackgroundMethodInfluentialBLA to vHPC inputs modulate anxiety-related behaviors
Felix-Ortiz, A. C., Beyeler, A., Seo, C., Leppla, C. A., Wildes, C. P., & Tye, K. M. (2013) · Neuron · doi:10.1016/j.neuron.2013.06.016 · Cited by 592 · cited 5× · see citing works
“…not express robust preferences for positive or negative valence of conditioned cues, although they mediate innate negative valence as optogenetic activation of BLA terminals in the vHPC increases anxiety-related behaviors (Beyeler et al., 2016; Felix-Ortiz and Tye, 2014; Felix-Ortiz et al., 2013).”
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“…and Maren, 2009; Li et al., 2013; Maren and Quirk, 2004; Penzo et al., 2014; Sanford et al., 2017; Viviani et al., 2011) versus appetitive or anxiolytic behaviors (Corbit and Balleine, 2005; Hall et al., 2001; Han et al., 2017; Holland and Gallagher, 2003; Kim et al., 2017; Tye et al., 2011).”
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“908 Cell Reports 22, 905–918, January 23, 2018 only valence coding properties but also information including action selection (go or no-go) and prediction error (correct or error) (Grabenhorst et al., 2012; Baxter et al., 2000; Schoenbaum et al., 1999).”
BackgroundSchoenbaum, G., Chiba, A. A., & Gallagher, M. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-05-01876.1999 · Cited by 579 · cited 2× · see citing works
“908 Cell Reports 22, 905–918, January 23, 2018 only valence coding properties but also information including action selection (go or no-go) and prediction error (correct or error) (Grabenhorst et al., 2012; Baxter et al., 2000; Schoenbaum et al., 1999).”
BackgroundBidirectional switch of the valence associated with a hippocampal contextual memory engram
Redondo, R. L., Kim, J., Arons, A. L., Ramirez, S., Liu, X., & Tonegawa, S. (2014) · Nature · doi:10.1038/nature13725 · Cited by 512 · cited 2× · see citing works
“The valence encoding properties of BLA neurons have been investigated based upon immediate early gene expression (Gore et al., 2015; Redondo et al., 2014) and projection target (Beyeler et al.”
MethodExperience-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 · cited 2× · see citing works
“This may synthesize apparently conflicting studies reporting the role of 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 a…”
BackgroundA competitive inhibitory circuit for selection of active and passive fear responses
Fadok, J. P., Krabbe, S., Marković, M., Courtin, J., Xu, C., Massi, L., Botta, P., Bylund, K., Müller, C. R., Kovacevic, A., et al. (2017) · Nature · doi:10.1038/nature21047 · Cited by 475 · see citing works
Amygdala inputs to the ventral hippocampus bidirectionally modulate social behavior
Felix-Ortiz, A. C., & Tye, K. M. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.4257-13.2014 · Cited by 473 · cited 2× · see citing works
“…not express robust preferences for positive or negative valence of conditioned cues, although they mediate innate negative valence as optogenetic activation of BLA terminals in the vHPC increases anxiety-related behaviors (Beyeler et al., 2016; Felix-Ortiz and Tye, 2014; Felix-Ortiz et al., 2013).”
BackgroundBasolateral 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
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“This may synthesize apparently conflicting studies reporting the role of 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 a…”
BackgroundAntagonistic negative and positive neurons of the basolateral amygdala
Kim, J., Pignatelli, M., Xu, S., Itohara, S., & Tonegawa, S. (2016) · Nature Neuroscience · doi:10.1038/nn.4414 · Cited by 450 · cited 8× · see citing works
“Optogenetic stimulation of Rspo2 neurons promotes freezing behaviors, and photostimulation of Ppp1r1b neurons supports intra-cranial self-stimulation (Kim et al., 2016).”
BackgroundResultInfluentialFelix‐Ortiz, A. C., Burgos-Robles, A., Bhagat, N. D., Leppla, C. A., & Tye, K. M. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.07.041 · Cited by 414 · cited 2× · see citing works
“Defining BLA populations by projection target has revealed functional divergences in valence coding (Beyeler et al., 2016;Burgos-Robles et al., 2017; Felix-Ortiz et al., 2013, 2016; Namburi et al., 2015; Stuber et al., 2011; Tye et al., 2011).”
BackgroundMethodDivergent routing of positive and negative information from the amygdala during memory retrieval
Beyeler, A., Namburi, P., Glober, G. F., Simonnet, C., Calhoon, G. G., Conyers, G. F., Luck, R., Wildes, C. P., & Tye, K. M. (2016) · Neuron · doi:10.1016/j.neuron.2016.03.004 · Cited by 412 · cited 21× · see citing works
“This retrograde-based investigation of collateralization complements our previous anterograde-based investigation of collateralization published in Figure S3 of Beyeler et al. (2016).”
BackgroundMethodInfluentialSelf-citationOxytocin Selectively Gates Fear Responses Through Distinct Outputs from the Central Amygdala
Viviani, D., Charlet, A., van den Burg, E., Robinet, C., Hurni, N., Abatis, M., Magara, F., & Stoop, R. (2011) · Science · doi:10.1126/science.1201043 · Cited by 381 · cited 2× · see citing works
“This may synthesize apparently conflicting studies reporting the role of 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 a…”
BackgroundActivating positive memory engrams suppresses depression-like behaviour
Ramirez, S., Liu, X., MacDonald, C. J., Moffa, A., Zhou, J. Y., Redondo, R. L., & Tonegawa, S. (2015) · Nature · doi:10.1038/nature14514 · Cited by 373 · cited 1× · see citing works
“The accumulation of evidence surrounding the BLA-NAc projection has consistently supported the role of this projection in mediating positive valence and appetitive behavior (Beyeler et al., 2016; Britt et al., 2012; Namburi et al., 2015; Ramirez et al., 2015; Stuber et al., 2011).”
BackgroundFanselow, M. S., & Kim, J. J. (1994) · Behavioral Neuroscience · doi:10.1037//0735-7044.108.1.210 · Cited by 360 · cited 2× · see citing works
“The basolateral amygdala (BLA) complex, including the lateral amygdala (LA) and the basal amygdala (BA), receives dense sensory inputs and is necessary for the acquisition of fear conditioning (Fanselow and Kim, 1994; LeDoux et al., 1990; Maren and Quirk, 2004; Miserendino et al., 1990; Wilensky et al., 1999) and rewa…”
BackgroundHall, J., Parkinson, J. A., Connor, T. M., Dickinson, A., & Everitt, B. J. (2001) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01577.x · Cited by 355 · cited 2× · see citing works
“…and Maren, 2009; Li et al., 2013; Maren and Quirk, 2004; Penzo et al., 2014; Sanford et al., 2017; Viviani et al., 2011) versus appetitive or anxiolytic behaviors (Corbit and Balleine, 2005; Hall et al., 2001; Han et al., 2017; Holland and Gallagher, 2003; Kim et al., 2017; Tye et al., 2011).”
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Extended Amygdala and Basal Forebrain
Alheid, G. F. (2003) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2003.tb07082.x · Cited by 334 · cited 1× · see citing works
“Two genetically identified populations were found to correspond to the previously described magnocellular and parvocellular neurons (Alheid, 2003).”
ResultDAVIS, M., & SHI, C. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb09273.x · Cited by 328 · cited 1× · see citing works
“This may synthesize apparently conflicting studies reporting the role of 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…”
Amygdala inputs to prefrontal cortex guide behavior amid conflicting cues of reward and punishment
Burgos-Robles, A., Kimchi, E. Y., Izadmehr, E. M., Porzenheim, M. J., Ramos-Guasp, W. A., Nieh, E. H., Felix-Ortiz, A. C., Namburi, P., Leppla, C. A., Presbrey, K. N., et al. (2017) · Nature Neuroscience · doi:10.1038/nn.4553 · Cited by 318 · cited 2× · see citing works
“Defining BLA populations by projection target has revealed functional divergences in valence coding (Beyeler et al., 2016;Burgos-Robles et al., 2017; Felix-Ortiz et al., 2013, 2016; Namburi et al., 2015; Stuber et al., 2011; Tye et al., 2011).”
BackgroundMethodHomeostatic circuits selectively gate food cue responses in insular cortex
Livneh, Y., Ramesh, R. N., Burgess, C. R., Levandowski, K. M., Madara, J. C., Fenselau, H., Goldey, G. J., Diaz, V. E., Jikomes, N., Resch, J. M., et al. (2017) · Nature · doi:10.1038/nature22375 · Cited by 316 · cited 2× · see citing works
“…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., 2011) versus appetitive or anxiolytic behaviors (Corbit and Balleine, 2005;…”
BackgroundIntegrated Control of Predatory Hunting by the Central Nucleus of the Amygdala
Han, W., Téllez, L. A., Rangel, M. J., Motta, S. C., Zhang, X., Pérez-Martínez, I. O., Canteras, N. S., Shammah‐Lagnado, S. J., van den Pol, A. N., & de Araújo, I. E. (2017) · Cell · doi:10.1016/j.cell.2016.12.027 · Cited by 292 · cited 2× · see citing works
“…and Maren, 2009; Li et al., 2013; Maren and Quirk, 2004; Penzo et al., 2014; Sanford et al., 2017; Viviani et al., 2011) versus appetitive or anxiolytic behaviors (Corbit and Balleine, 2005; Hall et al., 2001; Han et al., 2017; Holland and Gallagher, 2003; Kim et al., 2017; Tye et al., 2011).”
BackgroundGore, F., Schwartz, E. C., Brangers, B. C., Aladi, S., Stujenske, J. M., Likhtik, E., Russo, M. J., Gordon, J. A., Salzman, C. D., & Axel, R. (2015) · Cell · doi:10.1016/j.cell.2015.06.027 · Cited by 256 · cited 4× · see citing works
“Several studies focused on valence encoding in the BLA have reported data that are indirectly suggestive of intermingled populations (Gore et al., 2015; Namburi et al., 2015).”
BackgroundMethodInfluentialCanine Adenovirus Vectors: an Alternative for Adenovirus-Mediated Gene Transfer
Kremer, E. J., Boutin, S., Chillón, M., & Danos, O. (2000) · Journal of Virology · doi:10.1128/jvi.74.1.505-512.2000 · Cited by 245 · cited 1× · see citing works
“Finally, we sought to view the 3-dimensional BLA circuitry in the intact brain by expressing a cre-dependent fluorophore into the BLA and the retrogradely traveling canine adenovirus 2 (CAV2-cre), which allowed for the expression of cre recombinase (Kremer et al., 2000).”
MethodHolland, P. C., & Gallagher, M. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02585.x · Cited by 236 · cited 2× · see citing works
“…and Maren, 2009; Li et al., 2013; Maren and Quirk, 2004; Penzo et al., 2014; Sanford et al., 2017; Viviani et al., 2011) versus appetitive or anxiolytic behaviors (Corbit and Balleine, 2005; Hall et al., 2001; Han et al., 2017; Holland and Gallagher, 2003; Kim et al., 2017; Tye et al., 2011).”
BackgroundWilensky, A. E., Schafe, G. E., & LeDoux, J. E. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-24-j0006.1999 · Cited by 217 · cited 2× · see citing works
“The basolateral amygdala (BLA) complex, including the lateral amygdala (LA) and the basal amygdala (BA), receives dense sensory inputs and is necessary for the acquisition of fear conditioning (Fanselow and Kim, 1994; LeDoux et al., 1990; Maren and Quirk, 2004; Miserendino et al., 1990; Wilensky et al., 1999) and rewa…”
BackgroundRapid strengthening of thalamo-amygdala synapses mediates cue–reward learning
Tye, K. M., Stuber, G. D., de Ridder, B., Bonci, A., & Janak, P. H. (2008) · Nature · doi:10.1038/nature06963 · Cited by 216 · cited 1× · see citing works
“…inputs and is necessary for the acquisition of fear conditioning (Fanselow and Kim, 1994; LeDoux et al., 1990; Maren and Quirk, 2004; Miserendino et al., 1990; Wilensky et al., 1999) and reward associations (Baxter and Murray, 2002; Cador et al., 1989; Cardinal et al., 2002; Tye et al., 2008).”
BackgroundSelf-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 · cited 2× · see citing works
“This may synthesize apparently conflicting studies reporting the role of 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 a…”
BackgroundShabel, S. J., & Janak, P. H. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0905580106 · Cited by 190 · cited 2× · see citing works
“Ce This is an open access article under the CC BY-N positive and negative valence (Beyeler et al., 2016; Fuster and Uyeda, 1971; Paton et al., 2006; Shabel and Janak, 2009).”
BackgroundPenzo, M. A., Robert, V., & Li, B. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.4166-13.2014 · Cited by 187 · cited 2× · see citing works
“This may synthesize apparently conflicting studies reporting the role of 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 a…”
BackgroundThalamic Regulation of Sucrose Seeking during Unexpected Reward Omission
Monte, F. H. D., Minier-Toribio, A. M., Quiñones-Laracuente, K., Medina-Colón, E. M., & Quirk, G. J. (2017) · Neuron · doi:10.1016/j.neuron.2017.03.036 · Cited by 178 · cited 2× · see citing works
“…studies and conditions may be related to the relatively restricted network that this population recruits and that this may be flexible depending on the internal state signaled by sources such as the paraventricular thalamic input (Do-Monte et al., 2017; Haight et al., 2017; Livneh et al., 2017).”
BackgroundArchitectural Representation of Valence in the Limbic System
Namburi, P., Al‐Hasani, R., Calhoon, G. G., Bruchas, M. R., & Tye, K. M. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.358 · Cited by 133 · cited 4× · see citing works
“Another experimental difference is that we quantified responses of individual neurons to stimuli of both positive and negative valence to meet criteria for valence encoding (Namburi et al., 2016).”
BackgroundInfluentialDifferential Recruitment of Competing Valence-Related Amygdala Networks during Anxiety
Lee, S., Amir, A., Haufler, D., & Paré, D. (2017) · Neuron · doi:10.1016/j.neuron.2017.09.002 · Cited by 87 · cited 1× · see citing works
“Altogether, these findings are consistent with evidence that reward- and threat-predicting cues recruit distinct subsets of BLA neurons (Lee et al., 2017).”
ResultReactivity of limbic neurons of the monkey to appetitive and aversive signals.
Fuster, J., & Uyeda, A. A. (1971) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(71)90111-8 · Cited by 85 · cited 2× · see citing works
“Ce This is an open access article under the CC BY-N positive and negative valence (Beyeler et al., 2016; Fuster and Uyeda, 1971; Paton et al., 2006; Shabel and Janak, 2009).”
BackgroundPrediction of economic choice by primate amygdala neurons
Fabian Grabenhorst, B., Hernádi, I., & Schultz, W. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1212706109 · Cited by 78 · cited 2× · see citing works
“908 Cell Reports 22, 905–918, January 23, 2018 only valence coding properties but also information including action selection (go or no-go) and prediction error (correct or error) (Grabenhorst et al., 2012; Baxter et al., 2000; Schoenbaum et al., 1999).”
BackgroundFunctional Circuits and Anatomical Distribution of Response Properties in the Primate Amygdala
Zhang, W., Schneider, D. M., Belova, M. A., Morrison, S. E., Paton, J. J., & Salzman, C. D. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2970-12.2013 · Cited by 74 · cited 3× · see citing works
“In line with previous electrophysiological studies, we observed that the distribution of positive and negative valence coding neurons, as described by their preferential response to cues predicting a positive or a negative outcome, was intermingled in the BLA (Zhang et al., 2013).”
BackgroundResultInfluentialHaight, J. L., Fuller, Z. L., Fraser, K. M., & Flagel, S. B. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.10.043 · Cited by 54 · cited 2× · see citing works
“…studies and conditions may be related to the relatively restricted network that this population recruits and that this may be flexible depending on the internal state signaled by sources such as the paraventricular thalamic input (Do-Monte et al., 2017; Haight et al., 2017; Livneh et al., 2017).”
BackgroundNuclear disconnection within the amygdala reveals a direct pathway to fearPreprint
Jimenez, S. A., & Maren, S. (2009) · Learning & Memory · doi:10.1101/lm.1607109 · Cited by 48 · cited 2× · see citing works
“This may synthesize apparently conflicting studies reporting the role of 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 a…”
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Neurobiological links between stress and anxiety
Daviu, N., Bruchas, M. R., Moghaddam, B., Sandi, C., & Beyeler, A. (2019) · Neurobiology of Stress · doi:10.1016/j.ynstr.2019.100191 · Cited by 528 · see citing works
Identification of a prefrontal cortex-to-amygdala pathway for chronic stress-induced anxiety
Liu, W.-Z., Zhang, W., Zheng, Z.-H., Zou, J., Liu, X., Huang, S.-H., You, W.-J., He, Y., Zhang, J., Wang, X.-D., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-15920-7 · Cited by 454 · see citing works
An amygdalar neural ensemble that encodes the unpleasantness of pain
Corder, G. F., Ahanonu, B., Grewe, B. F., Wang, D., Schnitzer, M. J., & Scherrer, G. (2019) · Science · doi:10.1126/science.aap8586 · Cited by 406 · see citing works
Behavioral and neurobiological mechanisms of pavlovian and instrumental extinction learning
Bouton, M. E., Maren, S., & McNally, G. P. (2020) · Physiological Reviews · doi:10.1152/physrev.00016.2020 · Cited by 399 · see citing works
The neural mechanisms and circuitry of the pair bond
Walum, H., & Young, L. J. (2018) · Nature Reviews Neuroscience · doi:10.1038/s41583-018-0072-6 · Cited by 353 · see citing works
Heterogeneity within classical cell types is the rule: lessons from hippocampal pyramidal neurons
Cembrowski, M. S., & Spruston, N. (2019) · Nature Reviews Neuroscience · doi:10.1038/s41583-019-0125-5 · Cited by 258 · see citing works
Neural Circuit Motifs in Valence Processing
Tye, K. M. (2018) · Neuron · doi:10.1016/j.neuron.2018.10.001 · Cited by 247 · see citing works
The coding of valence and identity in the mammalian taste system
Wang, L., Gillis-Smith, S., Peng, Y., Zhang, J., Chen, X., Salzman, C. D., Ryba, N. J. P., & Zuker, C. S. (2018) · Nature · doi:10.1038/s41586-018-0165-4 · Cited by 242 · see citing works
Oxytocin Signaling in the Central Amygdala Modulates Emotion Discrimination in Mice
Ferretti, V., Maltese, F., Contarini, G., Nigro, M., Bonavia, A., Huang, H., Gigliucci, V., Morelli, G., Scheggia, D., Managò, F., et al. (2019) · Current Biology · doi:10.1016/j.cub.2019.04.070 · Cited by 212 · see citing works
“Projection-specific manipulations dissecting CeA connectivity, as previously reported [114, 115], could help to elucidate how CeA neurons process stimuli of positive or negative valence to direct behavior.”
BackgroundState-specific gating of salient cues by midbrain dopaminergic input to basal amygdala
Lutas, A., Kucukdereli, H., Alturkistani, O., Carty, C., Sugden, A. U., Fernando, K., Diaz, V. E., Flores-Maldonado, V., & Andermann, M. L. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0506-0 · Cited by 166 · see citing works
Distinct Cortical-Thalamic-Striatal Circuits through the Parafascicular Nucleus
Mandelbaum, G., Taranda, J., Haynes, T. M., Hochbaum, D. R., Huang, K. W., Hyun, M., Venkataraju, K. U., Straub, C., Wang, W., Robertson, K., et al. (2019) · Neuron · doi:10.1016/j.neuron.2019.02.035 · Cited by 177 · see citing works
Multi-dimensional coding by basolateral amygdala neurons
Kyriazi, P., Headley, D. B., & Pare, D. (2018) · Neuron · doi:10.1016/j.neuron.2018.07.036 · Cited by 130 · see citing works
“…neurons are treated as labeled lines for specific emotional behaviors and states, they are consistent with the fact that those variables are only partially correlated with anatomical position (Beyeler et al., 2018), projection target (Beyeler et al., 2016), or genetic profile (Kim et al., 2016).”
Orbitofrontal Circuits Control Multiple Reinforcement-Learning Processes
Groman, S. M., Keistler, C., Keip, A. J., Hammarlund, E., Dileone, R., Pittenger, C., Lee, D., & Taylor, J. R. (2019) · Neuron · doi:10.1016/j.neuron.2019.05.042 · Cited by 142 · see citing works
“, 2006), and emerging evidence indicates that separable neuronal populations encode positive or negative stimulus values (Paton et al., 2006; Morrison et al., 2011; Beyeler et al., 2018).”
BackgroundStress in Regulation of GABA Amygdala System and Relevance to Neuropsychiatric Diseases
Jie, F., Yin, G., Yang, W., Yang, M., Gao, S., Lv, J., & Li, B. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00562 · Cited by 139 · see citing works
Genetically identified amygdala–striatal circuits for valence-specific behaviors
Zhang, X., Guan, W., Yang, T., Furlan, A., Xiao, X., Yu, K., An, X., Galbavy, W., Ramakrishnan, C., Deisseroth, K., et al. (2021) · Nature Neuroscience · doi:10.1038/s41593-021-00927-0 · Cited by 126 · see citing works
An insular view of the social decision-making network
Rogers-Carter, M. M., & Christianson, J. P. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.06.005 · Cited by 121 · see citing works
“Abbreviations: MeA: Medial amygdala; AH: Anterior hypothalamus; VMH: Ventromedial hypothalamus; mPOA: Medial preoptic area; BNST: Bed nucleus stria terminalis; LS: Lateral septum; Hipp: Hippocampus; VTA: Ventral tegmental area; VP: Ventral pallidum; NAc: Nucleus accumbens core; PAG: Periaqueductal grey; BLA: Basolater…”
BackgroundInfluentialPopulation coding of valence in the basolateral amygdala
Zhang, X., & Li, B. (2018) · Nature Communications · doi:10.1038/s41467-018-07679-9 · Cited by 133 · see citing works
Sex differences in fear extinction
Velasco, E. R., Florido, A., Milad, M. R., & Andero, R. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.05.020 · Cited by 125 · see citing works
“Recent evidence points out additional functions of the amygdala, specifically the CeA, in valence assignment, feeding behavior, and rewardrelated actions that could render this structure, as an integrator of internal states promoting the engagement into different behaviors (Beyeler et al., 2018; Fadok et al., 2018; Gr…”
BackgroundConnectivity characterization of the mouse basolateral amygdalar complex
Hintiryan, H., Bowman, I., Johnson, D. L., Korobkova, L., Zhu, M., Khanjani, N., Gou, L., Gao, L., Yamashita, S., Bienkowski, M. S., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-22915-5 · Cited by 121 · see citing works
Input–output organization of the mouse claustrum
Zingg, B., Dong, H., Tao, H. W., & Zhang, L. I. (2018) · The Journal of Comparative Neurology · doi:10.1002/cne.24502 · Cited by 126 · see citing works
“Many of these regions have been shown to modulate their activity in response to rewarding or aversive stimuli or to cues that predict such outcomes (Beyeler et al., 2018; Burgos-Robles et al., 2017; Hangya, Ranade, Lorenc, & Kepecs, 2015; Jimenez et al., 2018; Matias, Lottem, Dugué, & Mainen, 2017; Zhu, Wienecke, Nach…”
BackgroundAn endocannabinoid-regulated basolateral amygdala–nucleus accumbens circuit modulates sociability
Folkes, O. M., Báldi, R., Kondev, V., Marcus, D. J., Hartley, N. D., Turner, B. D., Ayers, J. K., Baechle, J. J., Misra, M. P., Altemus, M., et al. (2020) · Journal of Clinical Investigation · doi:10.1172/jci131752 · Cited by 119 · see citing works
Valence coding in amygdala circuits
Pignatelli, M., & Beyeler, A. (2018) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2018.10.010 · Cited by 120 · see citing works
Grogans, S. E., Bliss‐Moreau, E., Buss, K. A., Clark, L. A., Fox, A. S., Keltner, D. J., Cowen, A., Kim, J. J., Kragel, P. A., MacLeod, C., et al. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105237 · Cited by 126 · see citing works
Neuronal types in the mouse amygdala and their transcriptional response to fear conditioning
Hochgerner, H., Singh, S., Tibi, M., Lin, Z., Skarbianskis, N., Admati, I., Ophir, O., Reinhardt, N., Netser, S., Wagner, S., et al. (2023) · Nature Neuroscience · doi:10.1038/s41593-023-01469-3 · Cited by 110 · see citing works
“In addition, their molecular identities correlated with different anterior–posterior distributions, which could link to previous findings that BLA principal cells along the anterior–posterior axis encode opposing valences 5,11,52 .”
BackgroundEndocannabinoid Signaling Collapse Mediates Stress-Induced Amygdalo-Cortical Strengthening
Marcus, D. J., Bedse, G., Gaulden, A. D., Ryan, J. D., Kondev, V., Winters, N. D., Rosas-Vidal, L. E., Altemus, M., Mackie, K., Lee, F. S., et al. (2020) · Neuron · doi:10.1016/j.neuron.2019.12.024 · Cited by 104 · see citing works
Cortico-Limbic Interactions Mediate Adaptive and Maladaptive Responses Relevant to Psychopathology
Kovner, R., Oler, J., & Kalin, N. (2019) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2019.19101064 · Cited by 94 · see citing works
Neurotensin orchestrates valence assignment in the amygdala
Li, H., Namburi, P., Olson, J. M., Borio, M., Lemieux, M., Beyeler, A., Calhoon, G. G., HitoraーImamura, N., Coley, A. A., Libster, A. M., et al. (2022) · Nature · doi:10.1038/s41586-022-04964-y · Cited by 82 · see citing works
“During associative learning, the basolateral complex of the amygdala (BLA) forms associations with positive or negative outcomes, as supported by evidence from neural recordings 2,3,12,13 , synaptic changes 1,14,15 and optogenetic manipulations 1,5,16,17 .”
Extensive and spatially variable within-cell-type heterogeneity across the basolateral amygdala
O’Leary, T. P., Sullivan, K. E., Wang, L., Clements, J., Lemire, A. L., & Cembrowski, M. S. (2020) · eLife · doi:10.7554/elife.59003 · Cited by 75 · see citing works
“, 2003), and topographical gradients of connectivity are present across the BLA (Beyeler et al., 2018).”
BackgroundMethodInfluentialMa, J., du Hoffmann, J., Kindel, M., Beas, B. S., Chudasama, Y., & Penzo, M. A. (2021) · Nature Neuroscience · doi:10.1038/s41593-021-00912-7 · Cited by 83 · see citing works
Distinct serotonergic pathways to the amygdala underlie separate behavioral features of anxiety
Yu, X., Zhu, Y., Sun, Q., Deng, F., Wan, J., Zheng, D., Gong, W., Xie, S., Shen, C.-J., Fu, J., et al. (2022) · Nature Neuroscience · doi:10.1038/s41593-022-01200-8 · Cited by 83 · see citing works
Nucleus Accumbens Cell Type- and Input-Specific Suppression of Unproductive Reward Seeking
Lafferty, C. K., Yang, A. K., Mendoza, J. A., & Britt, J. P. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.02.095 · Cited by 76 · see citing works
Levine, O. B., Skelly, M. J., Miller, J. D., Rivera-Irizarry, J. K., Rowson, S. A., DiBerto, J. F., Rinker, J. A., Thiele, T. E., Kash, T. L., & Pleil, K. E. (2021) · Nature Communications · doi:10.1038/s41467-021-25368-y · Cited by 78 · see citing works
Amygdala-cortical collaboration in reward learning and decision making
Wassum, K. M. (2022) · eLife · doi:10.7554/elife.80926 · Cited by 76 · see citing works
Zhang, W., Liu, W.-Z., He, Y., You, W.-J., Zhang, J., Xu, H. A., Tian, X.-L., Li, B., Mei, L., Holmes, A., et al. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.12.010 · Cited by 72 · see citing works
Arbitration of Approach-Avoidance Conflict by Ventral Hippocampus
Bryant, K. G., & Barker, J. M. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.615337 · Cited by 72 · see citing works
“One interesting aspect of the PFC and BLA targets, specifically, is that a substantial portion of vHPC neurons project to both regions and have been found to be important in encoding fear contexts (Ishikawa and Nakamura, 2006; Jin and Maren, 2015).”
BackgroundInfluentialDistinct reward processing by subregions of the nucleus accumbens
Chen, G., Lai, S., Bao, G., Ke, J., Meng, X., Lu, S., Wu, X., Xu, H. Z., Wu, F., Xu, Y., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112069 · Cited by 69 · see citing works
The central amygdala recruits mesocorticolimbic circuitry for pursuit of reward or pain
Warlow, S. M., Naffziger, E. E., & Berridge, K. C. (2020) · Nature Communications · doi:10.1038/s41467-020-16407-1 · Cited by 75 · see citing works
Motivational competition and the paraventricular thalamus
McNally, G. P. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.02.021 · Cited by 74 · see citing works
Neuronal diversity of the amygdala and the bed nucleus of the stria terminalis
Beyeler, A., & Dabrowska, J. (2020) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-815134-1.00003-9 · Cited by 65 · see citing works
“Notably, in mice, BLA-CeM projectors are densest in LA compared to BLA-NAc and BLA-vHPC cells and are mainly lateral in the BA, which is the opposing topographic pattern of BLANAc neurons, which have an opposing role in valence (Beyeler et al., 2018).”
BackgroundMethodInfluentialAn Amygdala Circuit Mediates Experience-Dependent Momentary Arrests during Exploration
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 · see citing works
“Furthermore, we calculated the preference ratio between the entrances to ROIon and ROIoff and found no significant difference between the control and Jaws group during the probe test in day 6 (Figure 5F), again suggesting that the manipulation that affected exploratory arrests based on spatial/behavioral experience di…”
Stress-induced plasticity of a CRH/GABA projection disrupts reward behaviors in mice
Birnie, M. T., Short, A. K., de Carvalho, G., Taniguchi, L., Gunn, B. G., Pham, A. L., Itoga, C. A., Xu, X., Chen, L. Y., Mahler, S. V., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-36780-x · Cited by 64 · see citing works
Piantadosi, S. C., Zhou, Z. C., Pizzano, C., Pedersen, C. E., Nguyen, T. K., Thai, S., Stuber, G. D., & Bruchas, M. R. (2023) · Neuron · doi:10.1016/j.neuron.2023.11.007 · Cited by 64 · see citing works
Intermingled Ensembles in Visual Association Cortex Encode Stimulus Identity or Predicted Outcome
Ramesh, R. N., Burgess, C. R., Sugden, A. U., Gyetvan, M., & Andermann, M. L. (2018) · Neuron · doi:10.1016/j.neuron.2018.09.024 · Cited by 64 · see citing works
“Intermingled neurons in the rodent and primate amygdala encode cues associated with positive or negative outcomes (Beyeler et al., 2018; Morrison and Salzman, 2010; O’Neill et al., 2018; Schoenbaum et al., 1998), and silencing or lesioning the amygdala affects behavioral responses to learned cues (Baxter and Murray, 2…”
Compartmentalized dendritic plasticity during associative learning
d‘Aquin, S., Szőnyi, A., Mahn, M., Krabbe, S., Gründemann, J., & Lüthi, A. (2022) · Science · doi:10.1126/science.abf7052 · Cited by 60 · see citing works
“Studies point to the importance of a neuron’s intrinsic excitability at the time ofmemory formation (45), its afferent inputs and/or output targets (18, 46, 47), the role of inhibitory interneurons (23, 24, 38), and the clustering of synaptic inputs along the dendritic arbor (38, 48).”
BackgroundA bidirectional corticoamygdala circuit for the encoding and retrieval of detailed reward memories
Sias, A. C., Morse, A. K., Wang, S. C., Greenfield, V. Y., Goodpaster, C. M., Wrenn, T. M., Wikenheiser, A. M., Holley, S. M., Cepeda, C., Levine, M. S., et al. (2021) · eLife · doi:10.7554/elife.68617 · Cited by 60 · see citing works
Valence encoding in the amygdala influences motivated behavior
Smith, D. M., & Torregrossa, M. M. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113370 · Cited by 60 · see citing works
Embracing Complexity in Defensive Networks
Headley, D. B., Kanta, V., Kyriazi, P., & Paré, D. (2019) · Neuron · doi:10.1016/j.neuron.2019.05.024 · Cited by 57 · see citing works
Erbin in Amygdala Parvalbumin-Positive Neurons Modulates Anxiety-like Behaviors
Luo, Z.-Y., Huang, L., Lin, S., Yin, Y., Jie, W., Hu, N.-Y., Hu, Y.-Y., Guan, Y., Liu, J., You, Q.-L., et al. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2019.10.021 · Cited by 58 · see citing works
The center of the emotional universe: Alcohol, stress, and CRF1 amygdala circuitry
Agoglia, A. E., & Herman, M. A. (2018) · Alcohol · doi:10.1016/j.alcohol.2018.03.009 · Cited by 53 · see citing works
“…negative association processing behind the acquisition and expression of conditioned fear (for review see Ehrlich 2009) and recent evidence suggests that amygdala microcircuits are also critical for the coding of both positive and negative-valence cues (Beyeler et al, 2018; Beyeler et al, Alcohol.”
BackgroundKim, J., Kang, S., Choi, T.-Y., Chang, K., & Koo, J. W. (2022) · Biological Psychiatry · doi:10.1016/j.biopsych.2022.01.006 · Cited by 55 · see citing works
Brain Mechanisms of Exercise-Induced Hypoalgesia: To Find a Way Out from “Fear-Avoidance Belief”
Kami, K., Tajima, F., & Senba, E. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23052886 · Cited by 52 · see citing works
“Therefore, the different neuronal types of the BLA, each with different projection targets, act to differentially control aversive and reward-related behaviors closely associated with pain and hypoalgesia, respectively [19].”
BackgroundWang, X.-Y., Xu, X., Chen, R., Jia, W.-B., Xu, P., Liu, X.-Q., Zhang, Y., Liu, X., & Zhang, Y. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.113170 · Cited by 49 · see citing works
“were all implicated in emotion encoding (43-48).”
Cell-Type- and Endocannabinoid-Specific Synapse Connectivity in the Adult Nucleus Accumbens Core
Deroche, M. A., Lassalle, O., Castell, L., Valjent, E., & Manzoni, O. J. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.1100-19.2019 · Cited by 48 · see citing works
“, 2008) and have a role in positive emotional valence (Beyeler et al., 2018).”
BackgroundKuniishi, H., Yamada, D., Wada, K., Yamada, M., & Sekiguchi, M. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-0837-3 · Cited by 47 · see citing works
Twining, R. C., Lepak, K., Kirry, A. J., & Gilmartin, M. R. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.1453-19.2020 · Cited by 48 · see citing works
“The VH receives valence-encoded information from both CS-responsive and appetitive UCS-responsive amygdala neurons (Beyeler et al., 2016, 2018), and VH neurons respond robustly to an aversive UCS (Weible et al., 2006).”
BackgroundTranslational opportunities for circuit-based social neuroscience: advancing 21st century psychiatry
Ford, C. L., & Young, L. J. (2021) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2020.11.007 · Cited by 46 · see citing works
“Moreover, these distinct clinical profiles and epigenetic biomarkers are also associated with alterations in resting state connectivity between areas critical for social cognition and behavior, such as the NAc, PFC, amygdala, and cingulate cortex.”
BackgroundInfluentialAn emotional-response model of bipolar disorders integrating recent findings on amygdala circuits
Bigot, M., Alonso, M., Houenou, J., Sarrazin, S., Dargél, A., Lledo, P., & Henry, C. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.07.037 · Cited by 42 · see citing works
“In a recent study, more than 1000 neurons were recorded in vivo during a Pavlovian task to map their spatial location in the BLA (Beyeler et al., 2018).”
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 44 · see citing works
Wang, Y., Liu, Z., Cai, L., Guo, R., Dong, Y., & Huang, Y. H. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2019.10.027 · Cited by 45 · see citing works
Unexpected Role of Physiological Estrogen in Acute Stress-Induced Memory Deficits
Hokenson, R. E., Short, A., Chen, Y., Pham, A. L., Adams, E. T., Bolton, J., Swarup, V., Gall, C., & Baram, T. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.2146-20.2020 · Cited by 36 · see citing works
“The number of MAS-induced fos(1) cells in the basolateral and medial amygdala, regions with monosynaptic connections to hippocampus (Pikkarainen et al., 1999; Petrovich et al., 2001; Beyeler et al., 2018), as well as the LS and the paraventricular nucleus of the thalamus, was selectivity increased in high estrogen fem…”
BackgroundMethodValence Encoding Signals in the Human Amygdala and the Willingness to Eat
Tiedemann, L. J., Alink, A., Beck, J., Büchel, C., & Brassen, S. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.2382-19.2020 · Cited by 41 · see citing works
“This fits with recent evidence in animals of topographically segregated neuron populations coding for positive and negative valence (Beyeler et al., 2016, 2018; Kim et al., 2016; O’Neill et al., 2018; Wang et al., 2018).”
BackgroundInfluentialThe interhemispheric amygdala-accumbens circuit encodes negative valence in mice
Tian, Z., Song, J., Zhao, X., Zhou, Y., Chen, X., Le, Q., Wang, F., Ma, L., & Liu, X. (2024) · Science · doi:10.1126/science.adp7520 · Cited by 41 · see citing works
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 38 · see citing works
Sharma, K., Kelly, E. A., Pfeifer, C. W., & Fudge, J. L. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhz106 · Cited by 39 · see citing works
“2014), there are abundant examples of collateral longrange projections in the rodent ( Sarter and Markowitsch 1984; Reichard et al. 2017; Beyeler et al. 2018; Han et al. 2018; Yamashita et al. 2018) and primate (Rockland 2013) brain.”
BackgroundAdvances in understanding meso‐cortico‐limbic‐striatal systems mediating risky reward seeking
Piantadosi, P. T., Halladay, L. R., Radke, A. K., & Holmes, A. (2021) · Journal of Neurochemistry · doi:10.1111/jnc.15342 · Cited by 37 · see citing works
“For example, molecularly distinct projection populations that contribute differently to positive and negative valence behaviors exist in the BLA (Beyeler et al., 2016, 2018; Kim, Zhang, et al., 2017; Shen et al., 2019) and other amygdala subregions (Hardaway et al., 2019; Janak & Tye, 2015; Miller…”
BackgroundInfluentialLiang, J., Chen, L., Li, Y., Chen, Y., Yuan, L., Qiu, Y., Ma, S., Fan, F., & Cheng, Y. (2024) · Schizophrenia Bulletin · doi:10.1093/schbul/sbae063 · Cited by 38 · see citing works
Valence processing in the PFC: Reconciling circuit-level and systems-level views
Coley, A. A., Padilla-Coreano, N., Patel, R. R., & Tye, K. M. (2021) · International review of neurobiology · doi:10.1016/bs.irn.2020.12.002 · Cited by 35 · see citing works
The emotion paradox in the aging body and brain
Mather, M. (2024) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.15138 · Cited by 34 · see citing works
High-Frequency Stimulation of Ventral CA1 Neurons Reduces Amygdala Activity and Inhibits Fear
Graham, J. A., D’Ambra, A. F., Jung, S. J., Teratani-Ota, Y., Vishwakarma, N., Venkatesh, R., Parigi, A. A., Antzoulatos, E. G., Fioravante, D., & Wiltgen, B. J. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.595049 · Cited by 35 · see citing works
Haaranen, M., Schäfer, A., Järvi, V., & Hyytiä, P. (2020) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2020.580849 · Cited by 35 · see citing works
Limoges, A., Yarur, H. E., & Tejeda, H. A. (2022) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2022.963691 · Cited by 33 · see citing works
“Further, the encoding of motivationally-relevant behaviors by the BLA may also be influenced by anterior-posterior gradients in reward and aversion neurons in the BLA and their outputs (Kim et al., 2016; Beyeler et al., 2018).”
BackgroundLesions of the rat basolateral amygdala reduce the behavioral response to ultrasonic vocalizations
Schönfeld, L.-M., Zech, M.-P., Schäble, S., Wöhr, M., & Kalenscher, T. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.112274 · Cited by 34 · see citing works
Serra, I., Esparza, J., Delgado, L., Martín-Monteagudo, C., Puigròs, M., Podlesniy, P., Trullás, R., & Navarrete, M. (2022) · Nature Communications · doi:10.1038/s41467-022-33020-6 · Cited by 34 · see citing works
Updating the striatal–pallidal wiring diagram
Fang, L. Z., & Creed, M. C. (2023) · Nature Neuroscience · doi:10.1038/s41593-023-01518-x · Cited by 33 · see citing works
Characterizing Different Strategies for Resolving Approach-Avoidance Conflict
Bravo-Rivera, H., Arzola, P. R., Caban, A. J., Vélez-Avilés, A. N., Ayala-Rosario, S. N., & Quirk, G. J. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.608922 · Cited by 33 · see citing works
Regional synapse gain and loss accompany memory formation in larval zebrafish
Dempsey, W. P., Du, Z., Nadtochiy, A., Smith, C. D., Czajkowski, K., Andreev, A., Robson, D. N., Li, J., Applebaum, S. S., Truong, T. V., et al. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2107661119 · Cited by 30 · see citing works
Synchronicity: The Role of Midbrain Dopamine in Whole-Brain Coordination
Beeler, J. A., & Dreyer, J. K. (2019) · eNeuro · doi:10.1523/eneuro.0345-18.2019 · Cited by 31 · see citing works
“The amygdala forms a model of the valence of stimuli in relation to the organism (Beyeler et al., 2018; O’Neill et al., 2018; Pryce, 2018).”
BackgroundUnderstanding the heterogeneity of anxiety using a translational neuroscience approach
Drzewiecki, C. M., & Fox, A. S. (2024) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-024-01162-3 · Cited by 33 · see citing works
“Critically, different cell types are not uniformly distributed within regions (Beyeler et al., 2018; McCullough et al., 2018), and different voxels likely reflect distinct compositions of Ce cell types.”
BackgroundMorgan, A., Kondev, V., Bedse, G., Báldi, R., Marcus, D. J., & Patel, S. (2019) · Neurobiology of Stress · doi:10.1016/j.ynstr.2019.100190 · Cited by 31 · see citing works
Manoocheri, K., & Carter, A. G. (2022) · eLife · doi:10.7554/elife.82688 · Cited by 32 · see citing works
“There is likely additional diversity in these circuits, as gradients in cell types and projection targets are also observed in the medial-lateral and ventral–dorsal axes of the BLA ( McGarry and Carter, 2017 ; Beyeler et al., 2018 ; O’Leary et al., 2020 ).”
Review of EEG Affective Recognition with a Neuroscience Perspective
Lim, R., Lew, W.-C. L., & Kai, K.-A. (2024) · Brain Science · doi:10.3390/brainsci14040364 · Cited by 33 · see citing works
“For instance, the amygdala, conventionally found to be activated in the presence of fear-associated stimuli, has recently been proven to function as valence-encoding nuclei via various chemogenetic and optogenetic experiments in animal model studies [42–45].”
BackgroundAstrocyte ensembles manipulated with AstroLight tune cue-motivated behavior
Serra, I., Martín-Monteagudo, C., Romero, J. S., Quintanilla, J. P., Ganchala, D., Arévalo, M., García‐Marqués, J., & Navarrete, M. (2025) · Nature Neuroscience · doi:10.1038/s41593-025-01870-0 · Cited by 31 · see citing works
“Given that optostimulation of ChR2 leads to non-selective cation flow through the plasma membrane 9,16,17 and that astrocyte activity is primarily based on Ca 2+ variations, we specifically targeted Ca 2+ using designer receptors exclusively activated by designer drugs (DREADDs) coupled to G q…”
Optimizing Calcium Detection Methods in Animal Systems: A Sandbox for Synthetic Biology
Li, E. S., & Saha, M. S. (2021) · Biomolecules · doi:10.3390/biom11030343 · Cited by 31 · see citing works
“Rather than trying to manipulate the neuronal activity, the intention of this method is to trigger APs when short light pulses are applied to the transduced cells, thus identifying the neuronal population for later monitoring of natural activity [159].”
BackgroundThe basolateral amygdala to lateral septum circuit is critical for regulating social novelty in mice
Rodriguez, L. A., Kim, S.-H., Page, S. C., Nguyen, C. V., Pattie, E. A., Hallock, H. L., Valerino, J., Maynard, K. R., Jaffe, A. E., & Martinowich, K. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-022-01487-y · Cited by 31 · see citing works
“DISCUSSION BLA projections to the LS control social novelty The BLA is critical for valence processing in a variety of contexts [58, 59], a function that may extend to processing social stimuli [60].”
BackgroundAn amygdala-to-cingulate cortex circuit for conflicting choices in chronic pain
Valentinova, K., Acuña, M. A., Ntamati, N. R., Nevian, N. E., & Nevian, T. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.113125 · Cited by 32 · see citing works
“Furthermore, chemogenetic activation of the BLA-ACC projection induces avoidance in pain-free animals, while chemo-genetic inhibition or LFS of the BLA-ACC projection in vivo reba-lances approach-avoidance choices of neuropathic animals when facing conflicts.”
Kuniishi, H., Nakatake, Y., Sekiguchi, M., & Yamada, M. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-022-01358-6 · Cited by 30 · see citing works
“Interestingly, several studies have demonstrated that neurons in the medial and dorsal BLA preferentially project to the nucleus accumbens, involved in reward and social processing, while neurons in the lateral and ventral BLA project to the central amygdala, involved in aversive behaviours [67, 73, 75].”
BackgroundRobinson, S. L., & Thiele, T. E. (2020) · Neuropharmacology · doi:10.1016/j.neuropharm.2020.107983 · Cited by 30 · see citing works
“As the anterior and posterior amygdala have been shown to differentially contribute to valence coding of positive and negative stimuli, this gradient may suggest a similarly differential role of SST+ cells in these processes (Beyeler et al., 2018).”
BackgroundHan, R.-W., Zhang, Z., Chen, J., Hu, Z.-Y., & Pan, B. (2024) · Nature Communications · doi:10.1038/s41467-024-47966-2 · Cited by 28 · see citing works
An Honest Reckoning With the Amygdala and Mental Illness
Fox, A. S., & Shackman, A. J. (2024) · American Journal of Psychiatry · doi:10.1176/appi.ajp.20240941 · Cited by 26 · see citing works
Canine Adenovirus 2: A Natural Choice for Brain Circuit Dissection
Lavoie, A., & Liu, B. (2020) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2020.00009 · Cited by 24 · see citing works
Sonkusare, S., Nguyen, V. T., Moran, R., van der Meer, J. N., Ren, Y., Koussis, N. C., Dionisio, S. A., Breakspear, M. J., & Guo, C. C. (2020) · Cortex · doi:10.1016/j.cortex.2020.05.018 · Cited by 28 · see citing works
Neural Oscillations in Aversively Motivated Behavior
Totty, M. S., & Maren, S. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.936036 · Cited by 26 · see citing works
Inhibition of Pyramidal Neurons in the Basal Amygdala Promotes Fear Learning
Tipps, M. E., de Velasco, E. M. F., Schaeffer, A., & Wickman, K. D. (2018) · eNeuro · doi:10.1523/eneuro.0272-18.2018 · Cited by 24 · see citing works
“Similarly, the afferent and efferent connections of pyramidal neurons in the BLA complex are diverse, and these distinctions have significant implications for both conditioned fear and anxiety (Janak and Tye, 2015; Beyeler et al., 2016, 2018; BurgosRobles et al., 2017).”
BackgroundKami, K., Tajima, F., & Senba, E. (2020) · Molecular Pain · doi:10.1177/1744806920971377 · Cited by 25 · see citing works
Nowlan, A. C., Choe, J., Tromblee, H., Kelahan, C., Hellevik, K., & Shea, S. D. (2024) · Current Biology · doi:10.1016/j.cub.2024.10.078 · Cited by 25 · see citing works
Smith, P. H., Uhlrich, D. J., & Manning, K. (2019) · The Journal of Comparative Neurology · doi:10.1002/cne.24644 · Cited by 25 · see citing works
“(Beyeler et al., 2018; Kim, Pignatelli, Xu, Itohara, & Tonegawa, 2016; Kim, Zhang, Muralidhar, LeBlanc, & Tonegawa, 2017; Namburi et al., 2015).”
Neural Coding of Thermal Preferences in the NematodeCaenorhabditis elegans
Matsuyama, H. J., & Mori, I. (2020) · eNeuro · doi:10.1523/eneuro.0414-19.2020 · Cited by 24 · see citing works
Dieterich, A., Floeder, J. R., Stech, K., Lee, J., Srivastava, P., Barker, D. J., & Samuels, B. A. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.643272 · Cited by 22 · see citing works
Keller, N. E., Hennings, A. C., Leiker, E., Lewis‐Peacock, J. A., & Dunsmoor, J. E. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.0075-22.2022 · Cited by 27 · see citing works
Feasibility and utility of amygdala neurofeedback
Goldway, N., Jalon, I., Keynan, J. N., Hellrung, L., Horstmann, A., Paret, C., & Hendler, T. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104694 · Cited by 24 · see citing works
- Authors
- Beyeler, A., Chang, C.-J., Silvestre, M., Lévêque, C., Namburi, P., Wildes, C. P., & Tye, K. M.
- Affiliations
- Université de Bordeaux (FR)
- Massachusetts Institute of Technology (US)
- Corresponding author
- Beyeler, Anna
- Tye, Kay M.
- Venue
- Cell Reports
- Publisher
- Elsevier BV
- Published
- 2018-01
- Volume
- 22
- Issue
- 4
- Pages
- 905-918
- ISSN
- 2211-1247 (ISSN-L)
- PMC
- PMC5891824
- OpenAlex
- W2784903304
- Cited by
- 306
- References
- 58
- Citations by year
- 2026: 29 · 2025: 44 · 2024: 34 · 2023: 34 · 2022: 34 · 2021: 46 · 2020: 35 · 2019: 34 · 2018: 16
- FWCI
- 19.47
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Cell Reports (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion, cc-by-nc-nd)
- PubMed Central (acceptedVersion, cc-by-nc-nd)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc-nd)
- Funders
- National Institute of Diabetes and Digestive and Kidney Diseases
- Alfred P. Sloan Foundation
- Whitehall Foundation
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
- National Institute of Mental Health (DP2-DK-102256)
- JPB Foundation
- Klingenstein Third Generation Foundation
- National Institutes of Health (R01-MH102441)
- National Alliance for Research on Schizophrenia and Depression
- McKnight Foundation
- 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 › Neurotransmitter Receptor Influence on Behavior
- Keywords
- basolateral amygdala, positive and negative valence, nucleus accumbens, central amygdala, ventral hippocampus, clarity, emotional processing, neural circuit organization
- MeSH terms
- Amygdala, Animals, Male, Neurons, Mice, Basolateral Nuclear Complex
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