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Genetically identified amygdala–striatal circuits for valence-specific behaviors
Open accessAbstract
The basolateral amygdala (BLA) plays essential roles in behaviors motivated by stimuli with either positive or negative valence, but how it processes motivationally opposing information and participates in establishing valence-specific behaviors remains unclear. Here, by targeting Fezf2-expressing neurons in the BLA, we identify and characterize two functionally distinct classes in behaving mice, the negative-valence neurons and positive-valence neurons, which innately represent aversive and rewarding stimuli, respectively, and through learning acquire predictive responses that are essential for punishment avoidance or reward seeking. Notably, these two classes of neurons receive inputs from separate sets of sensory and limbic areas, and convey punishment and reward information through projections to the nucleus accumbens and olfactory tubercle, respectively, to drive negative and positive reinforcement. Thus, valence-specific BLA neurons are wired with distinctive input-output structures, forming a circuit framework that supports the roles of the BLA in encoding, learning and executing valence-specific motivated behaviors.
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Cites
Russell, J. A. (1980) · Journal of Personality and Social Psychology · doi:10.1037/h0077714 · Cited by 16,334
A robust and high-throughput Cre reporting and characterization system for the whole mouse brain
Madisen, L., Zwingman, T. A., Sunkin, S. M., Oh, S. W., Zariwala, H. A., Gu, H., Ng, L. L., Palmiter, R. D., Hawrylycz, M. J., Jones, A. R., et al. (2010) · Nature Neuroscience · doi:10.1038/nn.2467 · Cited by 6,907
Ultrasensitive fluorescent proteins for imaging neuronal activity
Chen, T.-W., Wardill, T. J., Sun, Y., Pulver, S. R., Renninger, S. L., Baohan, A., Schreiter, E. R., Kerr, R. A., Orger, M. B., Jayaraman, V., et al. (2013) · Nature · doi:10.1038/nature12354 · Cited by 6,474
From motivation to action: Functional interface between the limbic system and the motor system
MOGENSON, G., JONES, D., & YIM, C. (1980) · Progress in Neurobiology · doi:10.1016/0301-0082(80)90018-0 · Cited by 2,331
From circuits to behaviour in the amygdala
Janak, P. H., & Tye, K. M. (2015) · Nature · doi:10.1038/nature14188 · Cited by 2,011
A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex
Taniguchi, H., He, M., Wu, P., Kim, S., Paik, R., Sugino, K., Kvitsani, D., Fu, Y., Lu, J., Lin, Y., et al. (2011) · Neuron · doi:10.1016/j.neuron.2011.07.026 · Cited by 1,828
Self-citationWhole-Brain Mapping of Direct Inputs to Midbrain Dopamine Neurons
Watabe‐Uchida, M., Zhu, L., Ogawa, S. K., Vamanrao, A., & Uchida, N. (2012) · Neuron · doi:10.1016/j.neuron.2012.03.017 · Cited by 1,275
Dimensionality reduction for large-scale neural recordings
Cunningham, J. P., & Yu, B. M. (2014) · Nature Neuroscience · doi:10.1038/nn.3776 · Cited by 1,219
The neocortical circuit: themes and variations
Harris, K. D., & Shepherd, G. M. G. (2015) · Nature Neuroscience · doi:10.1038/nn.3917 · Cited by 1,215
Circuit architecture of VTA dopamine neurons revealed by systematic input-output mapping
Beier, K. T., Steinberg, E. E., DeLoach, K. E., Xie, S., Miyamichi, K., Schwarz, L., Gao, X. J., Kremer, E. J., Malenka, R. C., & Luo, L. (2015) · Cell · doi:10.1016/j.cell.2015.07.015 · Cited by 1,068
The subcellular organization of neocortical excitatory connections
Petreanu, L., Mao, T., Sternson, S. M., & Svoboda, K. (2009) · Nature · doi:10.1038/nature07709 · Cited by 1,047
Simultaneous Denoising, Deconvolution, and Demixing of Calcium Imaging Data
Pnevmatikakis, E. A., Soudry, D., Gao, Y., Machado, T. A., Merel, J., Pfau, D., Reardon, T. R., Mu, Y., Lacefield, C., Yang, W., et al. (2016) · Neuron · doi:10.1016/j.neuron.2015.11.037 · Cited by 1,022
The primate amygdala represents the positive and negative value of visual stimuli during learning
Paton, J. J., Belova, M. A., Morrison, S. E., & Salzman, C. D. (2006) · Nature · doi:10.1038/nature04490 · Cited by 917
Excitatory transmission from the amygdala to nucleus accumbens facilitates reward seeking
Stuber, G. D., Sparta, D. R., Stamatakis, A. M., van Leeuwen, W. A., Hardjoprajitno, J. E., Cho, S., Tye, K. M., Kempadoo, K. A., Zhang, F., Deisseroth, K., et al. (2011) · Nature · doi:10.1038/nature10194 · Cited by 878
Self-citationIntact-brain analyses reveal distinct information carried by SNc dopamine subcircuits
Lerner, T. N., Shilyansky, C., Davidson, T. J., Evans, K. E., Beier, K. T., Zalocusky, K. A., Crow, A. K., Malenka, R. C., Luo, L., Tomer, R., et al. (2015) · Cell · doi:10.1016/j.cell.2015.07.014 · Cited by 794
Self-citationWhy neurons mix: high dimensionality for higher cognition
Fusi, S., Miller, E. K., & Rigotti, M. (2016) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2016.01.010 · Cited by 766
Viral-genetic tracing of the input-output organization of a central noradrenaline circuit
Schwarz, L. A., Miyamichi, K., Gao, X. J., Beier, K. T., Weissbourd, B., DeLoach, K. E., Ren, J., Ibanes, S., Malenka, R. C., Kremer, E. J., et al. (2015) · Nature · doi:10.1038/nature14600 · Cited by 744
Efficient and accurate extraction of in vivo calcium signals from microendoscopic video data
Zhou, P., Resendez, S. L., Rodríguez-Romaguera, J., Jimenez, J., Neufeld, S. Q., Giovannucci, A., Friedrich, J. H., Pnevmatikakis, E. A., Stuber, G. D., Hen, R., et al. (2018) · eLife · doi:10.7554/elife.28728 · Cited by 737
Synaptic 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
Natural light-gated anion channels: A family of microbial rhodopsins for advanced optogenetics
Govorunova, E. G., Sineshchekov, O. A., Janz, R., Liu, X., & Spudich, J. L. (2015) · Science · doi:10.1126/science.aaa7484 · Cited by 699
A 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
The learning curve: implications of a quantitative analysis.
Gallistel, C., Fairhurst, S. P., & Balsam, P. (2004) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.0404965101 · Cited by 587
Targeting cells with single vectors using multiple-feature Boolean logic
Fenno, L. E., Mattis, J., Ramakrishnan, C., Hyun, M., Lee, S. Y., He, M., Tucciarone, J., Selimbeyoglu, A., Berndt, A., Grosenick, L., et al. (2014) · Nature Methods · doi:10.1038/nmeth.2996 · Cited by 557
Self-citationBidirectional 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
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
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 467
Self-citationAntagonistic 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 464
Divergent 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
Emotion, motivation, and the brain: Reflex foundations in animal and human research
Lang, P. J., & Davis, M. (2006) · Progress in Brain Research · doi:10.1016/s0079-6123(06)56001-7 · Cited by 410
A New DREADD Facilitates the Multiplexed Chemogenetic Interrogation of Behavior
Vardy, E., Robinson, J. E., Li, C., Olsen, R. H. J., DiBerto, J. F., Giguère, P. M., Sassano, F. M., Huang, X., Zhu, H., Urban, D. J., et al. (2015) · Neuron · doi:10.1016/j.neuron.2015.03.065 · Cited by 398
Tracking the Same Neurons across Multiple Days in Ca2+ Imaging Data
Sheintuch, L., Rubin, A., Brande-Eilat, N., Geva, N., Sadeh, N., Pinchasof, O., & Ziv, Y. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.10.013 · Cited by 392
Strategies and Tools for Combinatorial Targeting of GABAergic Neurons in Mouse Cerebral Cortex
He, M., Tucciarone, J., Lee, S., Nigro, M. J., Kim, Y., Levine, J. M., Kelly, S. M., Krugikov, I., Wu, P., Chen, Y., et al. (2016) · Neuron · doi:10.1016/j.neuron.2016.08.021 · Cited by 339
Self-citationRabies Virus CVS-N2c ΔG Strain Enhances Retrograde Synaptic Transfer and Neuronal Viability
Reardon, T. R., Murray, A., Turi, G. F., Wirblich, C., Croce, K. R., Schnell, M. J., Jessell, T. M., & Losonczy, A. (2016) · Neuron · doi:10.1016/j.neuron.2016.01.004 · Cited by 313
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 concepts of the ventral striatopallidal system and extended amygdala
DE OLMOS, J. S., & HEIMER, L. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb09258.x · Cited by 281
Amygdala Reward Neurons Form and Store Fear Extinction Memory
Zhang, X., Kim, J., & Tonegawa, S. (2019) · Neuron · doi:10.1016/j.neuron.2019.12.025 · Cited by 280
Self-citationHigh-efficiency optogenetic silencing with soma-targeted anion-conducting channelrhodopsins
Mahn, M., Gibor, L., Patil, P., Malina, K. C.-K., Oring, S., Printz, Y., Levy, R., Lampl, I., & Yizhar, O. (2018) · Nature Communications · doi:10.1038/s41467-018-06511-8 · Cited by 279
Cell-Type-Based Analysis of MicroRNA Profiles in the Mouse Brain
He, M., Liu, Y., Wang, X., Zhang, M. Q., Hannon, G. J., & Huang, Z. J. (2012) · Neuron · doi:10.1016/j.neuron.2011.11.010 · Cited by 277
Self-citationGore, 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 276
Neural Circuit Motifs in Valence Processing
Tye, K. M. (2018) · Neuron · doi:10.1016/j.neuron.2018.10.001 · Cited by 268
Shen, C.-J., Zheng, D., Li, K., Yang, J., Pan, H., Yu, X.-D., Fu, J., Zhu, Y., Sun, Q.-X., Tang, M., et al. (2019) · Nature Medicine · doi:10.1038/s41591-018-0299-9 · Cited by 231
A basal ganglia circuit for evaluating action outcomes
Stephenson‐Jones, M., Yu, K., Ahrens, S., Tucciarone, J., van Huijstee, A. N., Mejia, L. A., Penzo, M. A., Tai, L.-H., Wilbrecht, L., & Li, B. (2016) · Nature · doi:10.1038/nature19845 · Cited by 224
Self-citationWesson, D. W., & Wilson, D. A. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.08.004 · Cited by 208
Active Avoidance Requires a Serial Basal Amygdala to Nucleus Accumbens Shell Circuit
Ramirez, F., Moscarello, J. M., LeDoux, J. E., & Sears, R. M. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.1331-14.2015 · Cited by 198
Involvement of the Olfactory Tubercle in Cocaine Reward: Intracranial Self-Administration Studies
Ikemoto, S. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-28-09305.2003 · Cited by 188
The role of amygdala nuclei in the expression of auditory signaled two-way active avoidance in rats.
Choi, J.-S., Cain, C. K., & LeDoux, J. E. (2010) · Learning & Memory · doi:10.1101/lm.1676610 · Cited by 187
The central amygdala controls learning in the lateral amygdala
Yu, K., Ahrens, S., Zhang, X., Schiff, H. C., Ramakrishnan, C., Fenno, L. E., Deisseroth, K. A., Zhao, F., Luo, M., Gong, L., et al. (2017) · Nature Neuroscience · doi:10.1038/s41593-017-0009-9 · Cited by 185
Self-citationStephenson‐Jones, M., Bravo-Rivera, C., Ahrens, S., Furlan, A., Xiao, X., Fernandes-Henriques, C., & Li, B. (2020) · Neuron · doi:10.1016/j.neuron.2019.12.006 · Cited by 165
Self-citationCentral Amygdala Somatostatin Neurons Gate Passive and Active Defensive Behaviors
Yu, K., da Silva, P. G., Albeanu, D. F., & Li, B. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.4419-15.2016 · Cited by 157
Self-citationThe basolateral amygdaloid complex as a cortical-like structure
Carlsen, J., & Heimer, L. (1988) · Brain Research · doi:10.1016/0006-8993(88)91418-7 · Cited by 149
Population coding of valence in the basolateral amygdala
Zhang, X., & Li, B. (2018) · Nature Communications · doi:10.1038/s41467-018-07679-9 · Cited by 147
Self-citationBasolateral amygdala circuitry in positive and negative valence
O’Neill, P.-K., Gore, F., & Salzman, C. D. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.02.012 · Cited by 141
Lodato, S., Molyneaux, B. J., Zuccaro, E., Goff, L. A., Chen, H.-H., Yuan, W., Meleski, A., Takahashi, E., Mahony, S., Rinn, J. L., et al. (2014) · Nature Neuroscience · doi:10.1038/nn.3757 · Cited by 135
McDonald, A. J., Muller, J. F., & Mascagni, F. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10204 · Cited by 134
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 133
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
Ikemoto, S., Qin, M., & Liu, Z. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0892-05.2005 · Cited by 124
A Genetically Defined Compartmentalized Striatal Direct Pathway for Negative Reinforcement
Xiao, X., Deng, H., Furlan, A., Yang, T., Zhang, X., Hwang, G.-R., Tucciarone, J., Wu, P., He, M., Palaniswamy, R., et al. (2020) · Cell · doi:10.1016/j.cell.2020.08.032 · Cited by 101
Self-citationAn Insula–Central Amygdala Circuit for Guiding Tastant-Reinforced Choice Behavior
Schiff, H. C., Bouhuis, A. L., Yu, K., Penzo, M. A., Li, H., He, M., & Li, B. (2018) · The Journal of Neuroscience · doi:10.1523/jneurosci.1773-17.2017 · Cited by 100
Self-citationZhang, Z., Liu, Q., Wen, P., Zhang, J., Rao, X., Zhou, Z., Zhang, H., He, X., Li, J., Zhou, Z., et al. (2017) · eLife · doi:10.7554/elife.25423 · Cited by 95
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Gründemann, J., & Lüthi, A. (2015) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2015.10.005 · Cited by 68
FitzGerald, B. J., Richardson, K., & Wesson, D. W. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00081 · Cited by 51
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Metadata
- Authors
- Zhang, X., Guan, W., Yang, T., Furlan, A., Xiao, X., Yu, K., An, X., Galbavy, W., Ramakrishnan, C., Deisseroth, K., Ritola, K., Hantman, A., He, M., Josh Huang, Z., & Li, B.
- Affiliations
- Cold Spring Harbor Laboratory (US)
- Duke University (US)
- Howard Hughes Medical Institute (US)
- Fudan University (CN)
- Corresponding author
- Zhang, Xian
- Li, Bo
- ORCID
- Venue
- Nature Neuroscience
- Published
- 2021-10-18
- Volume
- 24
- Issue
- 11
- Pages
- 1586-1600
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC8556347
- OpenAlex
- W3206682102
- Cited by
- 126
- References
- 67
- Citations by year
- 2026: 22 · 2025: 24 · 2024: 33 · 2023: 27 · 2022: 17 · 2021: 3
- FWCI
- 10.52
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Cold Spring Harbor Laboratory Institutional Repository (Cold Spring Harbor Laboratory) (submittedVersion)
- Rare & Special e-Zone (The Hong Kong University of Science and Technology) (submittedVersion)
- Funders
- U.S. Department of Health & Human Services | National Institutes of Health (R01MH101214, R01MH108924, R01NS104944)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- basolateral amygdala, Fezf2, nucleus accumbens, olfactory tubercle, punishment avoidance, reward seeking, neural circuits, motivated behavior
- MeSH terms
- Amygdala, Animals, Attention, Avoidance Learning, Corpus Striatum, DNA-Binding Proteins, Female, Male, Mice, Inbred C57BL, Mice, Transgenic, Motivation, Nerve Net, Nerve Tissue Proteins, Mice
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