Divergent routing of positive and negative information from the amygdala during memory retrieval
Open accessAbstract
Although the basolateral amygdala (BLA) is known to play a critical role in the formation of memories of both positive and negative valence, the coding and routing of valence-related information is poorly understood. Here, we recorded BLA neurons during the retrieval of associative memories and used optogenetic-mediated phototagging to identify populations of neurons that synapse in the nucleus accumbens (NAc), the central amygdala (CeA), or ventral hippocampus (vHPC). We found that despite heterogeneous neural responses within each population, the proportions of BLA-NAc neurons excited by reward predictive cues and of BLA-CeA neurons excited by aversion predictive cues were higher than within the entire BLA. Although the BLA-vHPC projection is known to drive behaviors of innate negative valence, these neurons did not preferentially code for learned negative valence. Together, these findings suggest that valence encoding in the BLA is at least partially mediated via divergent activity of anatomically defined neural populations.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Basolateral amygdala microcircuits separate reward and aversion, with valence coding that can bias motivated action toward appetitive cues through projections to the accumbens and toward aversive cues through projections to the central nucleus of the amygdala.
“They [29,30] showed parsing of reward and aversion in basolateral amygdala microcircuits. Specifically, they provided evidence of valence coding in the basolateral amygdala, that could bias motivated action to appetitive cues via projections to the accumbens and to aversive cues via projections to the central nucleus of the amygdala.”
From Development of the emotional brain (2019) · cites this paper as [29]
There is relatively little collateralization of BLA projection neurons to their target regions, suggesting a high degree of projection specificity.
“Notably, there appears to be relatively little collateralization of BLA PNs to these target regions (17), suggesting a high degree of projection specificity.”
From Chronic Stress Remodels Synapses in an Amygdala Circuit-Specific Manner (2019) · cites this paper as [17]
BLA projection neurons innervating the nucleus accumbens and ventral hippocampus primarily encode information with positive and negative valence, respectively.
“This work has, for instance, proposed that BLA PNs innervating the NAc and vHPC primarily encode information with positive and negative valence, respectively (17,20,22,23).”
From Chronic Stress Remodels Synapses in an Amygdala Circuit-Specific Manner (2019) · cites this paper as [17]
BLA projection neurons projecting to the ventral hippocampus or nucleus accumbens have been shown to sparsely innervate the dmPFC.
“Moreover, BLA PNs projecting to the vHPC or NAc have been shown to sparsely innervate the dmPFC (17).”
From Chronic Stress Remodels Synapses in an Amygdala Circuit-Specific Manner (2019) · cites this paper as [17]
Anticipatory licking during the CS-trace provides a reliable, trial-by-trial index of memory expression.
“in which anticipatory licking provides a reliable, trial-by-trial index of memory expression.”
From Infraslow histaminergic dynamics govern priming states to gate moment-to-moment memory accessibility (2026) · cites this paper as [26]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Etkin, A., & Wager, T. D. (2007) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2007.07030504 · Cited by 3,391 · see citing works
A mesoscale connectome of the mouse brain
Oh, S. W., Harris, J. A., Ng, L., Winslow, B., Cain, N., Mihalas, S., Wang, Q., Lau, C., Kuan, L., Henry, A. M., et al. (2014) · Nature · doi:10.1038/nature13186 · Cited by 2,612 · see citing works
From circuits to behaviour in the amygdala
Janak, P. H., & Tye, K. M. (2015) · Nature · doi:10.1038/nature14188 · Cited by 2,011 · cited 2× · see citing works
“The neural circuits underlying the assignment of valence to environmental stimuli are thought to be highly conserved in the mammalian brain (Janak and Tye, 2015) and are dysfunctional in psychopathologies including anxiety, depression, and addiction (Allsop et al.”
Self-citationBerridge, K. C., & Robinson, T. E. (2003) · Trends in Neurosciences · doi:10.1016/s0166-2236(03)00233-9 · Cited by 1,869 · see citing works
Neuron-type-specific signals for reward and punishment in the ventral tegmental area
Cohen, J. Y., Haesler, S., Vong, L., Lowell, B. B., & Uchida, N. (2012) · Nature · doi:10.1038/nature10754 · Cited by 1,318 · see citing works
Cortical pathways to the mammalian amygdala
McDonald, A. J. (1998) · Progress in Neurobiology · doi:10.1016/s0301-0082(98)00003-3 · Cited by 1,303 · see citing works
Amygdala 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 · see citing works
Self-citationDopamine neurons modulate neural encoding and expression of depression-related behaviour
Tye, K. M., Mirzabekov, J. J., Warden, M. R., Ferenczi, E. A., Tsai, H.-C., Finkelstein, J., Kim, S.-Y., Adhikari, A., Thompson, K. R., Andalman, A. S., et al. (2013) · Nature · doi:10.1038/nature11740 · Cited by 1,073 · see citing works
Self-citationThe Amygdala: a functional analysis
Aggleton, J. P. (2000) · Cited by 964 · see citing works
Encoding 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 · see citing works
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 · cited 5× · see citing works
“…cues associated with positive and negative valence Our results are consistent with previous studies reporting that intermingled neurons in the BLA respond to the valence of learned cues in rats (Shabel and Janak, 2009) and monkeys (Fuster and Uyeda, 1971; Paton et al., 2006; Zhang et al., 2013b).”
InfluentialExcitatory 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 · see citing works
Self-citationSynaptic 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 · see citing works
Distinct extended amygdala circuits for divergent motivational states
Jennings, J. H., Sparta, D. R., Stamatakis, A. M., Ung, R. L., Pleil, K. E., Kash, T. L., & Stuber, G. D. (2013) · Nature · doi:10.1038/nature12041 · Cited by 704 · cited 1× · see citing works
“Recently, the in vivo activity of projection-target-defined cells has been examined by expressing ChR2 in neurons of interest and using light-evoked firing as an instrument to identify these neurons in intact animals (Ciocchi et al., 2015; Jennings et al., 2013; Zhang et al., 2013a).”
Etkin, A., Prater, K. E., Schatzberg, A. F., Menon, V., & Greicius, M. D. (2009) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2009.104 · Cited by 664 · see citing works
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 · see citing works
Self-citationBLA 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 · see citing works
Self-citationLong-range connectivity defines behavioral specificity of amygdala neurons
Senn, V., Wolff, S. B. E., Herry, C., Grenier, F., Ehrlich, I., Gründemann, J., Fadok, J. P., Müller, C., Letzkus, J. J., & Lüthi, A. (2014) · Neuron · doi:10.1016/j.neuron.2013.11.006 · Cited by 522 · cited 1× · see citing works
“A uthor M anuscript A uthor M anuscript A uthor M anuscript A uthor M anuscript Nieh et al., 2015; Senn et al., 2014).”
Ambroggi, F., Ishikawa, A., Fields, H. L., & Nicola, S. M. (2008) · Neuron · doi:10.1016/j.neuron.2008.07.004 · Cited by 488 · 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 · see citing works
Self-citationGoosens, K. A., & Maren, S. (2001) · Learning & Memory · doi:10.1101/lm.37601 · Cited by 451 · see citing works
Decoding Neural Circuits that Control Compulsive Sucrose Seeking
Nieh, E. H., Matthews, G. A., Allsop, S. A., Presbrey, K. N., Leppla, C. A., Wichmann, R., Neve, R., Wildes, C. P., & Tye, K. M. (2015) · Cell · doi:10.1016/j.cell.2015.01.003 · Cited by 402 · see citing works
Self-citationQuantitative MRI of the hippocampus and amygdala in severe depression
Mervaala, E., Föhr, J., Könönen, M., Valkonen‐Korhonen, M., Vainio, P. A., Partanen, K. P. L., Partanen, J. V., Tiihonen, J., Viinamäki, H. T., Karjalainen, A.-M., et al. (2000) · Psychological Medicine · doi:10.1017/s0033291799001567 · Cited by 382 · see citing works
Ben‐Ari, Y., Tremblay, E. C., & Ottersen, O. P. (1980) · Neuroscience · doi:10.1016/0306-4522(80)90049-4 · Cited by 373 · see citing works
Selective information routing by ventral hippocampal CA1 projection neurons
Ciocchi, S., Passecker, J., Malagon‐Vina, H., Mikuš, N., & Klausberger, T. (2015) · Science · doi:10.1126/science.aaa3245 · Cited by 344 · see citing works
Comparative evaluation of synaptophysin-based methods for quantification of synapses
Calhoun, M. E., Jucker, M., Martin, L. J., Thinakaran, G., Price, D. L., & Mouton, P. R. (1996) · Journal of Neurocytology · doi:10.1007/bf02284844 · Cited by 303 · see citing works
Somerville, L. H., Kim, H., Johnstone, T., Alexander, A. L., & Whalen, P. J. (2004) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.01.007 · Cited by 260 · see citing works
Gore, 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 · see citing works
Optogenetic Dissection of Entorhinal-Hippocampal Functional Connectivity
Zhang, S., Ye, J., Miao, C., Tsao, A., Cerniauskas, I., Ledergerber, D., Moser, M., & Moser, E. I. (2013) · Science · doi:10.1126/science.1232627 · Cited by 256 · see citing works
Bordi, F., & LeDoux, J. E. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-07-02493.1992 · Cited by 218 · see citing works
Rapid 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 · see citing works
Self-citationDistributed circuits underlying anxiety
Adhikari, A. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00112 · Cited by 204 · see citing works
Shabel, S. J., & Janak, P. H. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0905580106 · Cited by 190 · see citing works
Neuronal organization of the lateral and basolateral amygdaloid nuclei in the rat
McDonald, A. J. (1984) · The Journal of Comparative Neurology · doi:10.1002/cne.902220410 · Cited by 162 · see citing works
Optogenetic insights on the relationship between anxiety-related behaviors and social deficits
Allsop, S. A., Vander Weele, C. M., Wichmann, R., & Tye, K. M. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00241 · Cited by 150 · see citing works
Self-citationArchitectural 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 · see citing works
Self-citationOptogenetic dissection of neural circuits underlying emotional valence and motivated behaviors
Nieh, E. H., Kim, S., Namburi, P., & Tye, K. M. (2012) · Brain Research · doi:10.1016/j.brainres.2012.11.001 · Cited by 129 · see citing works
Self-citationShinonaga, Y., Takada, M., & Mizuno, N. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90045-0 · Cited by 127 · see citing works
Distinct Subtypes of Basolateral Amygdala Taste Neurons Reflect Palatability and Reward
Fontanini, A., Grossman, S. E., Figueroa, J. A., & Katz, D. B. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.3898-08.2009 · Cited by 126 · see citing works
Amorapanth, P. X., Nader, K., & LeDoux, J. E. (1999) · Learning & memory (Cold Spring Harbor, N.Y.) · doi:10.1101/lm.6.5.491 · Cited by 111 · see citing works
Progress in understanding mood disorders: optogenetic dissection of neural circuits
Lammel, S., Tye, K. M., & Warden, M. R. (2014) · Genes, Brain and Behavior · doi:10.1111/gbb.12049 · Cited by 98 · see citing works
Self-citationReactivity 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 · see citing works
Functional 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 · see citing works
Nuclear 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 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Anxiety Cells in a Hippocampal-Hypothalamic Circuit
Jimenez, J., Su, K., Goldberg, A., Luna, V. M., Biane, J. S., Ordek, G., Zhou, P., Ong, S. K., Wright, M. A., Zweifel, L. S., et al. (2018) · Neuron · doi:10.1016/j.neuron.2018.01.016 · Cited by 606 · see citing works
Striatal circuits for reward learning and decision-making
Cox, J., & Witten, I. B. (2019) · Nature reviews. Neuroscience · doi:10.1038/s41583-019-0189-2 · Cited by 554 · see citing works
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
Self-citationDevelopment of the emotional brain
Casey, B. J., Heller, A. S., Gee, D. G., & Cohen, A. O. (2019) · Neuroscience Letters · doi:10.1016/j.neulet.2017.11.055 · Cited by 485 · see citing works
A 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
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
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
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 · 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
A neuronal circuit for activating descending modulation of neuropathic pain
Huang, J., Gadotti, V. M., Chen, L., Souza, I. A., Huang, S., Wang, D., Ramakrishnan, C., Deisseroth, K. A., Zhang, Z., & Zamponi, G. W. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0481-5 · Cited by 329 · 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
“This retrograde-based investigation of collateralization complements our previous anterograde-based investigation of collateralization published in Figure S3 of Beyeler et al. (2016).”
BackgroundMethodInfluentialSelf-citationInhibition 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 311 · see citing works
From Structure to Behavior in Basolateral Amygdala-Hippocampus Circuits
Yang, Y., & Wang, J. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00086 · Cited by 301 · see citing works
Dopamine enhances signal-to-noise ratio in cortical-brainstem encoding of aversive stimuli
Weele, C. M. V., Siciliano, C. A., Matthews, G. A., Namburi, P., Izadmehr, E. M., Espinel, I. C., Nieh, E. H., Schut, E. H. S., Padilla-Coreano, N., Burgos-Robles, A., et al. (2018) · Nature · doi:10.1038/s41586-018-0682-1 · Cited by 288 · see citing works
Self-citationCorticoamygdala Transfer of Socially Derived Information Gates Observational Learning
Allsop, S. A., Wichmann, R., Mills, F., Burgos-Robles, A., Chang, C.-J., Felix-Ortiz, A. C., Vienne, A., Beyeler, A., Izadmehr, E. M., Glober, G., et al. (2018) · Cell · doi:10.1016/j.cell.2018.04.004 · Cited by 288 · see citing works
Self-citationAmygdala 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 279 · see citing works
Bocchio, M., Nabavi, S., & Capogna, M. (2017) · Neuron · doi:10.1016/j.neuron.2017.03.022 · Cited by 260 · see citing works
Amygdala Inhibitory Circuits Regulate Associative Fear Conditioning
Krabbe, S., Gründemann, J., & Lüthi, A. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.10.006 · Cited by 255 · 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
Self-citationBasolateral amygdala and stress-induced hyperexcitability affect motivated behaviors and addiction
Sharp, B. M. (2017) · Translational Psychiatry · doi:10.1038/tp.2017.161 · Cited by 244 · see citing works
Estimation of Current and Future Physiological States in Insular Cortex
Livneh, Y., Sugden, A. U., Madara, J. C., Essner, R. A., Flores, V. I., Sugden, L. A., Resch, J. M., Lowell, B. B., & Andermann, M. L. (2020) · Neuron · doi:10.1016/j.neuron.2019.12.027 · Cited by 209 · see citing works
NEVER Forget: Negative Emotional Valence Enhances Recapitulation
Bowen, H. J., Kark, S. M., & Kensinger, E. (2017) · Psychonomic Bulletin & Review · doi:10.3758/s13423-017-1313-9 · Cited by 192 · see citing works
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 223 · see citing works
Amygdala ensembles encode behavioral states
Gründemann, J., Bitterman, Y., Lu, T., Krabbe, S., Grewe, B. F., Schnitzer, M. J., & Lüthi, A. (2019) · Science · doi:10.1126/science.aav8736 · Cited by 223 · see citing works
Memory Allocation: Mechanisms and Function
Josselyn, S. A., & Frankland, P. W. (2018) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-080317-061956 · Cited by 221 · see citing works
Integration of Parallel Opposing Memories Underlies Memory Extinction
Felsenberg, J., Jacob, P. F., Walker, T. M., Barnstedt, O., Edmondson-Stait, A. J., Pleijzier, M. W., Otto, N., Schlegel, P., Sharifi, N., Perisse, E., et al. (2018) · Cell · doi:10.1016/j.cell.2018.08.021 · Cited by 217 · see citing works
Amygdala Circuit Substrates for Stress Adaptation and Adversity
Zhang, W.-H., Zhang, J.-Y., Holmes, A., & Pan, B.-X. (2021) · Biological Psychiatry · doi:10.1016/j.biopsych.2020.12.026 · Cited by 196 · see citing works
Dopamine D2 receptors in discrimination learning and spine enlargement
Iino, Y., Sawada, T., Yamaguchi, K., Tajiri, M., Ishii, S., Kasai, H., & Yagishita, S. (2020) · Nature · doi:10.1038/s41586-020-2115-1 · Cited by 176 · see citing works
Chronic Stress Remodels Synapses in an Amygdala Circuit-Specific Manner
Zhang, J.-Y., Liu, T.-H., He, Y., Pan, H.-Q., Zhang, W.-H., Yin, X.-P., Tian, X.-L., Li, B.-M., Wang, X.-D., Holmes, A., et al. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.06.019 · Cited by 183 · see citing works
Affective valence in the brain: modules or modes?
Berridge, K. C. (2019) · Nature reviews. Neuroscience · doi:10.1038/s41583-019-0122-8 · Cited by 183 · see citing works
Endogenous opioid peptides in the descending pain modulatory circuit
Bagley, E. E., & Ingram, S. (2020) · Neuropharmacology · doi:10.1016/j.neuropharm.2020.108131 · Cited by 186 · see citing works
State-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
Motivational neural circuits underlying reinforcement learning
Averbeck, B. B., & Costa, V. D. (2017) · Nature Neuroscience · doi:10.1038/nn.4506 · Cited by 175 · see citing works
Basolateral amygdala to orbitofrontal cortex projections enable cue-triggered reward expectations
Lichtenberg, N. T., Pennington, Z. T., Holley, S. M., Greenfield, V. Y., Cepeda, C., Levine, M. S., & Wassum, K. M. (2017) · The Journal of Neuroscience · doi:10.1523/jneurosci.0486-17.2017 · Cited by 171 · see citing works
Adaptive disinhibitory gating by VIP interneurons permits associative learning
Krabbe, S., Paradiso, E., d‘Aquin, S., Bitterman, Y., Courtin, J., Xu, C., Yonehara, K., Marković, M., Müller, C. R., Eichlisberger, T., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0508-y · Cited by 161 · see citing works
Social Behavior Is Modulated by Valence-Encoding mPFC-Amygdala Sub-circuitry
Huang, W., Zucca, A., Levy, J., & Page, D. T. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107899 · Cited by 163 · see citing works
Ma, H., Li, C., Wang, J., Zhang, X., Li, M., Zhang, R., Huang, Z., & Zhang, Y. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2019409118 · Cited by 158 · 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
“…or decreased their firing rates in response to the CS-Rs or CS-Ss (Figures 2A–2B, top row; rank-sum tests, p < 0.005), consistent with prior studies (Beyeler et al., 2016; Burgos-Robles et al., 2017; Lee et al., 2016, 2017; Namburi et al., 2015; Sangha et al., 2013; Shabel and Janak, 2009).”
InfluentialPrefrontal Cortex Drives Distinct Projection Neurons in the Basolateral Amygdala
McGarry, L. M., & Carter, A. G. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.10.046 · Cited by 141 · see citing works
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
Campbell, E. J., & Marchant, N. J. (2018) · British Journal of Pharmacology · doi:10.1111/bph.14146 · Cited by 140 · see citing works
Basolateral 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 139 · see citing works
Distinct cortical–amygdala projections drive reward value encoding and retrieval
Malvaez, M., Shieh, C., Murphy, M. D., Greenfield, V. Y., & Wassum, K. M. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0374-7 · Cited by 130 · 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
Kim, W. B., & Cho, J.-H. (2017) · The Journal of Neuroscience · doi:10.1523/jneurosci.3579-16.2017 · Cited by 131 · see citing works
Population 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
Inflammation‐driven brain and gut barrier dysfunction in stress and mood disorders
Doney, E., Cadoret, A., Dion‐Albert, L., Lebel, M., & Ménard, C. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15239 · Cited by 130 · see citing works
A feedback neural circuit for calibrating aversive memory strength
Ozawa, T., Ycu, E. A., Kumar, A., Yeh, L.-F., Ahmed, T., Koivumaa, J., & Johansen, J. P. (2016) · Nature Neuroscience · doi:10.1038/nn.4439 · Cited by 123 · see citing works
Zhou, L., Liu, M., Li, Q., Deng, J., Mu, D., & Sun, Y.-G. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.02.077 · Cited by 116 · see citing works
FGF21 suppresses alcohol consumption through an amygdalo-striatal circuit
Flippo, K. H., Trammell, S. A. J., Gillum, M. P., Aklan, İ., Perez, M. B., Yavuz, Y., Smith, N. K., Jensen-Cody, S. O., Zhou, B., Claflin, K. E., et al. (2022) · Cell Metabolism · doi:10.1016/j.cmet.2021.12.024 · Cited by 113 · see citing works
Pain modulates dopamine neurons via a spinal–parabrachial–mesencephalic circuit
Yang, H., de Jong, J. W., Cerniauskas, I., Peck, J. R., Lim, B. K., Gong, H., Fields, H. L., & Lammel, S. (2021) · Nature Neuroscience · doi:10.1038/s41593-021-00903-8 · Cited by 113 · 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
Self-citationLinking emotional valence and anxiety in a mouse insula-amygdala circuit
Nicolas, C., Ju, A., Wu, Y., Eldirdiri, H., Delcasso, S., Couderc, Y., Fornari, C., Mitra, A., Supiot, L., Vérité, A., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-40517-1 · Cited by 107 · see citing works
Self-citationTranslating Across Circuits and Genetics Toward Progress in Fear- and Anxiety-Related Disorders
Ressler, K. J. (2020) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2020.20010055 · Cited by 104 · see citing works
RDoC-based categorization of amygdala functions and its implications in autism
Hennessey, T., Andari, E., & Rainnie, D. G. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.04.007 · Cited by 105 · see citing works
Anxiety and Nicotine Dependence: Emerging Role of the Habenulo-Interpeduncular Axis
Molas, S., DeGroot, S. R., Zhao-Shea, R., & Tapper, A. R. (2016) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2016.11.001 · Cited by 100 · see citing works
Neural dynamics underlying associative learning in the dorsal and ventral hippocampus
Biane, J. S., Ladow, M. A., Stefanini, F., Boddu, S. P., Fan, A., Hassan, S., Dundar, N., Apodaca-Montano, D. L., Zhou, L. Z., Fayner, V., et al. (2023) · Nature Neuroscience · doi:10.1038/s41593-023-01296-6 · Cited by 95 · see citing works
Levy, I., & Schiller, D. (2021) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2020.11.007 · Cited by 95 · see citing works
Emotional Modulation of Learning and Memory: Pharmacological Implications
LaLumiere, R., McGaugh, J. D., & McIntyre, C. K. (2017) · Pharmacological Reviews · doi:10.1124/pr.116.013474 · Cited by 82 · see citing works
Mixed selectivity: Cellular computations for complexity
Tye, K. M., Miller, E. K., Taschbach, F., Benna, M. K., Rigotti, M., & Fusi, S. (2024) · Neuron · doi:10.1016/j.neuron.2024.04.017 · Cited by 99 · see citing works
Self-citationDopamine tunes prefrontal outputs to orchestrate aversive processing
Weele, C. M. V., Siciliano, C. A., & Tye, K. M. (2018) · Brain Research · doi:10.1016/j.brainres.2018.11.044 · Cited by 89 · see citing works
Self-citationThe role of the hippocampus in the consolidation of emotional memories during sleep
Pronier, É., Morici, J. F., & Girardeau, G. (2023) · Trends in Neurosciences · doi:10.1016/j.tins.2023.08.003 · Cited by 96 · see citing works
Coordinated Reductions in Excitatory Input to the Nucleus Accumbens Underlie Food Consumption
Reed, S. J., Lafferty, C. K., Mendoza, J. A., Yang, A. K., Davidson, T. J., Grosenick, L., Deisseroth, K. A., & Britt, J. P. (2018) · Neuron · doi:10.1016/j.neuron.2018.07.051 · Cited by 85 · see citing works
The Dopamine Prediction Error: Contributions to Associative Models of Reward Learning
Nasser, H. M., Calu, D. J., Schoenbaum, G. M., & Sharpe, M. J. (2017) · Frontiers in Psychology · doi:10.3389/fpsyg.2017.00244 · Cited by 89 · see citing works
Differential 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 · 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
Self-citationExtensive 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
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
Sex-Dependent Regulation of Aromatase-Mediated Synaptic Plasticity in the Basolateral Amygdala
Bender, R., Zhou, L.-P., Vierk, R., Brandt, N., Keller, A., Gee, C., Schäfer, M. K. E., & Rune, G. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.1532-16.2016 · Cited by 76 · 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
Neurocognitive Development of Motivated Behavior: Dynamic Changes across Childhood and Adolescence
Gee, D. G., Bath, K. G., Johnson, C. M., Meyer, H. C., Murty, V. P., van den Bos, W., & Hartley, C. A. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.1674-18.2018 · Cited by 81 · see citing works
On being a circuit psychiatrist
Gordon, J. A. (2016) · Nature Neuroscience · doi:10.1038/nn.4419 · Cited by 78 · see citing works
Divergent projections of the prelimbic cortex bidirectionally regulate active avoidance
Diehl, M. M., Iravedra-García, J. M., Morán-Sierra, J., Rojas-Bowe, G., Gonzalez-Diaz, F. N., Valentín-Valentín, V. P., & Quirk, G. J. (2020) · eLife · doi:10.7554/elife.59281 · Cited by 78 · see citing works
Expressions of emotions across species
Zych, A. D., & Gogolla, N. (2021) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2021.01.003 · Cited by 77 · 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
Millan, E. Z., Kim, H. A., & Janak, P. H. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.07.044 · Cited by 72 · see citing works
Advances in optogenetic and chemogenetic methods to study brain circuits in non-human primates
Galván, A., Caiola, M. J., & Albaugh, D. L. (2017) · Journal of Neural Transmission · doi:10.1007/s00702-017-1697-8 · Cited by 74 · see citing works
Functional neuroanatomy of the basolateral amygdala: Neurons, neurotransmitters, and circuits
McDonald, A. J. (2020) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-815134-1.00001-5 · Cited by 79 · see citing works
Hippocampal cells segregate positive and negative engrams
Shpokayte, M., McKissick, O. P., Guan, X., Yuan, B., Rahsepar, B., Fernandez, F. R., Ruesch, E. A., Grella, S. L., White, J. A., Liu, X. S., et al. (2022) · Communications Biology · doi:10.1038/s42003-022-03906-8 · Cited by 75 · see citing works
Aitta‐aho, T., Hay, Y. A., Phillips, B. U., Saksida, L. M., Bussey, T. J., Paulsen, O., & Apergis‐Schoute, J. (2018) · Current Biology · doi:10.1016/j.cub.2018.06.064 · Cited by 73 · see citing works
WHEN SCIENTIFIC PARADIGMS LEAD TO TUNNEL VISION: LESSONS FROM THE STUDY OF FEAR
Paré, D., & Quirk, G. (2017) · npj Science of Learning · doi:10.1038/s41539-017-0007-4 · Cited by 71 · 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
Li, S.-J., Vaughan, A., Sturgill, J. F., & Kepecs, Á. (2018) · Neuron · doi:10.1016/j.neuron.2018.05.028 · Cited by 69 · 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
Basolateral Amygdala Neurons Maintain Aversive Emotional Salience
Sengupta, A., Yau, J. O.-Y., Jean-Richard-dit-Bressel, P., Liu, Y., Millan, E. Z., Power, J., & McNally, G. P. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.2460-17.2017 · Cited by 71 · 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
Self-citationAn 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
Distinct µ-opioid ensembles trigger positive and negative fentanyl reinforcement
Chaudun, F., Python, L., Liu, Y., Hiver, A., Cand, J., Kieffer, B. L., Valjent, E., & Lüscher, C. (2024) · Nature · doi:10.1038/s41586-024-07440-x · Cited by 69 · see citing works
Stuber, G. D. (2023) · Science · doi:10.1126/science.adh8287 · Cited by 66 · 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
Cocaine-Induced Structural Plasticity in Input Regions to Distinct Cell Types in Nucleus Accumbens
Barrientos, C., Knowland, D., Wu, M. M. J., Lilascharoen, V., Huang, K. W., Malenka, R. C., & Lim, B. K. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.04.019 · Cited by 61 · see citing works
Zhou, H.-Y., He, J., Hu, Z., Xue, S.-G., Xu, J., Cui, Q., Gao, S., Zhou, B., Wu, P., Long, L., et al. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2019.03.967 · Cited by 63 · see citing works
Roberts, C., Sahakian, B. J., & Robbins, T. W. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.09.001 · Cited by 61 · see citing works
From Engrams to Pathologies of the Brain
Denny, C. A., Lebois, E. P., & Ramirez, S. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00023 · Cited by 64 · see citing works
Discrete subicular circuits control generalization of hippocampal seizures
Fei, F., Wang, X., Xu, C., Shi, J., Gong, Y., Cheng, H., Lai, N., Ruan, Y., Ding, Y., Wang, S., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-32742-x · Cited by 62 · see citing works
Orsini, C. A., Hernandez, C. M., Singhal, S. M., Kelly, K. B., Frazier, C. J., Bizon, J. L., & Setlow, B. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.2344-17.2017 · Cited by 58 · see citing works
Differential encoding of place value between the dorsal and intermediate hippocampus
Jin, S., & Lee, I. (2021) · Current Biology · doi:10.1016/j.cub.2021.04.073 · Cited by 60 · see citing works
A 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
Li, H., Vento, P. J., Parrilla-Carrero, J., Pullmann, D., Chao, Y. S., Eid, M., & Jhou, T. C. (2019) · Neuron · doi:10.1016/j.neuron.2019.08.040 · Cited by 59 · see citing works
- Authors
- Beyeler, A., Namburi, P., Glober, G. F., Simonnet, C., Calhoon, G. G., Conyers, G. F., Luck, R., Wildes, C. P., & Tye, K. M.
- Affiliations
- Massachusetts Institute of Technology (US)
- Corresponding author
- Tye, Kay M.
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2016-04
- Volume
- 90
- Issue
- 2
- Pages
- 348-361
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC4854303
- OpenAlex
- W2318838494
- Cited by
- 412
- References
- 44
- Citations by year
- 2026: 23 · 2025: 28 · 2024: 64 · 2023: 37 · 2022: 32 · 2021: 52 · 2020: 48 · 2019: 44 · 2018: 41 · 2017: 31 · 2016: 12
- FWCI
- 27.15
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc-nd)
- Funders
- National Institute of Mental Health (R01MH102441)
- National Institute of Diabetes and Digestive and Kidney Diseases (DP2DK102256)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Keywords
- basolateral amygdala, memory retrieval, positive and negative valence, nucleus accumbens, central amygdala, ventral hippocampus, reward-predictive cues, associative memory
- MeSH terms
- Animals, Cues, Hippocampus, Male, Neural Pathways, Nucleus Accumbens, Mental Recall, Mice, Basolateral Nuclear Complex, Central Amygdaloid Nucleus
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 ›
Are you an author, or do you see a problem with this page? Request a review
