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From circuits to behaviour in the amygdala
Open accessAbstract
The amygdala has long been associated with emotion and motivation, playing an essential part in processing both fearful and rewarding environmental stimuli. How can a single structure be crucial for such different functions? With recent technological advances that allow for causal investigations of specific neural circuit elements, we can now begin to map the complex anatomical connections of the amygdala onto behavioural function. Understanding how the amygdala contributes to a wide array of behaviours requires the study of distinct amygdala circuits.
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In the citing paper
“More recently, more in-depth research has illustrated that alterations in the HPA axis have been associated with the process of dealing with stress, especially toxic stress-induced negative health outcomes (83).”
From Epigenetic Modifications in Stress Response Genes Associated With Childhood Trauma (2019) · cites this paper as [83]
Experimental — accuracy not yet measuredIn the citing paper
“A growing appreciation for the complexity of the amygdala complex has resulted in a more nuanced understanding of this region’s role in fear learning, appetitive learning, and value encoding (Janak and Tye, 2015), and it is clear that the amygdala promotes adaptive behavioral responses to both positive and negative environmental stimuli.”
From A framework for understanding the emerging role of corticolimbic-ventral striatal networks in OCD-associated repetitive behaviors (2015) · cites this paper as Janak and Tye, 2015
In the citing paper
“In addition to a role in fear and threat conditioning, the amygdala also regulates anxiety.”
From A framework for understanding the emerging role of corticolimbic-ventral striatal networks in OCD-associated repetitive behaviors (2015) · cites this paper as Janak and Tye, 2015
In the citing paper
“Since the amygdala is central to processing these forms of information (Janak and Tye, 2015), aberrant communication of anxiety-related information from amygdala to VS could mediate anxiety-driven compulsive behavior.”
From A framework for understanding the emerging role of corticolimbic-ventral striatal networks in OCD-associated repetitive behaviors (2015) · cites this paper as Janak and Tye, 2015
In the citing paper
“The BNST and the CeA have been implicated in diverse behavioral functions (Davis et al., 2010, Janak and Tye, 2015, Kim et al., 2013)”
From Dorsal raphe dopamine neurons represent the experience of social isolation (2016) · cites this paper as Janak and Tye, 2015
In the citing paper
“In particular, given its access to primary sensory information, the CeA could orchestrate appropriate behavioral responses to salient stimuli with different valences [88,93].”
From Oxytocin Signaling in the Central Amygdala Modulates Emotion Discrimination in Mice (2019) · cites this paper as [93]
In the citing paper
“Processing of this sensory information in the BLA results in the formation of associations between neutral predictive stimuli and outcomes of positive or negative valence56 via Hebbian mechanisms57-59.”
From Resolving the neural circuits of anxiety (2015) · cites this paper as [56]
In the citing paper
“This interpretation is in part dictated by the individual’s previous experience and includes the assignment of valence to the stimulus via BLA circuits56.”
From Resolving the neural circuits of anxiety (2015) · cites this paper as [56]
In the citing paper
“the valence detection function of BLA projection neurons56 fits within the interpretation circuits described here, helping to determine whether a given stimulus is threatening or appetitive.”
From Resolving the neural circuits of anxiety (2015) · cites this paper as [56]
In the citing paper
“The BLA is critical for associative learning”
From Infraslow histaminergic dynamics govern priming states to gate moment-to-moment memory accessibility (2026) · cites this paper as [30]
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“These neurons are thought to assign affective value to sensory signals with strong emotional valence (Janak and Tye, 2015; Namburi et al., 2015) and are the primary output neurons of this brain region that is known to play an integral role in the etiology of anxiety disorders and addiction (Stuber…”
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“Regarding larger mesocorticolimbic circuitry, CeA is known to modulate mesolimbic dopamine systems in tegmentum and nucleus accumbens activity (Ahn and Phillips, 2002) via outputs to intermediary ventral pallidum, lateral hypothalamus, ventral tegmentum, and other targets (Yoshida et al., 2006; Heimer, 2008; Janak and…”
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“The amygdala is an evolutionarily conserved hub for emotional processing, with homologous structure and function observed across vertebrate species (Janak and Tye, 2015).”
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“Auditory fear learning reflects a plasticity at sites of CS and US convergence, including the lateral amygdala, medial division of the medial geniculate body, and auditory cortex (ACx) (Janak and Tye, 2015; Letzkus et al., 2015; McGann, 2015; Weinberger, 2011).”
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“sensory structures elsewhere in the brain [17], [89].”
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“This region is comprised largely of glutamatergic pyramidal cells which project to other amygdala nuclei and many other limbic and cortical structures (Janak and Tye, 2015; McDonald, 1998).”
BackgroundRDoC-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 107
“fear), along with the medial amygdala (MeA) linked to the olfactory system (Janak and Tye, 2015; LeDoux, 2008).”
Integrating Organs-on-Chips: Multiplexing, Scaling, Vascularization, and Innervation
Park, D., Lee, J., Chung, J. J., Jung, Y., & Kim, S. H. (2020) · Trends in Biotechnology · doi:10.1016/j.tibtech.2019.06.006 · Cited by 105
Stamatakis, A. M., Schachter, M. J., Gulati, S., Zitelli, K. T., Malanowski, S., Tajik, A., Fritz, C., Trulson, M. O., & Otte, S. L. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00496 · Cited by 108
“The connection between the BLA and NAc plays a critical role in reward circuitry underlying emotion, reward, and motivated behaviors (Setlow et al., 2002; Ambroggi et al., 2008; Stuber et al., 2011; Janak and Tye, 2015).”
BackgroundPrimate amygdala neurons simulate decision processes of social partners
Grabenhorst, F., Báez-Mendoza, R., Genest, W., Deco, G., & Schultz, W. (2019) · Cell · doi:10.1016/j.cell.2019.02.042 · Cited by 103
Early detection of intentional harm in the human amygdala
Hesse, E., Mikulan, E., Decety, J., Sigman, M., García, M. D. C., Silva, W., Ciraolo, C. A., Vaucheret, E., Baglivo, F. H., Huepe, D., et al. (2015) · Brain · doi:10.1093/brain/awv336 · Cited by 142
“Because theta fronto-amygdaline oscilla- tion is enhanced during aversive stimuli processing (Janak and Tye, 2015), this may indicate a general role for low- frequency coupling between these regions in the face of aversion-inducing events.”
BackgroundNeural Basis of Observational Fear Learning: A Potential Model of Affective Empathy
Keum, S., & Shin, H.-S. (2019) · Neuron · doi:10.1016/j.neuron.2019.09.013 · Cited by 104
“Specifically, the basolateral nucleus of the amygdala (BLA) is regarded as one of the most fundamental neural structures for encoding negative and positive affective valences (Janak and Tye, 2015; Olsson and Phelps, 2007).”
BackgroundAn affective neuroscience model of boosting resilience in adults
Tabibnia, G. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.05.005 · Cited by 115
The interplay of hypoxic and mental stress: Implications for anxiety and depressive disorders
Burtscher, J., Niedermeier, M., Hüfner, K., van den Burg, E. H., Kopp, M., Stoop, R., Burtscher, M., Gatterer, H., & Millet, G. P. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104718 · Cited by 110
“The amygdala is an important structure in the emotional and motivational drivers of human behavior and likely involved in the etiopathogenesis of anxiety disorders (Janak and Tye, 2015).”
Neuroinflammation in preterm babies and autism spectrum disorders
Bokobza, C., Steenwinckel, J. V., Mani, S., Mezger, V., Fleiss, B., & Gressèns, P. (2018) · Pediatric Research · doi:10.1038/s41390-018-0208-4 · Cited by 112
Cortico-Limbic Interactions Mediate Adaptive and Maladaptive Responses Relevant to Psychopathology
Kovner, R., Oler, J. A., & Kalin, N. H. (2019) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2019.19101064 · Cited by 111
“The amygdala is associated with a variety of functions, including the encoding of both positive and negative valence (70, 71).”
BackgroundHasegawa, E., Maejima, T., Yoshida, T., Masseck, O. A., Herlitze, S., Yoshioka, M., Sakurai, T., & Mieda, M. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1614552114 · Cited by 106
“(30, 31), whereas the amygdala plays an important role in emotional processing (32) and likely involved in cataplexy triggered by strong emotion (4, 19, 33).”
BackgroundCognition and Reward Circuits in Schizophrenia: Synergistic, Not Separate
Robison, A. J., Thakkar, K. N., & Diwadkar, V. A. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2019.09.021 · Cited by 104
Martinelli, D. C., Chew, K. S., Rohlmann, A., Lum, M. Y., Ressl, S., Hattar, S. S., Brünger, A. T., Missler, M., & Südhof, T. C. (2016) · Neuron · doi:10.1016/j.neuron.2016.07.002 · Cited by 100
“To test whether C1ql3 is required for all BLA-derived synaptic projections, we examined the well-established BLA projection to the ventral hippocampus (Janak and Tye, 2015).”
InfluentialCocaine-induced projection-specific and cell type-specific adaptations in the nucleus accumbens
Zinsmaier, A. K., Dong, Y., & Huang, Y. H. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01112-2 · Cited by 101
“The amygdala is an evolutionarily conserved brain region that encodes and relays information pertaining to cues associated with emotional valence, including cocaineassociated cues [95, 96].”
BackgroundLevy, I., & Schiller, D. (2021) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2020.11.007 · Cited by 95
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 117
“79 The amygdala is a relatively primitive structure with the capacity for plasticity to form new associations and lies in the middle of the spectrum.”
Self-citationWolosker, H., & Balu, D. T. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-00870-x · Cited by 106
Multimodal and Site-Specific Plasticity of Amygdala Parvalbumin Interneurons after Fear Learning
Lucas, E. K., Jegarl, A. M., Morishita, H., & Clem, R. L. (2016) · Neuron · doi:10.1016/j.neuron.2016.06.032 · Cited by 97
“Cellular models of fear learning place a great deal of emphasis on amygdala excitatory neuronal plasticity (Janak and Tye, 2015; Johansen et al., 2011).”
Amygdala subnuclei resting-state functional connectivity sex and estrogen differences
Engman, J., Linnman, C., Van Dijk, K. R. A., & Milad, M. R. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.09.012 · Cited by 89
Dopamine 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 98
“, 2017; Sotres-Bayon and Quirk, 2010; Yizhar and Klavir, 2018), given the BLA’s role in processing salient and valance-defined stimuli (Janak and Tye, 2015; Namburi et al., 2015; Shabel and Janak, 2009).”
BackgroundSelf-citationDeveloping neuroscience-based treatments for alcohol addiction: A matter of choice?
Heilig, M. A., Augier, E., Pfarr, S., & Sommer, W. H. (2019) · Translational Psychiatry · doi:10.1038/s41398-019-0591-6 · Cited by 104
Duan, K., Gu, Q., Petralia, R. S., Wang, Y., Panja, D., Liu, X., Lehmann, M. L., Zhu, H., Zhu, J., & Li, Z. (2021) · Neuron · doi:10.1016/j.neuron.2021.09.008 · Cited by 93
Uematsu, A., Tan, B. Z., & Johansen, J. P. (2015) · Learning & Memory · doi:10.1101/lm.037283.114 · Cited by 89
Sleep Regulation by Neurotensinergic Neurons in a Thalamo-Amygdala Circuit
Ma, C., Zhong, P., Liu, D., Barger, Z., Zhou, L., Chang, W.-C., Kim, B., & Dan, Y. (2019) · Neuron · doi:10.1016/j.neuron.2019.05.015 · Cited by 97
“NTS Is a Marker for CeA Candidate Sleep Neurons The CeA is known to contain multiple subtypes of GABAergic neurons with distinct molecular markers, projection targets, and functional properties (Cai et al., 2014; Carter et al., 2013; Ciocchi et al., 2010; Douglass et al., 2017; Fadok et al., 2017; Haubensak et al., 20…”
BackgroundYoung, K. D., Zotev, V., Phillips, R., Misaki, M., Drevets, W. C., & Bodurka, J. (2018) · Psychiatry and Clinical Neurosciences · doi:10.1111/pcn.12665 · Cited by 83
“The amygdala is strongly connected to a wide variety of brain regions that play key roles in controlling one’s emotional, motivational, and social behavior.(62,81) Amygdala–medial PFC connectivity is considered particularly important for emotion regulation both with respect to decreasing negative affect(36) and increa…”
BackgroundRetrieving fear memories, as time goes by…
Monte, F. H. D., Quirk, G. J., Li, B., & Penzo, M. A. (2016) · Molecular Psychiatry · doi:10.1038/mp.2016.78 · Cited by 98
Crouse, R. B., Kim, K. K. O., Batchelor, H. M., Girardi, E., Kamaletdinova, R., Chan, J., Rajebhosale, P., Pittenger, S. T., Role, L. W., Talmage, D. A., et al. (2020) · eLife · doi:10.7554/elife.57335 · Cited by 98
A human colliculus-pulvinar-amygdala pathway encodes negative emotion
Kragel, P. A., Čeko, M., Theriault, J. E., Chen, D., Satpute, A. B., Wald, L. L., Lindquist, M. A., Barrett, L. F., & Wager, T. D. (2021) · Neuron · doi:10.1016/j.neuron.2021.06.001 · Cited by 101
“However, the pathways identified in animal research reflect communication among spe-cific neural ensembles (Janak and Tye, 2015; Kyriazi et al., 2018) that are not clearly resolved with human neuroimaging.”
BackgroundResultSydnor, V. J., Cieslak, M., Duprat, R., Deluisi, J. A., Flounders, M. W., Long, H., Scully, M., Balderston, N. L., Sheline, Y. I., Bassett, D. S., et al. (2022) · Science Advances · doi:10.1126/sciadv.abn5803 · Cited by 103
Ji, G., Zhang, W. Y., Mahimainathan, L., Narasimhan, M., Kiritoshi, T., Fan, X., Wang, J., Green, T. A., & Neugebauer, V. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.2468-16.2016 · Cited by 92
“BLA projection cells providing direct excitatory or feedforward inhibitory input to CeA neurons belong to different subpopulations (Janak and Tye, 2015).”
BackgroundFrank, M. G., Fonken, L. K., Dolzani, S. D., Annis, J. L., Siebler, P. H., Schmidt, D., Watkins, L. R., Maier, S. F., & Lowry, C. A. (2018) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2018.05.020 · Cited by 101
Human fear conditioning: From neuroscience to the clinic
Fullana, M. A., Dunsmoor, J. E., Schruers, K. R. J., Savage, H. S., Bach, D. R., & Harrison, B. J. (2019) · Behaviour Research and Therapy · doi:10.1016/j.brat.2019.103528 · Cited by 96
Michael, V., Goffinet, J., Pearson, J., Wang, F., Tschida, K., & MOONEY, R. D. (2020) · eLife · doi:10.7554/elife.63493 · Cited by 94
de Abreu, M. S., Demin, K. A., Giacomini, A. C. V. V., Amstislavskaya, T. G., Strekalova, T. V., Maslov, G. O., Kositsin, Y., Petersen, E. V., & Kalueff, A. V. (2021) · Neurobiology of Stress · doi:10.1016/j.ynstr.2021.100405 · Cited by 94
Monoaminergic Modulation of Motor Cortex Function
Vitrac, C., & Benoit‐Marand, M. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00072 · Cited by 94
“Amygdala has a key role on emotions processing and motivation, thus implicating NE in modulating plasticity in function of contextual feeling (Janak and Tye, 2015).”
BackgroundWellman, C. L., Bangasser, D. A., Bollinger, J. L., Coutellier, L., Logrip, M. L., Moench, K. M., & Urban, K. R. (2018) · The Journal of Neuroscience · doi:10.1523/jneurosci.1673-18.2018 · Cited by 88
“The CeA synthesizes inputs from amygdala subdivisions to regulate stress- and rewardrelated behavioral responses (Janak and Tye, 2015); thus, changes in the CeA and associated circuitry have a unique capacity to alter behavior.”
BackgroundWood, J., & Ahmari, S. E. (2015) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2015.00171 · Cited by 85
“Dysregulation of this circuit in OCD could potentially contribute to compulsive behavior. basolateral nuclei to the central nucleus of the amygdala, which functions as an output to numerous brain regions (LeDoux, 2007; Janak and Tye, 2015).”
BackgroundInfluential
Metadata
- Authors
- Janak, P. H., & Tye, K. M.
- Affiliations
- Johns Hopkins University (US)
- Massachusetts Institute of Technology (US)
- Corresponding author
- Janak, Patricia H.
- Tye, Kay M.
- Venue
- Nature
- Published
- 2015-01-14
- Volume
- 517
- Issue
- 7534
- Pages
- 284-292
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC4565157
- OpenAlex
- W1989982790
- Cited by
- 2,011
- References
- 126
- Citations by year
- 2026: 149 · 2025: 193 · 2024: 198 · 2023: 210 · 2022: 207 · 2021: 234 · 2020: 225 · 2019: 172 · 2018: 132 · 2017: 119 · 2016: 114 · 2015: 56
- FWCI
- 13.69
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc-sa)
- PMC
- Funders
- New York Stem Cell Foundation
- JPB Foundation
- National Institutes of Health
- National Institute on Alcohol Abuse and Alcoholism (R01AA014925, AA17072, AA014925, P50AA017072, R01AA016835)
- National Institute of Mental Health (R01MH102441, MH102441, R37MH102441)
- National Institute on Drug Abuse (DA015096, R01DA015096, R01DA035943)
- 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 › Neural and Behavioral Psychology Studies
- Keywords
- amygdala, neural circuits, emotions, motivation, fear, reward, behavioural function, structural connectivity, causal manipulation
- MeSH terms
- Amygdala, Animals, Behavior, Biological Evolution, Fear, Humans, Memory, Neural Pathways, Reward
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