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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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“learning, and for projections from the BLA in particular to mediate fear- and anxiety-behaviors, these effects appear to be mediated distinctly from those of BLA projections to NAc, as the BLA–NAc microcircuit drives reward and reinforcement [36].”
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“Furthermore, the manner in which information is sent to the two regions differs: the BL amygdala receives sensory information, while the CM amygdala is the major output station of the entire amygdala (17;20;21).”
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“…relevant information, consolidation and extinction of emotional memories (particularly those related to traumatic stress), generation of anxiety states, and its role in activation of the sympathetic nervous system (SNS) in the periphery (Duvarci and Pare, 2014; Janak and Tye, 2015; LeDoux, 2007).”
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“Several studies demonstrate that modulation of behaviors in the CeA is cell-type specific, with many studies focusing on the function of genetically distinct cells (Janak and Tye, 2015; Kim et al., 2017).”
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“A prototypical internal state: Fear The abovementioned properties of internal states can be conceptualized in the context of emotion and can be well illustrated using one of the most well-studied states in neuroscience and psychology—fear (Adolphs, 2008; Dukes et al., 2021; Fanselow, 2018; Fanselow and Pennington, 201…”
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“But as described in greater detail elsewhere (Calhoon & Tye, 2015; Gungor & Paré, in press; Janak & Tye, 2015; Shackman & Fox, 2016; Tovote et al., 2015), more recent observations in rodents, monkeys, and humans make it clear that the central extended amygdala forms a tightly interconnected…”
InfluentialIncreased amygdala responses to emotional faces after psilocybin for treatment-resistant depression
Roseman, L., Demetriou, L., Wall, M. B., Nutt, D. J., & Carhart-Harris, R. L. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.12.041 · Cited by 230
“The amygdala is a complex subcortical structure that is sensitive to emotional stimuli (Janak and Tye, 2015; Sergerie et al., 2008).”
Brain circuits for pain and its treatment
Lindsay, N. M., Chen, C., Gilam, G., Mackey, S., & Scherrer, G. (2021) · Science Translational Medicine · doi:10.1126/scitranslmed.abj7360 · Cited by 246
“Over the course of evolution, the size of the BLA versus the CeA within the amygdaloid complex markedly increased (84), evincing the critical importance of the BLA in human emotions and presumably in pain affect.”
BackgroundRoy, D. S., Park, Y.-G., Kim, M. E., Zhang, Y., Ogawa, S. K., DiNapoli, N., Gu, X., Cho, J. H., Choi, H., Kamentsky, L. D., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-29384-4 · Cited by 253
Thompson, J. M., & Neugebauer, V. (2017) · Pain Research and Management · doi:10.1155/2017/8296501 · Cited by 238
“CeA neurons expressing PKCδ (PKCδ) are inhibited by exposure to the fear-conditioned stimulus and have been termed “OFF cells,”, whereas PKCδ-negative neurons are excited when presented with the conditioned stimulus, and reciprocal inhibitory connections exist between these cell types [1, 90, 91].”
BackgroundNavigating the Neural Space in Search of the Neural Code
Jazayeri, M., & Afraz, A. (2017) · Neuron · doi:10.1016/j.neuron.2017.02.019 · Cited by 240
“Many advanced optogenetic experiments aim tomaintain perturbations close to the NMOI by targeting specific signaling pathways (Gradinaru et al., 2010; Janak and Tye, 2015; Yizhar et al., 2011).”
Effects of sleep on memory for conditioned fear and fear extinction.
Pace-Schott, E. F., Germain, A., & Milad, M. R. (2015) · Psychological Bulletin · doi:10.1037/bul0000014 · Cited by 218
“As in other mammals, the human amygdala is involved in the affective labeling of stimuli particularly fear (Janak & Tye, 2015) and interacts continuously with the hippocampus in processing emotional aspects of episodic memories (Fanselow & Dong, 2010; McGaugh, 2004).”
BackgroundPage, C. E., & Coutellier, L. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.07.024 · Cited by 213
Deep brain activities can be detected with magnetoencephalography
Pizzo, F., Roehri, N., Villalon, S. M., Trébuchon, A., Chen, S., Lagarde, S., Carron, R., Gavaret, M., Giusiano, B., McGonigal, A., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-08665-5 · Cited by 222
Cortical and Subcortical Gray Matter Volume in Youths With Conduct Problems
Rogers, J. C., & Brito, S. A. D. (2015) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2015.2423 · Cited by 234
Tran, M. N., Maynard, K. R., Spangler, A., Huuki, L. A., Montgomery, K. D., Sadashivaiah, V., Tippani, M., Barry, B. K., Hancock, D. B., Hicks, S. C., et al. (2021) · Neuron · doi:10.1016/j.neuron.2021.09.001 · Cited by 219
Paquola, C., Bennett, M. R., & Lagopoulos, J. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.08.011 · Cited by 217
Amygdala, neuropeptides, and chronic pain-related affective behaviors
Neugebauer, V., Mazzitelli, M., Cragg, B., Ji, G., Navratilova, E., & Porreca, F. (2020) · Neuropharmacology · doi:10.1016/j.neuropharm.2020.108052 · Cited by 220
Ko, J. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00041 · Cited by 229
“Most of the inputs to the BLA are excitatory glutamatergic inputs (Janak and Tye, 2015).”
BackgroundTwo views on the cognitive brain
Barack, D. L., & Krakauer, J. W. (2021) · Nature reviews. Neuroscience · doi:10.1038/s41583-021-00448-6 · Cited by 230
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
“In particular, given its access to primary sensory information, the CeA could orchestrate appropriate behavioral responses to salient stimuli with different valences [88, 93].”
BackgroundThe mouse prefrontal cortex: Unity in diversity
Le Merre, P., Ährlund-Richter, S., & Carlén, M. (2021) · Neuron · doi:10.1016/j.neuron.2021.03.035 · Cited by 207
Viewpoints: Approaches to defining and investigating fear
Mobbs, D., Adolphs, R., Fanselow, M. S., Barrett, L. F., LeDoux, J. E., Ressler, K., & Tye, K. M. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0456-6 · Cited by 202
Self-citationFace and Voice Perception: Understanding Commonalities and Differences
Young, A. W., Frühholz, S., & Schweinberger, S. R. (2020) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2020.02.001 · Cited by 212
The Cholinergic System, the Adrenergic System and the Neuropathology of Alzheimer’s Disease
Bekdash, R. A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22031273 · Cited by 222
“Cholinergic signaling was also detected in the amygdala, a brain region that plays a role in the consolidation and encoding of emotional memories and α7 nAchR has been shown to induce LTP in the amygdala [47].”
BackgroundA 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 206
“Within the amygdala, information processing and behavioral output occur through highly interconnected subdivisions defined by distinct cell types (Janak and Tye, 2015).”
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
“Acting as a central hub in the brain’s stress circuitry, the amygdala has a central role in conferring resilience and susceptibility to stress-related neuropsychiatric disorders (1,5) and represents a key target for alleviating the symptoms associated with these conditions.”
Remediation of childhood math anxiety and associated neural circuits through cognitive tutoring
Supekar, K., Iuculano, T., Chen, L., & Menon, V. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.0786-15.2015 · Cited by 187
“This view is consistent with evidence, based on optogenetic manipulation in animal models, that such reductions in amygdala hyperactivity and hyperconnectivity are anxiolytic (Janak and Tye, 2015).”
Vainik, U., García‐García, I., & Dagher, A. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14352 · Cited by 202
“Another nucleus, the basolateral complex, sends projections to the nucleus accumbens, putatively influencing food reward processing (Janak & Tye, 2015).”
BackgroundAffective valence in the brain: modules or modes?
Berridge, K. C. (2019) · Nature reviews. Neuroscience · doi:10.1038/s41583-019-0122-8 · Cited by 196
Molecular mechanisms underlying alcohol-drinking behaviours
Ron, D., & Barak, S. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2016.85 · Cited by 165
“The extended amygdala includes major components of the stress regulatory sys-tem of the brain, which also have a major role in negative reinforcement, in which alcohol intake serves to suppress negative states, to control behaviour 4,64 .”
Amygdala-hippocampal dynamics during salient information processing
Zheng, J., Anderson, K. L., Leal, S. L., Shestyuk, A. Y., Gülşen, G., Mnatsakanyan, L., Vadera, S., Hsu, F. P. K., Yassa, M. A., Knight, R. T., et al. (2017) · Nature Communications · doi:10.1038/ncomms14413 · Cited by 190
“To label these sub-regions of the amygdala, three key points were identified: (1) the medial tip of the alveus (up to the optic tract); (2) the most lateral point of the entorhinal sulcus; and (3) bottom of the circular sulcus.”
BackgroundMethodApathy and anxiety are early markers of Alzheimer's disease
Johansson, M., Stomrud, E., Lindberg, O. E., Westman, E., Johansson, P., van Westen, D., Mattsson, N., & Hansson, O. (2019) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2019.10.008 · Cited by 192
Tang, S., Lu, L., Zhang, L., Hu, X., Bu, X., Li, H., Hu, X., Gao, Y., Zeng, Z., Gong, Q., et al. (2018) · EBioMedicine · doi:10.1016/j.ebiom.2018.09.010 · Cited by 187
“The amygdala is adjacent to the hippocampus within the medial temporal lobe, and they are richly connected with each other [37,38].”
BackgroundA distributed fMRI-based signature for the subjective experience of fear
Zhou, F., Zhao, W., Qi, Z., Geng, Y., Yao, S., Kendrick, K. M., Wager, T. D., & Becker, B. (2021) · Nature Communications · doi:10.1038/s41467-021-26977-3 · Cited by 155
Research Review: Pediatric Anxiety Disorders—What Have We Learnt in the Last 10 Years?
Strawn, J. R., Lu, L., Peris, T. S., Levine, A., & Walkup, J. T. (2021) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.13262 · Cited by 168
Multidimensional processing in the amygdala
Gothard, K. M. (2020) · Nature reviews. Neuroscience · doi:10.1038/s41583-020-0350-y · Cited by 178
Herman, J. P., Nawreen, N., Smail, M. A., & Cotella, E. M. (2020) · Stress · doi:10.1080/10253890.2020.1859475 · Cited by 190
Morel, C., Montgomery, S. E., Li, L., Cuttoli, R. D.-D., Teichman, E. M., Juarez, B., Tzavaras, N., Ku, S. M., Flanigan, M. E., Cai, M., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-29155-1 · Cited by 178
Zhang, J.-E., Tan, L., Ren, Y., Liang, J., Lin, R., Feng, Q., Zhou, J., Hu, F., Ren, J., Wei, C., et al. (2016) · Cell · doi:10.1016/j.cell.2016.06.026 · Cited by 170
Kofuji, P., & Araque, A. (2021) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-101920-112225 · Cited by 171
Venniro, M., Caprioli, D., Zhang, M., Whitaker, L. R., Zhang, S., Warren, B. L., Cifani, C., Marchant, N. J., Yizhar, O., Bossert, J. M., et al. (2017) · Neuron · doi:10.1016/j.neuron.2017.09.024 · Cited by 162
Neuropathology of suicide: Recent findings and future directions
Lutz, P.-E., Mechawar, N., & Turecki, G. (2017) · Molecular Psychiatry · doi:10.1038/mp.2017.141 · Cited by 158
Cortical ensembles orchestrate social competition through hypothalamic outputs
Padilla-Coreano, N., Batra, K., Patarino, M., Chen, Z., Rock, R. R., Zhang, R., Hausmann, S. B., Weddington, J., Patel, R. R., Zhang, Y. E., et al. (2022) · Nature · doi:10.1038/s41586-022-04507-5 · Cited by 162
Self-citationNoradrenergic dysregulation in the pathophysiology of PTSD
Hendrickson, R. C., & Raskind, M. A. (2016) · Experimental Neurology · doi:10.1016/j.expneurol.2016.05.014 · Cited by 183
Left and right hemispheric lateralization of the amygdala in pain
Allen, H. N., Bobnar, H. J., & Kolber, B. J. (2020) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2020.101891 · Cited by 151
“The amygdala consists of the lateral, basolateral, central, and medial nuclei (Janak and Tye, 2015).”
Background
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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