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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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“The amygdala, tightly nestled on top of and densely interconnected with the hippocampus, plays an essential role in emotional processing, affective/mood state, fear conditioning and extinction and social behaviours (Fox and Shackman, 2019; Hur et al., 2019; Janak and Tye, 2015; Lindquist et al., 2012; Putnam and Chang…”
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“It is known that mPFC projection neurons send immense outputs to the basolateral amygdala (BLA), a region critical for emotion control (17, 18).”
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“whereas the LA/BLA receive polymodal sensory information via cortical afferents coursing into the region from the EC(89) and form the primary input nuclei in the amygdala’s emotion-related neural circuitry.(45) Here, the highly integrated stress-affective–related information is then transmitted to the CeA to mediate t…”
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“The amygdala nuclei are functionally associated with mental disorders including multiple anxiety disorders, addiction, and autism (Janak and Tye, 2015).”
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“In addition, the amygdala is also involved in modulating attention and evaluating environmental stimuli in terms of their emotional relevance [80,88].”
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“…regions onto inhibitory interneurons and intercalated cell masses within and around BLA tend to provide control over BLA output cells, thus effectively reducing downstream affective outputs of BLA (Asede, et al., 2015; Duvarci and Pare, 2014; Ehrlich, et al., 2009; Janak and Tye, 2015).”
BackgroundLOONEN, A. J. M., & Ivanova, S. А. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2016.00539 · Cited by 69
“A major role is played by the deep corticoid complex (mainly basolateral nuclei) in bidirectional interaction with the prefrontal cortical areas, the hippocampal complex as well as sensory cortical areas (Janak and Tye, 2015; Rutishauser et al., 2015; Wassum and Izquierdo, 2015; Benarroch, 2015a; McDonald and Mott, 20…”
BackgroundNagayoshi, Y., Chujo, T., Hirata, S., Nakatsuka, H., Chen, C.-W., Takakura, M., Miyauchi, K., Ikeuchi, Y., Carlyle, B. C., Kitchen, R. R., et al. (2021) · Science Advances · doi:10.1126/sciadv.abf3072 · Cited by 69
“Other brain regions, such as the amygdala and cerebellum, are also involved in the learning and memory (47, 48) and may also be affected by Ftsj1 deficiency.”
BackgroundImaging the Limbic System in Parkinson’s Disease—A Review of Limbic Pathology and Clinical Symptoms
Banwinkler, M., Theis, H., Prange, S., & van Eimeren, T. (2022) · Brain Sciences · doi:10.3390/brainsci12091248 · Cited by 70
“Unidirectional outputs encompass the striatum, nucleus accumbens, and the bed nucleus of the stria terminalis, which are involved in translating the input signals into behavioral outputs [25,26].”
BackgroundGABAergic Neurons of the Central Amygdala Promote Cataplexy
Mahoney, C. E., Agostinelli, L. J., Brooks, J. N. K., Lowell, B. B., & Scammell, T. E. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.4065-15.2017 · Cited by 69
“Similar increases in amygdala activity to both positive and aversive stimuli are best explained by the intermingling of distinct neuronal populations with specific connectivity (Shabel and Janak, 2009; Janak and Tye, 2015; Namburi et al., 2015).”
BackgroundOzawa, M., Davis, P. W., Ni, J., Maguire, J. L., Papouin, T., & Reijmers, L. G. J. E. (2020) · Nature Communications · doi:10.1038/s41467-020-18199-w · Cited by 61
An 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
“The main input structure of the amygdala, the basolateral nucleus (BLA), has been shown to be involved in the learning of contextual information related to appetitive and aversive experiences (Phillips and LeDoux, 1992; Herry et al., 2008; Janak and Tye, 2015; Namburi et al., 2015; Beyeler et al., 2016; Kim et al., 20…”
GABAergic implications in anxiety and related disorders
Arora, I., Mal, P., Arora, P., Paul, A., & Kumar, M. (2024) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2024.150218 · Cited by 74
Control of Long-Term Plasticity by Glutamate Transporters
Valtcheva, S., & Venance, L. (2019) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2019.00010 · Cited by 64
“In vivo EAAT2 blockade by DHK in the infralimbic part of the prefrontal cortex (John et al., 2012) or intracerebroventricular infusion of DHK (Bechtholt-Gompf et al., 2010) results in depressive-like behaviors and anhedonia, which are translated by a reduction in motivation and reward-seeking.”
BackgroundGiovanniello, J., Yu, K., Furlan, A., Nachtrab, G. T., Sharma, R., Chen, X., & Li, B. (2020) · The Journal of Neuroscience · doi:10.1523/jneurosci.2090-20.2020 · Cited by 65
“Extensive studies, exemplified by those focusing on Pavlovian fear conditioning, have shown that the CeA plays important roles in the establishment of adaptive defensive behaviors (Duvarci and Pare, 2014; Herry and Johansen, 2014; Janak and Tye, 2015; Fadok et al., 2018; Li, 2019).”
BackgroundLearning dynamics of electrophysiological brain signals during human fear conditioning
Sperl, M. F. J., Wroblewski, A., Mueller, M., Straube, B., & Mueller, E. M. (2020) · NeuroImage · doi:10.1016/j.neuroimage.2020.117569 · Cited by 65
Ensemble coding in amygdala circuits for associative learning
Gründemann, J., & Lüthi, A. (2015) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2015.10.005 · Cited by 68
Ye, J., & Veinante, P. (2019) · Brain Structure and Function · doi:10.1007/s00429-018-01825-1 · Cited by 68
Subba, R., Sandhir, R., Singh, S. P., Mallick, B. N., & Mondal, A. C. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15136 · Cited by 69
“The amygdala is associated with emotion, fear, motivation, and reward (Janak & Tye, 2015) and is implicated in diabetes- associated cognitive and mood disturbances (McNay, 2015).”
BackgroundNeural systems that facilitate the representation of social rank
Dwortz, M. F., Curley, J. P., Tye, K. M., & Padilla-Coreano, N. (2022) · Philosophical Transactions of the Royal Society B · doi:10.1098/rstb.2020.0444 · Cited by 64
“It should be noted that other neuropeptides, serotonin and OT, are also important for social reward learning within this circuit in mice [59,60].”
BackgroundSelf-citationDifferential Activation Patterns in the Same Brain Region Led to Opposite Emotional States
Shibata, K., Watanabe, T., Kawato, M., & Sasaki, Y. (2016) · PLoS Biology · doi:10.1371/journal.pbio.1002546 · Cited by 59
“In animal studies, the importance of a role of activity of a certain group of neurons in a region rather than mean activity of the region has been observed [1,2].”
BackgroundSeno, M. D. D. J., de Assis, D. V., Gouveia, F. V., Antunes, G. F., Kuroki, M. A., de Oliveira, C. C., dos Santos, L. C. T., Pagano, R. L., & Martinez, R. C. R. (2018) · Scientific Reports · doi:10.1038/s41598-018-31962-w · Cited by 63
Centanni, S. W., Bedse, G., Patel, S., & Winder, D. G. (2019) · Alcoholism: Clinical and Experimental Research · doi:10.1111/acer.14178 · Cited by 58
“In addition, the CeA and BNST send and receive numerous cortical and subcortical projections synapsing onto cells in different subnuclei, and onto either GABAergic interneurons or output neurons (Dong et al., 2001, Janak and Tye, 2015).”
BackgroundZhou, 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
Blood Pressure in Seizures and Epilepsy
Nass, R. D., Hampel, K. G., Elger, C. E., & Surges, R. (2019) · Frontiers in Neurology · doi:10.3389/fneur.2019.00501 · Cited by 64
“The amygdala comprises multiple interconnected nuclei deeply nested in the temporal lobe (37).”
BackgroundNeurotensin in reward processes
Torruella-Suárez, M. L., & McElligott, Z. A. (2020) · Neuropharmacology · doi:10.1016/j.neuropharm.2020.108005 · Cited by 63
“While originally associated with aversive associative learning, more recent work has appreciated it as a region that encodes both positive and negative emotional valence (Janak and Tye, 2015).”
BackgroundInterneuron Types and Their Circuits in the Basolateral Amygdala
Hájos, N. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.687257 · Cited by 66
“In spite of a separate role for LA and BA in certain cognitive processes (Janak and Tye, 2015; Manassero et al., 2018), there is no evidence to date of the presence of different cell types or distinct wiring principles in these two amygdalar nuclei.”
BackgroundMulder, D., Aarts, E., Vásquez, A. A., & Bloemendaal, M. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02146-4 · Cited by 70
“Alpha diversity reflects within-sample diversity, expressed in the number of different types of bacteria a sample or group contains (richness) and how equal the abundance of these bacteria is distributed within a sample or group (evenness).”
BackgroundGlutamatergic plasticity and alcohol dependence-induced alterations in reward, affect and cognition
Burnett, E. J., Chandler, L. J., & Trantham‐Davidson, H. (2015) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2015.08.012 · Cited by 66
“Its projections to the NAc, CeA and BNST provide a path through which this sensory information can be transformed into a behavioral response (Figure 1) (Janak and Tye, 2015).”
Alcohol‐dependent molecular adaptations of the NMDA receptor system
Morisot, N., & Dorit Ron, A. (2016) · Genes Brain & Behavior · doi:10.1111/gbb.12363 · Cited by 61
“…and memory-dependent mechanisms such as goal-directed (Yin & Knowlton 2006), reward learning (Sesack & Grace 2010) and anxiety-related behaviors (Janak & Tye 2015), thus, future directions will be required to link these signaling cascades to specific circuitries that contribute to the behavior.”
BackgroundNeural Circuit Mechanisms Underlying Emotional Regulation of Homeostatic Feeding
Sweeney, P., & Yang, Y. (2017) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2017.02.006 · Cited by 67
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 65
“Such preferential wiring indicates that associative learning is processed through innate circuits capable of linking negative or positive emotions to neutral sensory stimuli in the service of biasing behaviors in an adaptive manner (Janak and Tye, 2015).”
BackgroundRisal, S., Manti, M., Lu, H., Fornes, R., Larsson, H., Benrick, A., Deng, Q., Cesta, C. E., Rosenqvist, M. A., & Stener‐Victorin, E. (2021) · Translational Psychiatry · doi:10.1038/s41398-020-01183-9 · Cited by 61
Modulating reconsolidation: a link to causal systems-level dynamics of human memories
Sandrini, M., Cohen, L. G., & Censor, N. (2015) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2015.06.002 · Cited by 67
Ventral Tegmental Area Afferents and Drug-Dependent Behaviors
Oliva, I., & Wanat, M. J. (2016) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2016.00030 · Cited by 68
“The CeA contains predominantly GABA neurons and is involved with fear conditioning (187, 188, 190), as well as with mediating the general motivational influence”
BackgroundNeurobiological candidate endophenotypes of social anxiety disorder
Bas‐Hoogendam, J. M., Blackford, J. U., Brühl, A. B., Blair, K. S., van der Wee, N. J. A., & Westenberg, P. M. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.08.040 · Cited by 68
Massaly, N., Morón, J. A., & Al-Hasani, R. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2016.00480 · Cited by 59
“The amygdala is very much involved in the processing of both positive and negative valence (see review Janak and Tye, 2015).”
BackgroundConserved features of anterior cingulate networks support observational learning across species
Burgos-Robles, A., Gothard, K. M., Monfils, M., Morozov, A., & Vicentic, A. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.09.009 · Cited by 64
“The amygdala, especially the basolateral nuclei (including in rodents the lateral, basolateral, and basomedial regions; which from now on we will refer to as the “BLA”) is unequivocally fundamental for learning fear associations through classical conditioning methods in which direct experience of punishment is require…”
BackgroundHierarchical models of pain: Inference, information-seeking, and adaptive control.
Seymour, B., & Mancini, F. (2020) · NeuroImage · doi:10.1016/j.neuroimage.2020.117212 · Cited by 59
“…learning processes (e.g. cerebellar learning of precisely timed motor limb withdrawal or eye-blink responses ( Zhang et al., 2016 ; Ernst et al., 2019 ), and amygdalar learning of autonomic responses, freezing and other generalised aversive responses ( Herry et al., 2014 ; Janak et al., 2015 )).”
Total Number and Ratio of GABAergic Neuron Types in the Mouse Lateral and Basal Amygdala
Vereczki, V., Müller, K., Krizsán, É., Máté, Z., Fekete, Z., Rovira-Esteban, L., Veres, J. M., Erdélyi, F., & Hájos, N. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.2700-20.2021 · Cited by 65
Role of Wnt signaling in synaptic plasticity and memory
Narvaes, R. F., & Furini, C. R. G. (2021) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2021.107558 · Cited by 65
A network of amygdala connections predict individual differences in trait anxiety
Greening, S. G., & Mitchell, D. G. V. (2015) · Human Brain Mapping · doi:10.1002/hbm.22952 · Cited by 70
“Furthermore, it is noteworthy that the amygdala, rather than acting as a homogenous unit, is made up of multiple functionally heterogeneous nuclei that can make different or even opposing functional contributions [Amaral, 2002; Janak and Tye, 2015].”
BackgroundMalvaez, M., Greenfield, V. Y., Wang, A. S., Yorita, A. M., Feng, L., Linker, K. E., Monbouquette, H. G., & Wassum, K. M. (2015) · Scientific Reports · doi:10.1038/srep12511 · Cited by 61
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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