From circuits to behaviour in the amygdala

Janak, Patricia H.; Tye, Kay M.

doi:10.1038/nature14188

Cited by 2,011Memory and Neural MechanismsNeuroscience and Neuropharmacology ResearchNeural and Behavioral Psychology Studies

From circuits to behaviour in the amygdala

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Janak, Patricia H., Tye, Kay M.·2015·Nature

DOI 10.1038/nature14188PMC PMC4565157

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Abstract

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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Alterations in the HPA axis have been associated with the process of dealing with stress, especially toxic stress-induced negative health outcomes.
“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]
The ‘Beyond fear in the amygdala’ passage discusses neural circuits and anxiety, not HPA-axis alterations or health outcomes. Searches for HPA-axis terms, toxic stress, and related endocrine terms found no passage in our copy addressing the attributed association. (LLM, conf=0.75)
Experimental — accuracy not yet measured
The amygdala promotes adaptive behavioral responses to both positive and negative environmental stimuli.
“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
The amygdala also regulates anxiety.
“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
Aberrant communication of anxiety-related information from amygdala to VS could mediate anxiety-driven compulsive behavior.
“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
The BNST and the CeA have been implicated in diverse behavioral functions.
“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

The CeA could orchestrate appropriate behavioral responses to salient stimuli with different valences.
“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]
Processing of sensory information in the BLA results in the formation of associations between neutral predictive stimuli and outcomes of positive or negative valence via Hebbian mechanisms.
“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]
Interpretation is in part dictated by the individual's previous experience and includes the assignment of valence to the stimulus via BLA circuits.
“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]
The valence detection function of BLA projection neurons fits within the interpretation circuits described here, helping to determine whether a given stimulus is threatening or appetitive.
“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]
The BLA is critical for associative learning.
“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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Marowsky, A., Yanagawa, Y., Obata, K., & Vogt, K. E. (2005) · Neuron · doi:10.1016/j.neuron.2005.10.029 · Cited by 328 · see citing works
Emotion, decision making, and the amygdala.
Seymour, B., & Dolan, R. (2008) · Neuron · doi:10.1016/j.neuron.2008.05.020 · Cited by 324 · see citing works
Optical activation of lateral amygdala pyramidal cells instructs associative fear learning
Johansen, J. P., Hamanaka, H., Monfils, M. H., Behnia, R., Deisseroth, K., Blair, H. T., & LeDoux, J. E. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1002418107 · Cited by 308 · see citing works
Excitotoxic lesions of the amygdala fail to produce impairment in visual learning for auditory secondary reinforcement but interfere with reinforcer devaluation effects in rhesus monkeys
Málková, L., Gaffan, D., & Murray, E. A. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-15-06011.1997 · Cited by 295 · see citing works
Visual responses of neurons in the dorsolateral amygdala of the alert monkey.
Sanghera, M., Rolls, E., & Roper-Hall, A. (1979) · Experimental Neurology · doi:10.1016/0014-4886(79)90175-4 · Cited by 287 · see citing works
Damage to the Lateral and Central, but Not Other, Amygdaloid Nuclei Prevents the Acquisition of Auditory Fear ConditioningPreprint
Nader, K., Majidishad, P., Amorapanth, P., & LeDoux, J. E. (2001) · Learning & Memory · doi:10.1101/lm.38101 · Cited by 272 · see citing works
XI. An investigation into the functions of the occipital and temporal lobes of the monkey's brain
Brown, S., & Schäfer, E. A. (1888) · Philosophical Transactions of the Royal Society of London (B ) · doi:10.1098/rstb.1888.0011 · Cited by 263 · see citing works
Synaptic organization of projections from the amygdala to visual cortical areas TE and V1 in the macaque monkey
Freese, J. L., & Amaral, D. G. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.20945 · Cited by 242 · see citing works
Double dissociation of the effects of lesions of basolateral and central amygdala on conditioned stimulus‐potentiated feeding and Pavlovian‐instrumental transfer
Holland, P. C., & Gallagher, M. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02585.x · Cited by 236 · see citing works
The lateral nucleus of the amygdala mediates expression of the amphetamine-produced conditioned place preference
Hiroi, N., & White, N. (1991) · Journal of Neuroscience · doi:10.1523/jneurosci.11-07-02107.1991 · Cited by 228 · see citing works
The organization of projections from the amygdala to visual cortical areas TE and V1 in the macaque monkey
Freese, J. L., & Amaral, D. G. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20520 · Cited by 228 · 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
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Rapid Associative Encoding in Basolateral Amygdala Depends on Connections with Orbitofrontal Cortex
Saddoris, M. P., Gallagher, M., & Schoenbaum, G. M. (2005) · Neuron · doi:10.1016/j.neuron.2005.02.018 · Cited by 214 · see citing works
Substantial similarity in amygdala neuronal activity during conditioned appetitive and aversive emotional arousal
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
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Fear Conditioning Potentiates Synaptic Transmission onto Long-Range Projection Neurons in the Lateral Subdivision of Central Amygdala
Penzo, M. A., Robert, V., & Li, B. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.4166-13.2014 · Cited by 187 · see citing works
Surprise! Neural correlates of Pearce–Hall and Rescorla–Wagner coexist within the brain
Roesch, M. R., Esber, G. R., Li, J., Daw, N. D., & Schoenbaum, G. M. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07986.x · Cited by 186 · see citing works
Medial prefrontal D1 dopamine neurons control food intake
Land, B. B., Narayanan, N. S., Liu, R.-J., Gianessi, C. A., Brayton, C. E., Grimaldi, D. M., Sarhan, M., Guarnieri, D. J., Deisseroth, K. A., Aghajanian, G. K., et al. (2014) · Nature Neuroscience · doi:10.1038/nn.3625 · Cited by 180 · see citing works
Neuronal responsiveness to various sensory stimuli, and associative learning in the rat amygdala.
Uwano, T., Nishijo, H., Ono, T., & Tamura, R. (1995) · Neuroscience · doi:10.1016/0306-4522(95)00125-3 · Cited by 176 · see citing works
Disruption of alcohol-related memories by mTORC1 inhibition prevents relapse
Barak, S., Liu, F., Hamida, S. B., Yowell, Q. V., Neasta, J., Kharazia, V., Janak, P. H., & Ron, D. (2013) · Nature Neuroscience · doi:10.1038/nn.3439 · Cited by 172 · see citing works
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Differential Fear Conditioning Induces Reciprocal Changes in the Sensory Responses of Lateral Amygdala Neurons to the CS<sup>+</sup> and CS<sup>−</sup>
Collins, D. R., & Paré, D. (2000) · Learning & Memory · doi:10.1101/lm.7.2.97 · Cited by 171 · see citing works
Fear extinction causes target-specific remodeling of perisomatic inhibitory synapses
Trouche, S., Sasaki, J. M., Tu, T., & Reijmers, L. (2013) · Neuron · doi:10.1016/j.neuron.2013.07.047 · Cited by 166 · see citing works
The Role of an Amygdalo-Nigrostriatal Pathway in Associative Learning
Han, J., McMahan, R. W., Holland, P. C., & Gallagher, M. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-10-03913.1997 · Cited by 154 · 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
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A triple dissociation of memory systems: Hippocampus, amygdala, and dorsal striatum.
McDonald, R., & White, N. (1993) · Behavioral Neuroscience · doi:10.1037/a0034883 · Cited by 146 · see citing works
Auditory fear conditioning increases CS‐elicited spike firing in lateral amygdala neurons even after extensive overtraining
Maren, S. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.00281.x · Cited by 139 · see citing works
Stereological analysis of the rat and monkey amygdala
Chareyron, L. J., Lavenex, P. B., Amaral, D. G., & Lavenex, P. (2011) · The Journal of Comparative Neurology · doi:10.1002/cne.22677 · Cited by 137 · see citing works
The Central Amygdala and Alcohol: Role of -Aminobutyric Acid, Glutamate, and NeuropeptidesPreprint
Roberto, M., Gilpin, N. W., & Siggins, G. R. (2012) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a012195 · Cited by 136 · see citing works
Amygdala and bed nucleus of the stria terminalis circuitry: Implications for addiction-related behaviors
Stamatakis, A. M., Sparta, D. R., Jennings, J. H., McElligott, Z. A., Decot, H., & Stuber, G. D. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.05.046 · Cited by 132 · see citing works
Safety Encoding in the Basal Amygdala
Sangha, S., Chadick, J. Z., & Janak, P. H. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.3302-12.2013 · Cited by 131 · see citing works
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Manipulating a “Cocaine Engram” in Mice
Hsiang, H.-L. (., Epp, J. R., van den Oever, M. C., Yan, C., Rashid, A. J., Insel, N., Ye, L., Niibori, Y., Deisseroth, K., Frankland, P. W., et al. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.3327-14.2014 · Cited by 131 · see citing works
Amygdala Neurons Differentially Encode Motivation and Reinforcement
Tye, K. M., & Janak, P. H. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.5281-06.2007 · Cited by 130 · see citing works
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Optogenetic dissection of basolateral amygdala projections during cue-induced reinstatement of cocaine seeking
Stefanik, M. T., & Kalivas, P. W. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00213 · Cited by 121 · see citing works
Different Time Courses for Learning-Related Changes in Amygdala and Orbitofrontal Cortex
Morrison, S. E., Saez, A., Lau, B., & Salzman, C. D. (2011) · Neuron · doi:10.1016/j.neuron.2011.07.016 · Cited by 121 · see citing works
Visualizing an emotional valence map in the limbic forebrain by TAI-FISH
Xiu, J., Zhang, Q., Zhou, T., Zhou, T.-T., Chen, Y., & Hu, H. (2014) · Nature Neuroscience · doi:10.1038/nn.3813 · Cited by 112 · see citing works
Posttraining optogenetic manipulations of basolateral amygdala activity modulate consolidation of inhibitory avoidance memory in rats
Huff, M. L., Miller, R. L., Deisseroth, K., Moorman, D. E., & LaLumiere, R. T. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1219593110 · Cited by 104 · see citing works
Identification of the reptilian basolateral amygdala: an anatomical investigation of the afferents to the posterior dorsal ventricular ridge of the lizard Podarcis hispanica
Lanuza, E., Belekhova, M. G., Martı́nez-Marcos, A., Font, C., & Martínez‐Garciá, F. (1998) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1998.00363.x · Cited by 85 · see citing works
Inhibition of projections from the basolateral amygdala to the entorhinal cortex disrupts the acquisition of contextual fear
Sparta, D. R., Smithuis, J., Stamatakis, A. M., Jennings, J. H., Kantak, P. A., Ung, R. L., & Stuber, G. D. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00129 · Cited by 75 · 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
Unilateral inactivation of the basolateral amygdala attenuates context‐induced renewal of Pavlovian‐conditioned alcohol‐seeking
Chaudhri, N., Woods, C. A., Sahuque, L. L., Gill, T. M., & Janak, P. H. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12278 · Cited by 73 · see citing works
Self-citation
Amygdala neural activity reflects spatial attention towards stimuli promising reward or threatening punishment
Peck, C. J., & Salzman, C. D. (2014) · eLife · doi:10.7554/elife.04478 · Cited by 66 · see citing works
NMDA-dependent facilitation of corticostriatal plasticity by the amygdala
Popescu, A. T., Saghyan, A. A., & Paré, D. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0609831104 · Cited by 62 · see citing works
Amygdala Mechanisms of Pavlovian Psychostimulant Conditioning and Relapse
Buffalari, D. M., & See, R. E. (2009) · Current topics in behavioral neurosciences · doi:10.1007/7854_2009_18 · Cited by 36 · see citing works
Similar Neural Activity during Fear and Disgust in the Rat Basolateral Amygdala
Shabel, S. J., Schairer, W. W., Donahue, R. J., Powell, V. E., & Janak, P. H. (2011) · PLoS ONE · doi:10.1371/journal.pone.0027797 · Cited by 17 · see citing works
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[62]Kim S-Y Diverging neural pathways assemble a behavioural state from separable features in anxiety Nature 2013 496 219 223 23515158 PMC6690364

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Stress & the gut-brain axis: Regulation by the microbiome
Foster, J. A., Rinaman, L., & Cryan, J. F. (2017) · Neurobiology of Stress · doi:10.1016/j.ynstr.2017.03.001 · Cited by 1,150 · see citing works
“Altered amygdalar processes are associated with a variety of neuropsychiatric disorders, ranging from autism spectrum (Schumann and Amaral, 2006; Mosconi et al., 2009) to anxiety disorders (LeDoux, 2007; Janak and Tye, 2015).”
A Comprehensive Overview on Stress Neurobiology: Basic Concepts and Clinical Implications
Godoy, L. D., Rossignoli, M. T., Delfino-Pereira, P., Garcia‐Cairasco, N., & Umeoka, E. H. D. L. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00127 · Cited by 884 · see citing works
Gut instincts: microbiota as a key regulator of brain development, ageing and neurodegeneration
Dinan, T. G., & Cryan, J. F. (2017) · The Journal of Physiology · doi:10.1113/jp273106 · Cited by 813 · see citing works
“Structural and functional changes in the amygdala are associated with a variety of neuropsychiatric disorders ranging from autism spectrum (Schumann & Amaral, 2006; Mosconi et al. 2009) to anxiety disorders (Ledoux, 2007; Janak & Tye, 2015).”
Background
Topographic organization of the human subcortex unveiled with functional connectivity gradients
Tian, Y., Margulies, D. S., Breakspear, M. J., & Zalesky, A. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-00711-6 · Cited by 781 · see citing works
Resolving the neural circuits of anxiety
Calhoon, G. G., & Tye, K. M. (2015) · Nature Neuroscience · doi:10.1038/nn.4101 · Cited by 766 · see citing works
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Basal Forebrain Cholinergic Circuits and Signaling in Cognition and Cognitive Decline
Ballinger, E. C., Ananth, M. R., Talmage, D. A., & Role, L. W. (2016) · Neuron · doi:10.1016/j.neuron.2016.09.006 · Cited by 735 · see citing works
“Specifically, we discuss recent work on the role of cholinergic signaling in spatial memory, which heavily engages the hippocampus, and in emotionally salient memories, with a focus on studies in the amygdala (Burgess et al., 2002; Janak and Tye, 2015).”
Neurobiological Interactions Between Stress and the Endocannabinoid System
Morena, M., Patel, S., Bains, J. S., & Hill, M. N. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.166 · Cited by 663 · see citing works
“…as the central amygdala (CeA), medial amygdala, bed nucleus of the stria terminalis (BNST), nucleus accumbens, and distinct hypothalamic nuclei such as the lateral, anterior, and dorsomedial hypothalamus (Hermans et al, 2014b; Janak and Tye, 2015; Ulrich-Lai and Herman, 2009; Veinante et al, 2013).”
Background
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
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Explicit and implicit emotion regulation: a multi-level framework
Braunstein, L. M., Gross, J. J., & Ochsner, K. N. (2017) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsx096 · Cited by 539 · see citing works
“…responses to goal-relevant stimuli in general and potential threats in particular (Phelps, 2006; Davis and Whalen, 2001; Cunningham and Brosch, 2012; Janak and Tye, 2015); the ventral striatum, involved in learning the reinforcement/reward value of stimuli (O’doherty, 2004; Delgado, 2007) and the…”
Background
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
“This region receives sensory inputs of multiple modalities, and projects to output structures controlling behavioral responses (Janak and Tye, 2015; McDonald, 1998).”
Understanding Emotions: Origins and Roles of the Amygdala
Šimić, G., Tkalčić, M., Vukić, V., Mulc, D., Španić, E., Šagud, M., Olucha-Bordonau, F. E., Vukšić, M., & Hof, P. R. (2021) · Biomolecules · doi:10.3390/biom11060823 · Cited by 556 · see citing works
“One of the key features of anxiety disorders is the inability to suppress fear appropriately in situations that do not pose a real danger [102].”
Background
Circuits and functions of the lateral habenula in health and in disease
Hu, H., Cui, Y., & Yang, Y. (2020) · Nature reviews. Neuroscience · doi:10.1038/s41583-020-0292-4 · Cited by 471 · see citing works
Brain circuit dysfunction in post-traumatic stress disorder: from mouse to man
Fenster, R. J., Lebois, L. A. M., Ressler, K. J., & Suh, J. (2018) · Nature Reviews Neuroscience · doi:10.1038/s41583-018-0039-7 · Cited by 456 · see citing works
Divergent routing of positive and negative information from the amygdala during memory retrieval
Beyeler, A., Namburi, P., Glober, G. F., Simonnet, C., Calhoon, G. G., Conyers, G. F., Luck, R., Wildes, C. P., & Tye, K. M. (2016) · Neuron · doi:10.1016/j.neuron.2016.03.004 · Cited by 412 · 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-citation
Antagonistic negative and positive neurons of the basolateral amygdala
Kim, J., Pignatelli, M., Xu, S., Itohara, S., & Tonegawa, S. (2016) · Nature Neuroscience · doi:10.1038/nn.4414 · Cited by 450 · see citing works
Detecting Activated Cell Populations Using Single-Cell RNA-Seq
Wu, Y. E., Pan, L., Zuo, Y., Li, X., & Hong, W. (2017) · Neuron · doi:10.1016/j.neuron.2017.09.026 · Cited by 438 · see citing works
The Parabrachial Nucleus: CGRP Neurons Function as a General Alarm
Palmiter, R. D. (2018) · Trends in Neurosciences · doi:10.1016/j.tins.2018.03.007 · Cited by 442 · see citing works
Thirst-associated preoptic neurons encode an aversive motivational drive.
Allen, W. E., DeNardo, L. A., Chen, M. Z., Liu, C. D., Loh, K. M., Fenno, L. E., Ramakrishnan, C., Deisseroth, K., & Luo, L. (2017) · Science · doi:10.1126/science.aan6747 · Cited by 390 · see citing works
Dark microglia: A new phenotype predominantly associated with pathological states
Bisht, K., Sharma, K. P., Lecours, C., Gabriela Sánchez, M., El Hajj, H., Milior, G., Olmos‐Alonso, A., Gómez‐Nicola, D., Luheshi, G., Vallières, L., et al. (2016) · Glia · doi:10.1002/glia.22966 · Cited by 421 · see citing works
“3H).”
Bidirectional modulation of anxiety-related and social behaviors by amygdala projections to the medial prefrontal cortex
Felix‐Ortiz, A. C., Burgos-Robles, A., Bhagat, N. D., Leppla, C. A., & Tye, K. M. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.07.041 · Cited by 414 · see citing works
“The mPFC has also been shown to represent social interactions, with some populations of neurons exhibiting increased activity and others showing decreased activity during bouts of social interaction (Jodo et al., 2010).”
Self-citation
Neuromodulation by the immune system: a focus on cytokines
Salvador, A. F., de Lima, K. A., & Kipnis, J. (2021) · Nature Reviews Immunology · doi:10.1038/s41577-021-00508-z · Cited by 389 · see citing works
An amygdalar neural ensemble that encodes the unpleasantness of pain
Corder, G. F., Ahanonu, B., Grewe, B. F., Wang, D., Schnitzer, M. J., & Scherrer, G. (2019) · Science · doi:10.1126/science.aap8586 · Cited by 406 · see citing works
Dorsal raphe dopamine neurons represent the experience of social isolation
Matthews, G. A., Nieh, E. H., Vander Weele, C. M., Halbert, S. A., Pradhan, R. V., Yosafat, A. S., Glober, G. F., Izadmehr, E. M., Thomas, R. E., Lacy, G. D., et al. (2016) · Cell · doi:10.1016/j.cell.2015.12.040 · Cited by 402 · see citing works
“The BNST and the CeA have been implicated in diverse behavioral functions (Davis et al., 2010; Janak and Tye, 2015; Kim et al., 2013), and DA receptor signaling in these regions modulates synaptic transmission and activity (Kash et al., 2008; de la Mora et al., 2010).”
BackgroundSelf-citation
Surviving threats: neural circuit and computational implications of a new taxonomy of defensive behaviour
LeDoux, J. E., & Daw, N. D. (2018) · Nature reviews. Neuroscience · doi:10.1038/nrn.2018.22 · Cited by 391 · see citing works
Heterosynaptic plasticity underlies aversive olfactory learning in Drosophila
Hige, T., Aso, Y., Modi, M. N., Rubin, G. M., & Turner, G. C. (2015) · Neuron · doi:10.1016/j.neuron.2015.11.003 · Cited by 354 · 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
Synaptic mechanisms underlying persistent cocaine craving
Wolf, M. E. (2016) · Nature reviews. Neuroscience · doi:10.1038/nrn.2016.39 · Cited by 389 · see citing works
What is memory? The present state of the engram
Poo, M.-M., Pignatelli, M., Ryan, T. J., Tonegawa, S., Bonhoeffer, T., Martin, K. C., Rudenko, A., Tsai, L., Tsien, R. W., Fishell, G., et al. (2016) · BMC Biology · doi:10.1186/s12915-016-0261-6 · Cited by 391 · see citing works
“I am not aware of a review article that documents the insect/vertebrate parallels in the dopamine systems but the literature on the amygdala, a vertebrate center for valence learning, is vast [145] and can be compared to the large fly literature devoted to mushroom body learning and memory [146].”
Background
The neural mechanisms and circuitry of the pair bond
Walum, H., & Young, L. J. (2018) · Nature Reviews Neuroscience · doi:10.1038/s41583-018-0072-6 · Cited by 353 · see citing works
Neuroinflammation mechanisms of neuromodulation therapies for anxiety and depression
Guo, B., Zhang, M., Hao, W., Wang, Y., Zhang, T., & Liu, C. (2023) · Translational Psychiatry · doi:10.1038/s41398-022-02297-y · Cited by 389 · see citing works
“As the center of fear, the amygdala changes behaviors (freezing and startle), activate the autonomic nervous system, and transmit information to the hippocampus and bed nucleus of the terminal striatum [34].”
Background
“Liking” and “wanting” in eating and food reward: Brain mechanisms and clinical implications
Morales, I., & Berridge, K. C. (2020) · Physiology & Behavior · doi:10.1016/j.physbeh.2020.113152 · Cited by 346 · 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
“We address the following questions: (1) Is correlated firing between the BLA and PL dynamic upon presentations of cues associated with positive (rewards) or negative (punishments) outcomes?; (2) What is the directionality of information flow?; (3) Can we use neural activity and behavior during Pavlovian discrimination…”
BackgroundSelf-citation
Adult microbiota‐deficient mice have distinct dendritic morphological changes: differential effects in the amygdala and hippocampus
Luczynski, P., Whelan, S. O., O'SULLIVAN, C. T. D., Clarke, G. A., Shanahan, F., Dinan, T. G., & Cryan, J. F. (2016) · European Journal of Neuroscience · doi:10.1111/ejn.13291 · Cited by 345 · see citing works
“…such as sensory thalamus and sensory cortices, the prefrontal cortex, the lateral septum, the supraoptic nucleus, the paraventricular nucleus, the periaqueductal grey and the bed nucleus of the stria terminalis (Herman et al., 2003; Ledoux, 2007; UlrichLai & Herman, 2009; Janak & Tye, 2015).”
Background
Combined Social and Spatial Coding in a Descending Projection from the Prefrontal Cortex
Murugan, M., Jang, H. J., Park, M., Miller, E. M., Cox, J., Taliaferro, J. P., Parker, N. F., Bhave, V., Hur, H., Liang, Y., et al. (2017) · Cell · doi:10.1016/j.cell.2017.11.002 · Cited by 311 · see citing works
The neurobiology of social play and its rewarding value in rats
Vanderschuren, L. J. M. J., Achterberg, E. J. M., & Trezza, V. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.07.025 · Cited by 329 · see citing works
Why fish do not feel pain
Key, B. (2016) · Animal Sentience · doi:10.51291/2377-7478.1011 · Cited by 318 · 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
“Despite the well-appreciated role of the BLA in valence coding (Janak and Tye, 2015), questions regarding the anatomical organization of neurons encoding positive or negative valence remain unanswered.”
Background
Common brain mechanisms of chronic pain and addiction
Elman, I., & Borsook, D. (2016) · Neuron · doi:10.1016/j.neuron.2015.11.027 · Cited by 303 · see citing works
“reinforcement, in conjunction with the associations among arousing, sensory, and emotional stimuli properties (Janak and Tye, 2015).”
Background
Inhibition 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
The basolateral amygdala in reward learning and addiction
Wassum, K. M., & Izquierdo, A. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.08.017 · Cited by 306 · see citing works
“BLA microcircuitry The circuitry of the amygdala has been extensively reviewed elsewhere (see Duvarci and Pare, 2014; Ehrlich et al., 2009; Janak and Tye, 2015).”
BackgroundMethod
Reinforcement learning in artificial and biological systems
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Dual and Opposing Functions of the Central Amygdala in the Modulation of Pain
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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.
ORCID: Janak, Patricia H.
Tye, Kay M.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2015-01-14
Volume: 517
Issue: 7534
Pages: 284-292
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature14188
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 · 2012: 1
FWCI: 13.69
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
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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