A central alarm system that gates multi-sensory innate threat cues to the amygdala
Open accessAbstract
Perception of threats is essential for survival. Previous findings suggest that parallel pathways independently relay innate threat signals from different sensory modalities to multiple brain areas, such as the midbrain and hypothalamus, for immediate avoidance. Yet little is known about whether and how multi-sensory innate threat cues are integrated and conveyed from each sensory modality to the amygdala, a critical brain area for threat perception and learning. Here, we report that neurons expressing calcitonin gene-related peptide (CGRP) in the parvocellular subparafascicular nucleus in the thalamus and external lateral parabrachial nucleus in the brainstem respond to multi-sensory threat cues from various sensory modalities and relay negative valence to the lateral and central amygdala, respectively. Both CGRP populations and their amygdala projections are required for multi-sensory threat perception and aversive memory formation. The identification of unified innate threat pathways may provide insights into developing therapeutic candidates for innate fear-related disorders.
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A recent study in mice identified a population of SPFp neurons expressing CGRP that respond to multi-sensory threat stimuli and project to the lateral amygdala to regulate fear memory.
“A recent study conducted in mice focused on the subparafascicular nucleus (SPFp), which shares neuroanatomical borders with the PIL, and identified a population of SPFp neurons that express calcitonin gene-related peptide (CGRP). This study revealed that CGRP expressing neurons respond to multi-sensory threat stimuli and project to the lateral amygdala to regulate fear memory (26).”
From Social Interaction Elicits Activity in Glutamatergic Neurons in the Posterior Intralaminar Complex of the Thalamus (2024) · cites this paper as [26]
No statistical power estimation analyses were used to predetermine sample sizes; sample sizes were chosen to match previous publications.
“No statistical power estimation analyses were used to predetermine sample sizes, which instead were chosen to match previous publications (2, 11, 26-28).”
From Social Interaction Elicits Activity in Glutamatergic Neurons in the Posterior Intralaminar Complex of the Thalamus (2024) · cites this paper as [26]
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Cites
Detecting strange attractors in turbulence
Takens, F. (1981) · Lecture Notes in Mathematics · doi:10.1007/bfb0091924 · Cited by 10,459 · see citing works
LeDoux, J. E. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.155 · Cited by 8,444 · see citing works
Independent coordinates for strange attractors from mutual information
Fraser, A. M., & Swinney, H. L. (1986) · Physical Review A · doi:10.1103/physreva.33.1134 · Cited by 4,637 · see citing works
Packard, N. H., Crutchfield, J. P., Farmer, J. D., & Shaw, R. S. (1980) · Physical Review Letters · doi:10.1103/physrevlett.45.712 · Cited by 3,909 · see citing works
Detecting Causality in Complex Ecosystems
Sugihara, G., May, R. M., Ye, H., Hsieh, C., Deyle, E. R., Fogarty, M. J., & Munch, S. B. (2012) · Science · doi:10.1126/science.1227079 · Cited by 2,550 · see citing works
Modality-Specific Retrograde Amnesia of Fear
Kim, J. J., & Fanselow, M. S. (1992) · Science · doi:10.1126/science.1585183 · Cited by 2,483 · see citing works
From circuits to behaviour in the amygdala
Janak, P. H., & Tye, K. M. (2015) · Nature · doi:10.1038/nature14188 · Cited by 2,011 · see citing works
Rethinking the Emotional Brain
LeDoux, J. (2012) · Neuron · doi:10.1016/j.neuron.2012.02.004 · Cited by 1,594 · cited 1× · see citing works
“One candidate brain region for the integration of multi-sensory threat information is the amygdala, a well-known limbic structure crucial for initiating behavioral responses to environmental stimuli and forming associative memories (Janak and Tye, 2015; LeDoux, 2000, 2012).”
BackgroundCalcitonin Gene-Related Peptide: Physiology and Pathophysiology
Russell, F. A., King, R., Smillie, S.-J., Kodji, X., & Brain, S. D. (2014) · Physiological Reviews · doi:10.1152/physrev.00034.2013 · Cited by 1,278 · see citing works
Ventromedial hypothalamic neurons control a defensive emotion state
Kunwar, P. S., Zelikowsky, M., Remedios, R., Cai, H., Balban, M. Y., Meister, M., & Anderson, D. J. (2015) · eLife · doi:10.7554/elife.06633 · Cited by 1,112 · see citing works
Thermosensory activation of insular cortex
Craig, A. D., Chen, K., Bandy, D., & Reiman, E. M. (2000) · Nature Neuroscience · doi:10.1038/72131 · Cited by 1,004 · see citing works
Ashina, M. (2020) · New England Journal of Medicine · doi:10.1056/nejmra1915327 · Cited by 830 · see citing works
Innate and conditioned reactions to threat in rats with amygdaloid lesions.
Blanchard, D. C., & Blanchard, R. J. (1972) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0033521 · Cited by 753 · see citing works
Dynamical Systems and Turbulence, Warwick 1980
Rand, D. A. J., & Young, L.-S. (1981) · Lecture notes in mathematics · doi:10.1007/bfb0091903 · Cited by 721 · see citing works
A thalamic nucleus specific for pain and temperature sensation
Craig, A. D., Bushnell, M. C., Zhang, E.-T., & Blomqvist, A. G. (1994) · Nature · doi:10.1038/372770a0 · Cited by 614 · see citing works
Gross, C. T., & Canteras, N. S. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3301 · Cited by 596 · see citing works
Genetic identification of a neural circuit that suppresses appetite
Carter, M. E., Soden, M. E., Zweifel, L. S., & Palmiter, R. D. (2013) · Nature · doi:10.1038/nature12596 · Cited by 587 · see citing works
LeDoux, J. E., Ruggiero, D. A., & Reis, D. J. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902420204 · Cited by 530 · see citing works
Impaired auditory recognition of fear and anger following bilateral amygdala lesions
Scott, S. K., Young, A. W., Calder, A. J., Hellawell, D. J., Aggleton, J. P., & Johnsons, M. (1997) · Nature · doi:10.1038/385254a0 · Cited by 523 · see citing works
A thermosensory pathway that controls body temperature
Nakamura, K., & Morrison, S. F. (2007) · Nature Neuroscience · doi:10.1038/nn2027 · Cited by 503 · see citing works
Rizvi, T. A., Ennis, M., Behbehani, M. M., & Shipley, M. T. (1991) · Journal of Comparative Neurology · doi:10.1002/cne.903030111 · Cited by 500 · see citing works
Matrix metalloproteinase-9 is required for hippocampal late-phase long-term potentiation and memory
Nagy, V., Bozdagi, O., Matynia, A., Balcerzyk, M., Okulski, P., Dzwonek, J., Costa, R. M., Silva, A. J., Kaczmarek, L., & Huntley, G. W. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.4359-05.2006 · Cited by 499 · see citing works
The Human Amygdala and the Induction and Experience of Fear
Feinstein, J. S., Adolphs, R., Damasio, A., & Tranel, D. (2011) · Current Biology · doi:10.1016/j.cub.2010.11.042 · Cited by 497 · see citing works
Han, X., Chow, B. Y., Zhou, H., Klapoetke, N. C., Chuong, A. S., Rajimehr, R., Yang, A., Baratta, M. V., Winkle, J. A., Desimone, R., et al. (2011) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2011.00018 · Cited by 490 · see citing works
The dripping faucet as a model chaotic system
Shaw, R. (1984) · Medical Entomology and Zoology · Cited by 471 · see citing works
The medial hypothalamic defensive system: Hodological organization and functional implications
Canteras, N. S. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(01)00685-2 · Cited by 463 · see citing works
Basolateral to Central Amygdala Neural Circuits for Appetitive Behaviors
Kim, J., Zhang, X., Muralidhar, S., LeBlanc, S., & Tonegawa, S. (2017) · Neuron · doi:10.1016/j.neuron.2017.02.034 · Cited by 460 · see citing works
Elucidating an Affective Pain Circuit that Creates a Threat Memory
Han, S., Soleiman, M. T., Soden, M. E., Zweifel, L. S., & Palmiter, R. D. (2015) · Cell · doi:10.1016/j.cell.2015.05.057 · Cited by 447 · see citing works
Self-citationThe 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
Neuropeptides and neurotrophins in neonatal blood of children with autism or mental retardation
Nelson, K. B., Grether, J. K., Croen, L., Dambrosia, J. M., Dickens, B. F., Jelliffe‐Pawlowski, L. L., Hansen, R. L., & Phillips, T. M. (2001) · Annals of Neurology · doi:10.1002/ana.1024 · Cited by 435 · see citing works
Generalized Theorems for Nonlinear State Space Reconstruction
Deyle, E. R., & Sugihara, G. (2011) · PLoS ONE · doi:10.1371/journal.pone.0018295 · Cited by 401 · see citing works
Calcitonin Gene-Related Peptide (CGRP): A New Target for Migraine
Russo, A. F. (2014) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-010814-124701 · Cited by 396 · see citing works
Oxytocin Selectively Gates Fear Responses Through Distinct Outputs from the Central Amygdala
Viviani, D., Charlet, A., van den Burg, E., Robinet, C., Hurni, N., Abatis, M., Magara, F., & Stoop, R. (2011) · Science · doi:10.1126/science.1201043 · Cited by 381 · see citing works
The amygdala between sensation and affect: a role in pain
Veinante, P., Yalçın, İ., & Barrot, M. (2013) · Journal of Molecular Psychiatry · doi:10.1186/2049-9256-1-9 · Cited by 321 · see citing works
Osakada, F., Mori, T., Cetin, A. H., Marshel, J. H., Virgen, B., & Callaway, E. M. (2011) · Neuron · doi:10.1016/j.neuron.2011.07.005 · Cited by 314 · see citing works
Encoding of danger by parabrachial CGRP neurons
Campos, C., Bowen, A. J., Roman, C. W., & Palmiter, R. D. (2018) · Nature · doi:10.1038/nature25511 · Cited by 307 · see citing works
Independent hypothalamic circuits for social and predator fear
Silva, B. A., Mattucci, C., Krzywkowski, P., Murana, E., Illarionova, A., Grinevich, V., Canteras, N. S., Ragozzino, D., & Gross, C. T. (2013) · Nature Neuroscience · doi:10.1038/nn.3573 · Cited by 261 · see citing works
Towards a neurophysiological signature for fibromyalgia
López‐Solà, M., Woo, C., Pujol, J., Deus, J., Harrison, B. J., Monfort, J., & Wager, T. D. (2016) · Pain · doi:10.1097/j.pain.0000000000000707 · Cited by 255 · see citing works
Parallel ascending spinal pathways for affective touch and pain
Choi, S., Hachisuka, J., Brett, M. A., Magee, A. R., Omori, Y., Iqbal, N.-U.-A., Zhang, D., DeLisle, M. M., Wolfson, R. L., Bai, L., et al. (2020) · Nature · doi:10.1038/s41586-020-2860-1 · Cited by 255 · see citing works
The human amygdala and pain: Evidence from neuroimaging
Simons, L. E., Moulton, E. A., Linnman, C., Carpino, E. A., Becerra, L. R., & Borsook, D. (2012) · Human Brain Mapping · doi:10.1002/hbm.22199 · Cited by 251 · see citing works
Chiang, M. C., Nguyen, E. K., Canto-Bustos, M., Papale, A. E., Oswald, A.-M. M., & Ross, S. E. (2020) · Neuron · doi:10.1016/j.neuron.2020.03.014 · Cited by 248 · see citing works
Central Neural Mechanisms that Interrelate Sensory and Affective Dimensions of Pain
Price, D. D. (2002) · Molecular Interventions · doi:10.1124/mi.2.6.392 · Cited by 244 · see citing works
The coding of valence and identity in the mammalian taste system
Wang, L., Gillis-Smith, S., Peng, Y., Zhang, J., Chen, X., Salzman, C. D., Ryba, N. J. P., & Zuker, C. S. (2018) · Nature · doi:10.1038/s41586-018-0165-4 · Cited by 242 · see citing works
Improved Monosynaptic Neural Circuit Tracing Using Engineered Rabies Virus Glycoproteins
Kim, E. J., Jacobs, M. W., Ito-Cole, T., & Callaway, E. M. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.03.067 · Cited by 237 · see citing works
A VTA GABAergic Neural Circuit Mediates Visually Evoked Innate Defensive Responses
Zhou, Z., Liu, X., Chen, S., Zhang, Z., Liu, Y., Montardy, Q., Tang, Y., Wei, P., Liu, N., Li, L., et al. (2019) · Neuron · doi:10.1016/j.neuron.2019.05.027 · Cited by 211 · see citing works
The neural circuits of innate fear: detection, integration, action, and memorization
Silva, B. A., Gross, C. T., & Gräff, J. (2016) · Learning & Memory · doi:10.1101/lm.042812.116 · Cited by 186 · see citing works
Parabrachial Calcitonin Gene-Related Peptide Neurons Mediate Conditioned Taste Aversion
Carter, M. E., Han, S., & Palmiter, R. D. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.3729-14.2015 · Cited by 180 · see citing works
Self-citationA midline thalamic circuit determines reactions to visual threat
Salay, L. D., Ishiko, N., & Huberman, A. D. (2018) · Nature · doi:10.1038/s41586-018-0078-2 · Cited by 164 · see citing works
Kruger, L., Sternini, C., Brecha, N. C., & Mantyh, P. W. (1988) · The Journal of Comparative Neurology · doi:10.1002/cne.902730203 · Cited by 158 · see citing works
Parabrachial CGRP Neurons Establish and Sustain Aversive Taste Memories
Chen, J., Campos, C., Jarvie, B. C., & Palmiter, R. D. (2018) · Neuron · doi:10.1016/j.neuron.2018.09.032 · Cited by 157 · see citing works
Yasui, Y., Saper, C. B., & Cechetto, D. F. (1991) · The Journal of Comparative Neurology · doi:10.1002/cne.903080212 · Cited by 155 · see citing works
Migraine is Associated With Altered Processing of Sensory Stimuli
Harriott, A. M., & Schwedt, T. J. (2014) · Current Pain and Headache Reports · doi:10.1007/s11916-014-0458-8 · Cited by 133 · see citing works
Rosen, J. B., Asok, A., & Chakraborty, T. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00292 · Cited by 132 · see citing works
Gauriau, C., & Bernard, J. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.3272-03.2004 · Cited by 129 · see citing works
Divergent brainstem opioidergic pathways that coordinate breathing with pain and emotions
Liu, S., Ye, M., Pao, G. M., Song, S. M., Jhang, J., Jiang, H., Kim, J., Kang, S. J., Kim, D., & Han, S. (2021) · Neuron · doi:10.1016/j.neuron.2021.11.029 · Cited by 114 · see citing works
Self-citation2020 IEEE 26th International Conference on Parallel and Distributed Systems
(2020) · IEEE International Conference on Parallel and Distributed Systems (ICPADS) · doi:10.1109/icpads51040.2020.00002 · Cited by 112 · see citing works
Calcitonin gene-related peptide-containing pathways in the rat forebrain
Dobolyi, Á., Irwin, S., Makara, G. B., Usdin, T. B., & Palkovits, M. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20618 · Cited by 111 · see citing works
The lateral parabrachial nucleus is actively involved in the acquisition of fear memory in mice
Satô, M., Ito, M., Nagase, M., Sugimura, Y. K., Takahashi, Y., Watabe, A. M., & Kato, F. (2015) · Molecular Brain · doi:10.1186/s13041-015-0108-z · Cited by 108 · see citing works
Coolen, L. M., Veening, J. G., Wells, A. B., & Shipley, M. T. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10739 · Cited by 99 · see citing works
Corticostriatal control of defense behavior in mice induced by auditory looming cues
Li, Z., Wei, J., Zhang, G., Huang, J. J., Zingg, B., Wang, X., Tao, H. W., & Zhang, L. I. (2021) · Nature Communications · doi:10.1038/s41467-021-21248-7 · Cited by 99 · see citing works
Amygdala lesions in rhesus macaques decrease attention to threat
Monte, O. D., Costa, V. D., Noble, P. L., Murray, E. A., & Averbeck, B. B. (2015) · Nature Communications · doi:10.1038/ncomms10161 · Cited by 93 · see citing works
Lacalle, S. D., & Saper, C. B. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)00245-1 · Cited by 90 · see citing works
Zhang, G., Sun, W., Zingg, B., Shen, L., He, J., Xiong, Y., Tao, H. W., & Zhang, L. I. (2017) · Neuron · doi:10.1016/j.neuron.2017.12.010 · Cited by 90 · see citing works
A photoswitchable GPCR-based opsin for presynaptic inhibition
Copits, B. A., Gowrishankar, R., O’Neill, P., Li, J.-N., Girven, K. S., Yoo, J. J., Meshik, X., Parker, K. E., Spangler, S. M., Elerding, A. J., et al. (2021) · Neuron · doi:10.1016/j.neuron.2021.04.026 · Cited by 86 · see citing works
Self-citationRen, W., & Neugebauer, V. (2010) · Molecular Pain · doi:10.1186/1744-8069-6-93 · Cited by 84 · see citing works
Pharmacologic attenuation of cross-modal sensory augmentation within the chronic pain insula
Harte, S. E., Ichesco, E., Hampson, J. P., Peltier, S., Schmidt‐Wilcke, T., Clauw, D. J., & Harris, R. E. (2016) · Pain · doi:10.1097/j.pain.0000000000000593 · Cited by 83 · see citing works
Demarquay, G., & Mauguı̀ere, F. (2015) · Headache The Journal of Head and Face Pain · doi:10.1111/head.12651 · Cited by 79 · see citing works
Ashina, H., Iljazi, A., Al‐Khazali, H. M., Eigenbrodt, A. K., Larsen, E. L., Andersen, A. M., Hansen, K. J., Bräuner, K. B., Mørch-Jessen, T., Chaudhry, B. A., et al. (2020) · The Journal of Headache and Pain · doi:10.1186/s10194-020-01136-z · Cited by 79 · see citing works
Bowen, A. J., Chen, J., Huang, Y. W., Baertsch, N. A., Park, S., & Palmiter, R. D. (2020) · eLife · doi:10.7554/elife.59799 · Cited by 78 · see citing works
Associative and plastic thalamic signaling to the lateral amygdala controls fear behavior
Barsy, B., Kocsis, K., Magyar, A., Babiczky, Á., Szabó, M., Veres, J. M., Hillier, D., Ulbert, I., Yizhar, O., & Mátyás, F. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-0620-z · Cited by 77 · see citing works
Role of maternal behavior on aggression, fear and anxiety
Ferreira, A., Pereira, M., Agrati, D., Uriarte, N., & Fernández‐Guasti, A. (2002) · Physiology & Behavior · doi:10.1016/s0031-9384(02)00845-4 · Cited by 76 · see citing works
Impaired threat prioritisation after selective bilateral amygdala lesions
Bach, D. R., Hurlemann, R., & Dolan, R. J. (2014) · Cortex · doi:10.1016/j.cortex.2014.08.017 · Cited by 71 · see citing works
Coolen, L. M., Veening, J. G., Petersen, D. W., & Shipley, M. T. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10740 · Cited by 69 · see citing works
Shinohara, K., Watabe, A. M., Nagase, M., Okutsu, Y., Takahashi, Y., Kurihara, H., & Kato, F. (2017) · European Journal of Neuroscience · doi:10.1111/ejn.13662 · Cited by 69 · see citing works
Neuropeptides at the crossroad of fear and hunger: a special focus on neuropeptide Y
Comeras, L. B., Herzog, H., & Tasan, R. O. (2019) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.14179 · Cited by 63 · see citing works
D’Hanis, W., Linke, R., & Yilmazer‐Hanke, D. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21495 · Cited by 58 · see citing works
Yu, L., Hou, J., Fu, F., & Zhang, Y. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.03.009 · Cited by 56 · see citing works
Satb2 neurons in the parabrachial nucleus mediate taste perception
Jarvie, B. C., Chen, J., King, H. O., & Palmiter, R. D. (2021) · Nature Communications · doi:10.1038/s41467-020-20100-8 · Cited by 54 · see citing works
Fu, J., Yu, X.-D., Zhu, Y., Xie, S., Tang, M., Yu, B., & Li, X. (2020) · Neuroscience Bulletin · doi:10.1007/s12264-020-00545-z · Cited by 47 · see citing works
Usunoff, K. G., Itzev, D. E., Rolfs, A., Schmitt, O., & Wree, A. (2006) · Anatomy and Embryology · doi:10.1007/s00429-006-0099-8 · Cited by 45 · see citing works
Yasui, Y., Nakano, K., & Mizuno, N. (1992) · Experimental Brain Research · doi:10.1007/bf00230933 · Cited by 44 · see citing works
jGCaMP8 Fast Genetically Encoded Calcium Indicators
Zhang, Y., Rózsa, M., Bushey, D., Zheng, J., Reep, D., Liang, Y., Broussard, G. J., Tsang, A., Tsegaye, G., Patel, R., et al. (2020) · Figshare · doi:10.25378/janelia.13148243 · Cited by 40 · see citing works
Kocorowski, L. H., & Helmstetter, F. J. (2001) · Neurobiology of Learning and Memory · doi:10.1006/nlme.2000.3963 · Cited by 34 · see citing works
Medial Amygdala Arginine Vasopressin Neurons Regulate Innate Aversion to Cat Odors in Male Mice
Tong, W. H., Abdulai-Saiku, S., & Vyas, A. (2020) · Neuroendocrinology · doi:10.1159/000508862 · Cited by 25 · see citing works
Olfactory and visceral projections to the nucleus of the solitary tract
García-Díaz, D. E., Jimenez-Montufar, L. L., Guevara-Aguilar, R., Wayner, M. J., & Armstrong, D. L. (1988) · Physiology & Behavior · doi:10.1016/0031-9384(88)90327-7 · Cited by 24 · see citing works
Wei, P., Liu, N., Zhang, Z., Liu, X., Tang, Y., He, X., Wu, B., Zhou, Z., Liu, Y., Li, J., et al. (2015) · Nature Communications · doi:10.1038/ncomms9228 · Cited by 20 · see citing works
Massively Parallel Causal Inference of Whole Brain Dynamics at Single Neuron Resolution
Watanakeesuntorn, W., Takahashi, K., Ichikawa, K., Park, J. C., Sugihara, G., Takano, R., Haga, J., & Pao, G. M. (2020) · IEEE International Conference on Parallel and Distributed Systems (ICPADS) · doi:10.1109/icpads51040.2020.00035 · Cited by 20 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Molecular and anatomical characterization of parabrachial neurons and their axonal projections
Pauli, J. L., Chen, J., Basiri, M. L., Park, S., Carter, M. E., Sanz, E., McKnight, G. S., Stuber, G. D., & Palmiter, R. D. (2022) · eLife · doi:10.7554/elife.81868 · Cited by 162 · see citing works
Torres-Rodriguez, J. M., Wilson, T. D., Singh, S., Torruella-Suárez, M. L., Chaudhry, S., Adke, A. P., Becker, J. J., Neugebauer, B., Lin, J. J., González, S. M., et al. (2023) · Neuropsychopharmacology · doi:10.1038/s41386-023-01673-6 · Cited by 71 · see citing works
Cells and circuits for amygdala neuroplasticity in the transition to chronic pain
Kiritoshi, T., Yakhnitsa, V., Singh, S., Wilson, T. D., Chaudhry, S., Neugebauer, B., Torres-Rodriguez, J. M., Lin, J. J., Carrasquillo, Y., & Neugebauer, V. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114669 · Cited by 54 · see citing works
Multisensory integration in the mammalian brain: diversity and flexibility in health and disease
Choi, I., Demir, I., Oh, S., & Lee, S. (2023) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2022.0338 · Cited by 40 · see citing works
Wang, H., Wang, Q., Cui, L., Feng, X., Dong, P., Tan, L., Lin, L., Lian, H., Cao, S.-X., Huang, H., et al. (2024) · Nature Neuroscience · doi:10.1038/s41593-023-01562-7 · Cited by 42 · see citing works
Understanding the neural code of stress to control anhedonia
Xia, F., Fascianelli, V., Vishwakarma, N., Ghinger, F. G., Kwon, A., Gergues, M. M., Lalani, L. K., Fusi, S., & Kheirbek, M. A. (2024) · Nature · doi:10.1038/s41586-024-08241-y · Cited by 38 · see citing works
Parabrachial Calca neurons drive nociplasticity
Condon, L. F., Yu, Y., Park, S., Cao, F., Pauli, J. L., Nelson, T. S., & Palmiter, R. D. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114057 · Cited by 38 · see citing works
Kim, D.-I., Park, S., Park, S., Ye, M., Chen, J., Kang, S. J., Jhang, J., Hunker, A. C., Zweifel, L. S., Caron, K. M., et al. (2024) · Cell · doi:10.1016/j.cell.2024.06.035 · Cited by 34 · see citing works
Self-citationSubcortico-amygdala pathway processes innate and learned threats
Khalil, V., Faress, I., Mermet-Joret, N., Kerwin, P., Yonehara, K., & Nabavi, S. (2023) · eLife · doi:10.7554/elife.85459 · Cited by 27 · see citing works
Peptidergic and functional delineation of the Edinger-Westphal nucleus
Priest, M. F., Freda, S. N., Rieth, I. J., Badong, D., Dumrongprechachan, V., & Kozorovitskiy, Y. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112992 · Cited by 36 · see citing works
Parabrachial Nucleus Activity in Nociception and Pain in Awake Mice
Smith, J. A., Ji, Y., Lorsung, R. M., Breault, M. S., Koenig, J. A., Cramer, N., Masri, R. M., & Keller, A. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.0587-23.2023 · Cited by 27 · see citing works
Parabrachial neurons promote nociplastic pain
Palmiter, R. D. (2024) · Trends in Neurosciences · doi:10.1016/j.tins.2024.07.002 · Cited by 29 · see citing works
Arthurs, J., Pauli, J. L., & Palmiter, R. D. (2023) · Neuroscience · doi:10.1016/j.neuroscience.2023.03.003 · Cited by 23 · see citing works
Leithead, A. B., Godino, A., Barbier, M., & Harony-Nicolas, H. (2024) · Biological Psychiatry · doi:10.1016/j.biopsych.2023.05.016 · Cited by 21 · see citing works
Cruz, B., Vozella, V., Borgonetti, V., Bullard, R., Bianchi, P., Kirson, D., Bertotto, L. B., Bajo, M., Vlkolinský, R., Messing, R. O., et al. (2024) · Molecular Psychiatry · doi:10.1038/s41380-024-02514-8 · Cited by 22 · see citing works
Pain persists in mice lacking both Substance P and CGRPα signalingPreprint
MacDonald, D. I., Jayabalan, M., Seaman, J. T., Balaji, R., Nickolls, A. R., & Chesler, A. T. (2024) · eLife · doi:10.7554/elife.93754 · Cited by 18 · see citing works
Tringali, G., Lavanco, G., Castelli, V., Pizzolanti, G., Kuchař, M., Currò, D., Cannizzaro, C., & Brancato, A. (2023) · Phytotherapy Research · doi:10.1002/ptr.7972 · Cited by 17 · see citing works
Population coding of predator imminence in the hypothalamus
Cheung, K. Y. M., Nair, A., Li, L.-Y., Shapiro, M. G., & Anderson, D. J. (2025) · Neuron · doi:10.1016/j.neuron.2025.02.003 · Cited by 16 · see citing works
Kang, S. J., Kim, J., Kim, D., Roberts, B. Z., & Han, S. (2024) · Nature Neuroscience · doi:10.1038/s41593-023-01504-3 · Cited by 14 · see citing works
Self-citationParabrachial Calca neurons mediate second-order conditioning
Park, S., Zhu, A., Cao, F., & Palmiter, R. D. (2024) · Nature Communications · doi:10.1038/s41467-024-53977-w · Cited by 13 · see citing works
Sex Differences in Central Amygdala Glutamate Responses to Calcitonin Gene-Related Peptide
Lorsung, R. M., Cramer, N., Alipio, J. B., Ji, Y., Han, S., Masri, R. M., & Keller, A. (2024) · Journal of Neuroscience · doi:10.1523/jneurosci.1898-24.2024 · Cited by 13 · see citing works
Self-citationA circuit that integrates drive state and social contact to gate mating
Salay, L. D., Tsao, D. Y., & Anderson, D. J. (2025) · Nature · doi:10.1038/s41586-025-09327-x · Cited by 14 · see citing works
Sangalli, L., Eli, B., Mehrotra, S., Sabagh, S., & Fricton, J. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241512200 · Cited by 12 · see citing works
The lateral thalamus: a bridge between multisensory processing and naturalistic behaviors
Yang, M., Keller, D. W., Dobolyi, Á., & Valtcheva, S. (2024) · Trends in Neurosciences · doi:10.1016/j.tins.2024.11.005 · Cited by 12 · see citing works
Penzo, M. A., & Moscarello, J. M. (2023) · Trends in Neurosciences · doi:10.1016/j.tins.2023.06.006 · Cited by 8 · see citing works
Bucsea, O., Rupawala, M., Shiff, I., Wang, X., Meek, J. H., Fitzgerald, M., Lorenzo Fabrizi, D., Riddell, R. P., & Jones, L. (2022) · Pain · doi:10.1097/j.pain.0000000000002798 · Cited by 11 · see citing works
Laricchiuta, D., Gimenez, J., Sciamanna, G., Termine, A., Fabrizio, C., Valle, F. D., Caioli, S., Saba, L., Bardi, M. D., Balsamo, F., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.113066 · Cited by 10 · see citing works
Non-Hebbian plasticity transforms transient experiences into lasting memories
Faress, I. M. G., Khalil, V., Hou, W., Moreno, A., Andersen, N., Fonseca, R., Piriz, J., Capogna, M., & Nabavi, S. (2023) · eLife · doi:10.7554/elife.91421 · Cited by 9 · see citing works
Parabrachial CGRP neurons modulate active defensive behavior under a naturalistic threat
Pyeon, G. H., Cho, H., Chung, B. M., Choi, J.-S., & Jo, Y. S. (2025) · eLife · doi:10.7554/elife.101523 · Cited by 8 · see citing works
A top-down insular cortex circuit crucial for non-nociceptive fear learning
Han, J., Suh, B., & Han, J. (2025) · Science Advances · doi:10.1126/sciadv.adt6996 · Cited by 8 · see citing works
Amygdalostriatal transition zone neurons encode sustained cue responses to guide defensive behaviors
Mills, F., Lee, C. R., Howe, J. R., Li, H., Keisler, M. N., Shao, S., Taschbach, F., Lemieux, M., Aloboudi, F., White, J., et al. (2026) · Neuron · doi:10.1016/j.neuron.2026.08.012 · Cited by 10 · see citing works
Self-citationThalamic CGRP neurons define a spinothalamic pathway for affective pain
Kang, S. J., Liu, S., Kim, J., Kim, D., Oh, T. G., Peng, J., Ye, M., Lee, K., Evans, R. M., Goulding, M., et al. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2505889122 · Cited by 7 · see citing works
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Korkutata, M., Luca, R. D., Fitzgerald, B., Khanday, M. A., Arrigoni, E., & Scammell, T. E. (2025) · The Journal of Comparative Neurology · doi:10.1002/cne.70018 · Cited by 7 · see citing works
Parabrachial nucleus neuron circuits that control feeding behavior and energy balance
Zhao, Z., Chen, Y., Xuan, Y., Zhou, G., & Qiu, W. (2023) · Obesity Medicine · doi:10.1016/j.obmed.2023.100509 · Cited by 7 · see citing works
Kim, D., Kang, S. J., Jhang, J., Jo, Y. S., Park, S., Ye, M., Pyeon, G. H., Im, G.-H., Kim, S., & Han, S. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.11.09.622790 · Cited by 7 · see citing works
Self-citationVila‐Pueyo, M., Goadsby, P. J., Johnson, K. W., & Holland, P. R. (2025) · Headache The Journal of Head and Face Pain · doi:10.1111/head.15006 · Cited by 6 · see citing works
A subpopulation of projections from the parabrachial nucleus to the central amygdala mediates itch
Pavlenko, D., Ishida, H., Markan, A., & Akiyama, T. (2025) · Scientific Reports · doi:10.1038/s41598-025-08612-z · Cited by 6 · see citing works
Gustatory thalamic neurons mediate aversive behaviors
Cao, F., Park, S., Pauli, J. L., Seo, E. Y., Nguyen, A.-D., & Palmiter, R. D. (2025) · Nature Communications · doi:10.1038/s41467-025-63464-5 · Cited by 7 · see citing works
Auditory guidance of eye movements toward threat-related images in the absence of visual awareness
Hu, J., Badde, S., & Vetter, P. (2024) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2024.1441915 · Cited by 5 · see citing works
Neuromodulatory signaling contributing to the encoding of aversion
Wu, C.-H., Camelot, L., Lecca, S., & Mameli, M. (2025) · Trends in Neurosciences · doi:10.1016/j.tins.2025.04.003 · Cited by 5 · see citing works
Morningstar, M. D., Lopez, K. M., Mayfield, S. S., Almeida‐Mancero, R. N., Marquez, J., Flores, A. M., Hafer, B. R., Estrada, E., Holtzman, G. A., Goranson, E. V., et al. (2024) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.15503 · Cited by 5 · see citing works
Pistolesi, A., Tuniz, S., Luceri, C., Molli, A., Urru, M., Rocca, A. I. L., Tanturli, M., Cesaris, F. D., Buonvicino, D., & Chiarugi, A. (2025) · Pharmacological Research · doi:10.1016/j.phrs.2025.107818 · Cited by 5 · see citing works
Pain persists in mice lacking both Substance P and CGRPα signaling
MacDonald, D. I., Jayabalan, M., Seaman, J. T., Balaji, R., Nickolls, A. R., & Chesler, A. T. (2025) · eLife · doi:10.1101/2023.11.15.567208 · Cited by 5 · see citing works
Kim, D.-I., Park, S., Ye, M., Chen, J., Jhang, J., Hunker, A. C., Zweifel, L. S., Palmiter, R. D., & Han, S. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.01.19.524797 · Cited by 5 · see citing works
Self-citationSerotonin circuits act cooperatively with pathophysiology of opioid use disorder
Arakawa, H., & Akihiko, O. (2024) · Addiction Neuroscience · doi:10.1016/j.addicn.2024.100187 · Cited by 4 · see citing works
The parabrachial to central amygdala circuit is a key mediator of injury-induced pain sensitizationPreprint
Torres-Rodriguez, J. M., Wilson, T. D., Singh, S., Chaudhry, S., Adke, A. P., Becker, J. J., Lin, J. J., González, S. M., Soler‐Cedeño, O., & Carrasquillo, Y. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.02.08.527340 · Cited by 4 · see citing works
Neural signatures of stress susceptibility and resilience in the amygdala-hippocampal networkPreprint
Xia, F., Fascianelli, V., Vishwakarma, N., Ghinger, F. G., Fusi, S., & Kheirbek, M. A. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.10.23.563652 · Cited by 4 · see citing works
Tezanos, P., & Trejo, J. L. (2025) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2025.106145 · Cited by 3 · see citing works
Parabrachial Calca Neurons Influence Aversive and Appetitive Taste Function
Lemon, C. H., Li, J., Ali, M. S. S., Ngum, N., Zumpano, K. T., & Roberts, C. J. (2025) · eNeuro · doi:10.1523/eneuro.0191-25.2025 · Cited by 3 · see citing works
Non-Hebbian plasticity transforms transient experiences into lasting memories
Faress, I. M. G., Khalil, V., Hou, W., Moreno, A., Andersen, N., Fonseca, R., Piriz, J., Capogna, M., & Nabavi, S. (2024) · eLife · doi:10.7554/elife.91421.3 · Cited by 3 · see citing works
The parasubthalamic nucleus: A novel eating center in the brain
Lu, M., Zhang, J., Zhang, Q., Sun, J., Zou, D., Huang, J., & Liu, W. (2025) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2025.111250 · Cited by 3 · see citing works
Spinal VGLUT3 lineage neurons drive visceral mechanical allodynia but not visceromotor reflexesPreprint
Qi, L., Lin, S.-H., & Ma, Q. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.09.07.507044 · Cited by 3 · see citing works
Leithead, A. B., Godino, A., Barbier, M., & Harony‐Nicolas, H. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.04.24.538114 · Cited by 3 · see citing works
The nociceptive inputs of the paraventricular hypothalamic nucleus in formalin stimulated mice
Ren, S., Wang, S., Lv, S., Gao, J., Mao, Y., Liu, Y., Xie, Q., Zhang, T., Zhao, L., & Shi, J. (2024) · Neuroscience Letters · doi:10.1016/j.neulet.2024.137948 · Cited by 2 · see citing works
Rodriguez-Rozada, S., & Tovote, P. (2025) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2025.103105 · Cited by 2 · see citing works
Ingestion-activated CGRP neurons control learning but not satiety
Jarvie, B. C., Ravi, A., Nanavati, R., Namkung, H., Qiu, L., Ly, T., Oh, J. Y., Barnhill, O., & Knight, Z. A. (2026) · Neuron · doi:10.1016/j.neuron.2026.08.001 · Cited by 2 · see citing works
Differential neural decoding of alarm and avoidance information from vocal alarm calls in humans
Beinnes, G. K., Skjegstad, C. L., & Frühholz, S. (2025) · Communications Biology · doi:10.1038/s42003-025-08248-9 · Cited by 2 · see citing works
Non-Hebbian plasticity transforms transient experiences into lasting memoriesPreprint
Faress, I. M. G., Khalil, V., Hou, W., Moreno, A., Andersen, N., Fonseca, R., Piriz, J., Capogna, M., & Nabavi, S. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.04.06.535862 · Cited by 2 · see citing works
Pain persists in mice lacking both Substance P and CGRPα signalingPreprint
MacDonald, D. I., Jayabalan, M., Seaman, J. T., Nickolls, A. R., & Chesler, A. T. (2024) · eLife · doi:10.7554/elife.93754.1 · Cited by 2 · see citing works
Advances in neural circuits of innate fear defense behavior
Zhao, J., Qi, S. O. N. G., Wu, Y., & Liping, Y. A. N. G. (2023) · Journal of Zhejiang University (Medical Sciences) · doi:10.3724/zdxbyxb-2023-0131 · Cited by 1 · see citing works
Tohyama, S., Nagashima, T., Higashino, I., Arima‐Yoshida, F., Hiyoshi, K., Nagase, M., Yada, Y., Naoki, H., & Watabe, A. M. (2025) · Communications Biology · doi:10.1038/s42003-025-08367-3 · Cited by 1 · see citing works
Breivik, T. J., Gjermo, P. E., Opstad, P. K., Murison, R. C. C., von Hörsten, S., & Fristad, I. (2025) · Life · doi:10.3390/life15101572 · Cited by 1 · see citing works
Osnaya-Ramírez, R. I., Wang, H., Zhang, S., Maximo, J. T., Hahn, S., Liu, B., Brodnik, Z. D., Ye, R., & Morales, M. (2025) · Biological Psychiatry · doi:10.1016/j.biopsych.2025.11.014 · Cited by 1 · see citing works
Pauli, J. L., Park, S., Felix, R. R., & Palmiter, R. D. (2026) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2605466123 · Cited by 1 · see citing works
Comparative neuroanatomy of emotion expression: from flies to humans
Adolphs, R. (2026) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2025.0135 · Cited by 1 · see citing works
Parabrachial Calca neurons mediate second-order conditioningPreprint
Park, S., Zhu, A., Cao, F., & Palmiter, R. D. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.03.21.586150 · Cited by 1 · see citing works
Wang, G., Ma, L., Wang, L., & Pang, W. (2024) · Brain Sciences · doi:10.3390/brainsci14040368
Non-Hebbian plasticity transforms transient experiences into lasting memoriesPreprint
Faress, I. M. G., Khalil, V., Hou, W., Moreno, A., Andersen, N., Fonseca, R., Piriz, J., Capogna, M., & Nabavi, S. (2024) · eLife · doi:10.7554/elife.91421.2
Pain persists in mice lacking both Substance P and CGRPα signalingPreprint
MacDonald, D. I., Jayabalan, M., Seaman, J. T., Balaji, R., Nickolls, A. R., & Chesler, A. T. (2025) · eLife · doi:10.7554/elife.93754.2
How Salient Sensory Stimuli Induce Brain-Wide State Alterations
Li, M., Tan, K., Liu, T., & (苑克鑫), K. Y. (2026) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-112723-034728
Giacometti, C. (2023) · theses.fr (ABES) · doi:10.70675/a9788477z9d8ez4b11zb5b1zf5f523ba492c
Nagashima, T., Higashino, I., Arima‐Yoshida, F., Hiyoshi, K., Nagase, M., Yada, Y., Naoki, H., & Watabe, A. M. (2026) · BIO-PROTOCOL · doi:10.21769/bioprotoc.5714
Therapeutic Potential of Group 2 Innate Lymphoid Cells in Neuroinflammatory Diseases
Ye, Q., Yu, Q., & Ping, A. (2026) · Scandinavian Journal of Immunology · doi:10.1111/sji.70131
Judd, E. N., Pauli, J. L., Kenmochi, S. J., Bruchas, M. R., & Palmiter, R. D. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.08.06.743398
Self-citationPark, S., Clarke, H. H., Cao, F., Rose, A., Yang, E., Felix, R. R., Read, J., Chen, J., Pauli, J. L., & Palmiter, R. D. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.08.07.743567
Learning a threat converges on the circuit processing innate threatPreprint
Mermet-Joret, N., Nazari, M., Pommer, A. T., Ansarifar, S., Luz, J. S., Vestergaard, A.-K., & Nabavi, S. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.08.26.747219
Soft tactile stimulation engages CGRP neurons in the parabrachial nucleus
Anesten, F., Simfors, S., Ioneskou, K., Hezso, M., Gündogdu, B., Tran, A., Stjernvall, A., Ratiglia, V., Almasri, A., & Löken, L. S. (2026) · Neuroscience · doi:10.1016/j.neuroscience.2026.09.039
- Authors
- Kang, S. J., Liu, S., Ye, M., Kim, D.-I., Pao, G. M., Copits, B. A., Roberts, B. Z., Lee, K.-F., Bruchas, M. R., & Han, S.
- Affiliations
- Salk Institute for Biological Studies (US)
- Washington University in St. Louis (US)
- University of California San Diego (US)
- University of Washington (US)
- Corresponding author
- Han, Sung
- ORCID
- Venue
- Cell Reports
- Publisher
- Elsevier BV
- Published
- 2022-08
- Volume
- 40
- Issue
- 7
- Pages
- 111222
- ISSN
- 2211-1247 (ISSN-L)
- PMC
- PMC9420642
- OpenAlex
- W4292184182
- Cited by
- 77
- References
- 87
- Citations by year
- 2026: 11 · 2025: 21 · 2024: 22 · 2023: 20 · 2022: 3
- FWCI
- 8.51
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Cell Reports (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion, cc-by-nc-nd)
- Digital Commons@Becker (Washington University School of Medicine) (submittedVersion, cc-by-nc-nd)
- eScholarship (California Digital Library) (submittedVersion, cc-by-nc-nd)
- Funders
- National Institute of Mental Health (1R01MH111520, 1R01MH116203, R01MH112355)
- Mary K. Chapman Foundation
- Simons Foundation Autism Research Initiative (388708)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Multisensory perception and integration
- Keywords
- amygdala, calcitonin gene-related peptide, parabrachial nucleus, thalamus, lateral amygdala, central amygdala, aversive memory, threat avoidance, sensory integration
- MeSH terms
- Cues, Thalamus, Calcitonin Gene-Related Peptide, Parabrachial Nucleus, Central Amygdaloid Nucleus
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