Dorsal tegmental dopamine neurons gate associative learning of fear
Open accessAbstract
Functional neuroanatomy of Pavlovian fear has identified neuronal circuits and synapses associating conditioned stimuli with aversive events. Hebbian plasticity within these networks requires additional reinforcement to store particularly salient experiences into long-term memory. Here we have identified a circuit that reciprocally connects the ventral periaqueductal gray and dorsal raphe region with the central amygdala and that gates fear learning. We found that ventral periaqueductal gray and dorsal raphe dopaminergic (vPdRD) neurons encode a positive prediction error in response to unpredicted shocks and may reshape intra-amygdala connectivity via a dopamine-dependent form of long-term potentiation. Negative feedback from the central amygdala to vPdRD neurons might limit reinforcement to events that have not been predicted. These findings add a new module to the midbrain dopaminergic circuit architecture underlying associative reinforcement learning and identify vPdRD neurons as a critical component of Pavlovian fear conditioning. We propose that dysregulation of vPdRD neuronal activity may contribute to fear-related psychiatric disorders.
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Optogenetic or chemogenetic inhibition of DRN dopamine neurons during fear conditioning suppressed freezing in response to a footshock-predictive cue.
“It was also recently reported that optogenetic or chemogenetic inhibition of DRN dopamine neurons during fear conditioning suppressed freezing in response to a footshock-predictive cue, suggesting an additional role in aversive responding115.”
From Neural mechanisms of social homeostasis (2019) · cites this paper as [115]
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STAR: ultrafast universal RNA-seq aligner
Dobin, A., Davis, C. A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M., & Gingeras, T. R. (2013) · Bioinformatics · doi:10.1093/bioinformatics/bts635 · Cited by 51,709 · see citing works
HTSeq—a Python framework to work with high-throughput sequencing data
Anders, S., Pyl, P. T., & Huber, W. (2015) · Bioinformatics · doi:10.1093/bioinformatics/btu638 · Cited by 21,464 · see citing works
Kim, D., Pertea, G., Trapnell, C., Pimentel, H., Kelley, R., & Salzberg, S. L. (2013) · Genome Biology · doi:10.1186/gb-2013-14-4-r36 · Cited by 12,668 · see citing works
Pearce, J. M., & Hall, G. (1980) · Psychological Review · doi:10.1037/0033-295x.87.6.532 · Cited by 3,023 · see citing works
Dopamine in motivational control: rewarding, aversive, and alerting
Bromberg-Martin, E. S., Matsumoto, M., & Hikosaka, O. (2010) · Neuron · doi:10.1016/j.neuron.2010.11.022 · Cited by 2,396 · see citing works
Swanson, L. W. (1982) · Brain Research Bulletin · doi:10.1016/0361-9230(82)90145-9 · Cited by 1,718 · see citing works
Phasic vs Sustained Fear in Rats and Humans: Role of the Extended Amygdala in Fear vs Anxiety
Davis, M., Walker, D. L., Miles, L., & Grillon, C. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.109 · Cited by 1,488 · see citing works
Neuron-type-specific signals for reward and punishment in the ventral tegmental area
Cohen, J. Y., Haesler, S., Vong, L., Lowell, B. B., & Uchida, N. (2012) · Nature · doi:10.1038/nature10754 · Cited by 1,318 · see citing works
LeDoux, J. (2007) · Current Biology · doi:10.1016/j.cub.2007.08.005 · Cited by 1,281 · see citing works
Phasic Firing in Dopaminergic Neurons Is Sufficient for Behavioral Conditioning
Tsai, H.-C., Zhang, F., Adamantidis, A., Stuber, G. D., Bonci, A., de Lecea, L., & Deisseroth, K. (2009) · Science · doi:10.1126/science.1168878 · Cited by 1,266 · see citing works
Neuronal Reward and Decision Signals: From Theories to Data
Schultz, W. (2015) · Physiological Reviews · doi:10.1152/physrev.00023.2014 · Cited by 1,126 · see citing works
Schultz, W. (2007) · Trends in Neurosciences · doi:10.1016/j.tins.2007.03.007 · Cited by 1,028 · see citing works
Encoding of conditioned fear in central amygdala inhibitory circuits
Ciocchi, S., Herry, C., Grenier, F., Wolff, S. B. E., Letzkus, J. J., Vlachos, I., Ehrlich, I., Sprengel, R., Deisseroth, K., Stadler, M. B., et al. (2010) · Nature · doi:10.1038/nature09559 · Cited by 924 · see citing works
Functional characteristics of the midbrain periaqueductal gray.
Behbehani, M. M. (1995) · Progress in Neurobiology · doi:10.1016/0301-0082(95)00009-k · Cited by 879 · see citing works
Genetic dissection of an amygdala microcircuit that gates conditioned fear
Haubensak, W., Kunwar, P. S., Cai, H., Ciocchi, S., Wall, N. R., Ponnusamy, R., Biag, J., Dong, H.-W., Deisseroth, K., Callaway, E. M., et al. (2010) · Nature · doi:10.1038/nature09553 · Cited by 840 · see citing works
Self-citationPhasic excitation of dopamine neurons in ventral VTA by noxious stimuli
Brischoux, F., Chakraborty, S., Brierley, D. I., & Ungless, M. A. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0811507106 · Cited by 801 · see citing works
Uniform Inhibition of Dopamine Neurons in the Ventral Tegmental Area by Aversive Stimuli
Ungless, M. A., Magill, P. J., & Bolam, J. P. (2004) · Science · doi:10.1126/science.1093360 · Cited by 782 · see citing works
Midbrain circuits for defensive behaviour
Tovote, P., Esposito, M. S., Botta, P., Chaudun, F., Fadok, J. P., Marković, M., Wolff, S. B. E., Ramakrishnan, C., Fenno, L. E., Deisseroth, K. A., et al. (2016) · Nature · doi:10.1038/nature17996 · Cited by 739 · see citing works
An Optimized microRNA Backbone for Effective Single-Copy RNAi
Fellmann, C., Hoffmann, T., Sridhar, V., Hopfgartner, B., Muhar, M., Roth, M., Lai, D. Y., Barbosa, I. A. M., Kwon, J. S., Guan, Y., et al. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.11.020 · Cited by 705 · see citing works
Self-citationGABA Neurons of the VTA Drive Conditioned Place Aversion
Tan, K. R., Yvon, C., Turiault, M., Mirzabekov, J. J., Doehner, J., Labouèbe, G., Deisseroth, K. A., Tye, K. M., & Lüscher, C. (2012) · Neuron · doi:10.1016/j.neuron.2012.02.015 · Cited by 635 · see citing works
Neural systems involved in fear and anxiety measured with fear-potentiated startle.
Davis, M. (2006) · American Psychologist · doi:10.1037/0003-066x.61.8.741 · Cited by 589 · see citing works
Experience-dependent modification of a central amygdala fear circuit
Li, H., Penzo, M. A., Taniguchi, H., Kopec, C. D., Huang, Z. J., & Li, B. (2013) · Nature Neuroscience · doi:10.1038/nn.3322 · Cited by 497 · 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
Identification of Wake-Active Dopaminergic Neurons in the Ventral Periaqueductal Gray Matter
Lu, J., Jhou, T. C., & Saper, C. B. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.2244-05.2006 · Cited by 458 · 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
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
Neural substrates for expectation-modulated fear learning in the amygdala and periaqueductal gray
Johansen, J. P., Tarpley, J. W., LeDoux, J. E., & Blair, H. T. (2010) · Nature Neuroscience · doi:10.1038/nn.2594 · Cited by 312 · see citing works
Placing prediction into the fear circuit
McNally, G. P., Johansen, J. P., & Blair, H. T. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.03.005 · Cited by 298 · see citing works
de la Mora, M. P., Gallegos-Cari, A., Arizmendi-García, Y., Marcellino, D., & Fuxe, K. (2010) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2009.10.010 · Cited by 296 · see citing works
Hart, A. S., Rutledge, R. B., Glimcher, P. W., & Phillips, P. E. M. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.2489-13.2014 · Cited by 294 · see citing works
Dorsal Raphe Dopamine Neurons Modulate Arousal and Promote Wakefulness by Salient Stimuli
Cho, J. R., Treweek, J. B., Robinson, J. E., Xiao, C., Bremner, L. R., Greenbaum, A., & Gradinaru, V. (2017) · Neuron · doi:10.1016/j.neuron.2017.05.020 · Cited by 276 · see citing works
Mechanisms and functions of GABA co-release
Tritsch, N. X., Granger, A. J., & Sabatini, B. L. (2016) · Nature reviews. Neuroscience · doi:10.1038/nrn.2015.21 · Cited by 261 · see citing works
Representation of aversive prediction errors in the human periaqueductal gray
Roy, M., Shohamy, D., Daw, N., Jepma, M., Wimmer, G. E., & Wager, T. D. (2014) · Nature Neuroscience · doi:10.1038/nn.3832 · Cited by 246 · see citing works
Conditional modulation of spike-timing-dependent plasticity for olfactory learning
Cassenaer, S., & Laurent, G. (2012) · Nature · doi:10.1038/nature10776 · Cited by 215 · see citing works
Dopamine is necessary for cue-dependent fear conditioning
Fadok, J. P., Dickerson, T. M. K., & Palmiter, R. D. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.1616-09.2009 · Cited by 213 · see citing works
A neural switch for active and passive fear
Gozzi, A., Jain, A., Giovanelli, A., Bertollini, C., Crestan, V., Schwarz, A. J., Tsetsenis, T., Ragozzino, D., Gross, C. T., & Bifone, A. (2010) · Neuron · doi:10.1016/j.neuron.2010.07.008 · Cited by 209 · see citing works
McDevitt, R. A., Tiran-Cappello, A., Shen, H., Balderas, I., Britt, J. P., Marino, R. A. M., Chung, S. L., Richie, C. T., Harvey, B. K., & Bonci, A. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.08.037 · Cited by 203 · see citing works
Two Dimensions of Value: Dopamine Neurons Represent Reward But Not Aversiveness
Fiorillo, C. D. (2013) · Science · doi:10.1126/science.1238699 · Cited by 203 · see citing works
The Neuroscience of Learning: Beyond the Hebbian Synapse
Gallistel, C. R., & Matzel, L. D. (2012) · Annual Review of Psychology · doi:10.1146/annurev-psych-113011-143807 · Cited by 197 · see citing works
The role of dopamine in intracranial self-stimulation of the ventral tegmental area
Fibiger, H., LePiane, F., Jakubovic, A., & Phillips, A. (1987) · The Journal of Neuroscience · doi:10.1523/jneurosci.07-12-03888.1987 · Cited by 189 · see citing works
The central amygdala controls learning in the lateral amygdala
Yu, K., Ahrens, S., Zhang, X., Schiff, H. C., Ramakrishnan, C., Fenno, L. E., Deisseroth, K. A., Zhao, F., Luo, M., Gong, L., et al. (2017) · Nature Neuroscience · doi:10.1038/s41593-017-0009-9 · Cited by 176 · see citing works
Venniro, M., Caprioli, D., Zhang, M., Whitaker, L. R., Zhang, S., Warren, B. L., Cifani, C., Marchant, N. J., Yizhar, O., Bossert, J. M., et al. (2017) · Neuron · doi:10.1016/j.neuron.2017.09.024 · Cited by 162 · see citing works
Central Amygdala Somatostatin Neurons Gate Passive and Active Defensive Behaviors
Yu, K., da Silva, P. G., Albeanu, D. F., & Li, B. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.4419-15.2016 · Cited by 157 · see citing works
Direct Midbrain Dopamine Input to the Suprachiasmatic Nucleus Accelerates Circadian Entrainment
Grippo, R. M., Purohit, A. M., Zhang, Q., Zweifel, L. S., & Güler, A. D. (2017) · Current Biology · doi:10.1016/j.cub.2017.06.084 · Cited by 140 · see citing works
Correia, P. A., Lottem, E., Banerjee, D., Machado, A. S., Carey, M. R., & Mainen, Z. F. (2017) · eLife · doi:10.7554/elife.20975 · Cited by 138 · see citing works
A feedback neural circuit for calibrating aversive memory strength
Ozawa, T., Ycu, E. A., Kumar, A., Yeh, L.-F., Ahmed, T., Koivumaa, J., & Johansen, J. P. (2016) · Nature Neuroscience · doi:10.1038/nn.4439 · Cited by 123 · see citing works
De Bundel, D., Zussy, C., Espallergues, J., Gerfen, C. R., Girault, J.-A., & Valjent, E. (2016) · Molecular Psychiatry · doi:10.1038/mp.2015.210 · Cited by 112 · see citing works
McNally, G. P., & Cole, S. (2006) · Behavioral Neuroscience · doi:10.1037/0735-7044.120.2.313 · Cited by 94 · see citing works
Mileykovskiy, B. Y., & Morales, M. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.5731-10.2011 · Cited by 93 · see citing works
Scala, G. D., Mana, M. J., Jacobs, W. J., & Phillips, A. G. (1987) · Physiology & Behavior · doi:10.1016/0031-9384(87)90185-5 · Cited by 89 · see citing works
Dougalis, A. G., Matthews, G. A. C., Bishop, M. W., Brischoux, F., Kobayashi, K., & Ungless, M. A. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08255.x · Cited by 81 · see citing works
Postsynaptic BDNF signalling regulates long‐term potentiation at thalamo‐amygdala afferents
Meis, S., Endres, T., & Leßmann, V. (2011) · The Journal of Physiology · doi:10.1113/jphysiol.2011.220434 · Cited by 76 · see citing works
Self-citationAmygdala NRG1–ErbB4 Is Critical for the Modulation of Anxiety-Like Behaviors
Bi, L.-L., Sun, X.-D., Zhang, J., Lu, Y.-S., Chen, Y.-H., Wang, J., Geng, F., Liu, F., Zhang, M., Liu, J.-H., et al. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2014.274 · Cited by 76 · see citing works
Silberman, Y., & Winder, D. G. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.02.014 · Cited by 67 · see citing works
Asmundson, G. J. G., Bonin, M. F., Frombach, I. K., & Norton, G. R. (2000) · Behaviour Research and Therapy · doi:10.1016/s0005-7967(99)00101-1 · Cited by 65 · see citing works
A Central Amygdala-Substantia Innominata Neural Circuitry Encodes Aversive Reinforcement Signals.
Cui, Y., Lv, G., Jin, S., Peng, J., Yuan, J., He, X.-B., Gong, H., Xu, F.-Q., Xu, T.-H., & Li, H. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.10.062 · Cited by 59 · see citing works
Edelmann, E., & Leßmann, V. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00025 · Cited by 51 · see citing works
Nagatsu, I., Karasawa, N., Kondo, Y., & Inagaki, S. (1979) · Histochemistry and Cell Biology · doi:10.1007/bf00490094 · Cited by 50 · see citing works
Lee, H. J., Wheeler, D. S., & Holland, P. C. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07680.x · Cited by 36 · see citing works
Dopamine attenuates evoked inhibitory synaptic currents in central amygdala neurons
Naylor, J. C., Li, Q., Kang-Park, M.-H., Wilson, W. A., Kuhn, C. M., & Moore, S. D. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07457.x · Cited by 22 · see citing works
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Dopamine and glutamate in schizophrenia: biology, symptoms and treatment
McCutcheon, R. A., Krystal, J. H., & Howes, O. D. (2020) · World Psychiatry · doi:10.1002/wps.20693 · Cited by 612 · see citing works
GABA and glutamate neurons in the VTA regulate sleep and wakefulness
Yu, X., Li, W., Ma, Y., Tossell, K., Harris, J. J., Harding, E. C., Ba, W., Miracca, G., Wang, D., Li, L., et al. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0288-9 · Cited by 317 · see citing works
Neural mechanisms of social homeostasis
Matthews, G. A., & Tye, K. M. (2019) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.14016 · Cited by 273 · see citing works
Classification of midbrain dopamine neurons using single-cell gene expression profiling approaches
Poulin, J.-F., Gaertner, Z., Moreno-Ramos, O. A., & Awatramani, R. (2020) · Trends in Neurosciences · doi:10.1016/j.tins.2020.01.004 · Cited by 238 · see citing works
“DA neurons in this region also might be embedded in the circuits that transduce the antinociceptive effects of morphine [52], as well as in fear-induced learning [53].”
BackgroundState-specific gating of salient cues by midbrain dopaminergic input to basal amygdala
Lutas, A., Kucukdereli, H., Alturkistani, O., Carty, C., Sugden, A. U., Fernando, K., Diaz, V. E., Flores-Maldonado, V., & Andermann, M. L. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0506-0 · Cited by 166 · see citing works
Salinas-Hernández, X. I., Vogel, P., Betz, S., Kalisch, R., Sigurdsson, T., & Duvarci, S. (2018) · eLife · doi:10.7554/elife.38818 · Cited by 181 · see citing works
Neuromodulation in circuits of aversive emotional learning
Likhtik, E., & Johansen, J. P. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0503-3 · Cited by 162 · see citing works
Pain: A Precision Signal for Reinforcement Learning and Control
Seymour, B. (2019) · Neuron · doi:10.1016/j.neuron.2019.01.055 · Cited by 164 · see citing works
The neural circuitry of social homeostasis: Consequences of acute versus chronic social isolation
Lee, C. R., Chen, A., & Tye, K. M. (2021) · Cell · doi:10.1016/j.cell.2021.02.028 · Cited by 138 · see citing works
“Although historically regarded as a caudal extension of VTA dopamine neurons, DRN dopamine neurons project to distinct downstream regions and are functionally different from VTA dopamine neurons (Cho et al., 2017; Dougalis et al., 2012; Groessl et al., 2018; Hasue and Shammah-Lagnado, 2002; Matthews et al., 2016).”
BackgroundTang, W., Kochubey, O., Kintscher, M., & Schneggenburger, R. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.1796-19.2020 · Cited by 123 · see citing works
“Furthermore, dopamine neurons located in the dorsal raphe that project to the CeA, and dopamine neurons of the lateral portion of the substantia nigra that project to the posterior striatum, were recently shown to be involved in aversive learning (Groessl et al., 2018; Menegas et al., 2018).”
BackgroundFrontera, J. L., Aïssa, H. B., Sala, R. W., Mailhes‐Hamon, C., Georgescu, I. A., Léna, C., & Popa, D. (2020) · Nature Communications · doi:10.1038/s41467-020-18953-0 · Cited by 126 · see citing works
Lateral septum as a nexus for mood, motivation, and movement
Wirtshafter, H. S., & Wilson, M. A. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.03.029 · Cited by 122 · see citing works
Yu, W., Pati, D., Pina, M. M., Schmidt, K. T., Boyt, K. M., Hunker, A. C., Zweifel, L. S., McElligott, Z. A., & Kash, T. L. (2021) · Neuron · doi:10.1016/j.neuron.2021.03.001 · Cited by 112 · see citing works
Cai, L. X., Pizano, K., Gundersen, G. W., Hayes, C. L., Fleming, W., Holt, S., Cox, J., & Witten, I. B. (2020) · eLife · doi:10.7554/elife.54936 · Cited by 104 · see citing works
Goldstein, D. S. (2019) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00396.2018 · Cited by 96 · see citing works
“Individuals with relatively efficient central and autonomic catecholamine systems might have had survival advantages during their reproductive years in terms of being able to increase rapidly and massively the delivery of catecholamines to their receptors as part of vigilance (7), remembering distressing events (19, 4…”
BackgroundThe Raphe Dopamine System Controls the Expression of Incentive Memory
Lin, R., Liang, J., Wang, R., Yan, T., Zhou, Y., Liu, Y., Feng, Q., Sun, F., Li, Y., Li, A., et al. (2020) · Neuron · doi:10.1016/j.neuron.2020.02.009 · Cited by 93 · see citing works
“Here, we found that, besides responding to naturally incentive stimuli with either positive or negative valence (Figure S2) as shown in the previous studies (Cho et al., 2017; Groessl et al., 2018), DRN DA neurons can acquire excitatory responses through learning to the previously neutral cues that are conditioned wit…”
ResultCerebellar modulation of synaptic input to freezing-related neurons in the periaqueductal gray
Vaaga, C. E., Brown, S. T., & Raman, I. M. (2020) · eLife · doi:10.7554/elife.54302 · Cited by 89 · see citing works
Aversion hot spots in the dopamine system
Verharen, J. P. H., Zhu, Y., & Lammel, S. (2020) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2020.02.002 · Cited by 79 · see citing works
“general motivational salience, thereby providing a neurocomputational mechanism through which DR/PAG DA may facilitate learning [27].”
BackgroundPinto, D. F. C., Yang, H., Dorocic, I. P., de Jong, J. W., Han, V. J., Peck, J. R., Zhu, Y., Liu, C. J., Beier, K. T., Smidt, M. P., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-12392-2 · Cited by 76 · see citing works
Liao, X., Wang, W., Wang, L., Jin, H., Shu, L., Xu, X., & Zheng, Y. (2020) · Nano Energy · doi:10.1016/j.nanoen.2020.105548 · Cited by 61 · see citing works
The modulation of emotional and social behaviors by oxytocin signaling in limbic network
Triana-Del Rio, R., Ranade, S., Guardado, J., LeDoux, J., Klann, E., & Shrestha, P. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.1002846 · Cited by 58 · see citing works
“Dopamine also gates the associative learning of fear to switch from danger to safety conditioning (Groessl et al., 2018; Luo et al., 2018).”
BackgroundCho, J. R., Chen, X., Kahan, A., Robinson, J. E., Wagenaar, D. A., & Gradinaru, V. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.2690-20.2021 · Cited by 56 · see citing works
“The absence of aversive cue responses was puzzling, given that our and other previous results from freely-moving photometry or microendoscopic imaging showed robust increases (Fig. 1I; Groessl et al., 2018; Lin et al., 2020).”
BackgroundResultInfluentialThe ventrolateral periaqueductal grey updates fear via positive prediction error
Walker, R. A., Wright, K. M., Jhou, T. C., & McDannald, M. A. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14536 · Cited by 55 · see citing works
Therapeutic Challenges of Post-traumatic Stress Disorder: Focus on the Dopaminergic System
Torrisi, S. A., Leggio, G. M., Drago, F., & Salomone, S. (2019) · Frontiers in Pharmacology · doi:10.3389/fphar.2019.00404 · Cited by 59 · see citing works
“Besides these classic DAergic nuclei, relatively less-studied DAergic neurons in the ventral periaqueductal gray (vPAG) and dorsal raphe nucleus (DRN) finely modulate specific physiological functions, such as associative learning of fear, arousal states and social behavior (Matthews et al., 2016; Cho et al., 2017; Gro…”
BackgroundLaurent, R. S., Damonte, V. M., Tsuda, A. C., & Kauer, J. A. (2020) · Neuron · doi:10.1016/j.neuron.2020.02.029 · Cited by 51 · see citing works
“, 1991; Vianna and Brandão, 2003), such as the PAG dopaminergic input to the central amygdala that is integral for fear learning (Groessl et al., 2018) and to the bed nucleus of the stria terminalis that is antinociceptive (Li et al.”
BackgroundDopamine D2R is Required for Hippocampal-dependent Memory and Plasticity at the CA3-CA1 Synapse
Espadas, I., Ortiz, Ó., García‐Sanz, P., Sanz‐Magro, A., Alberquilla, S., Solís, Ó., Delgado-Garcia, J. M., Gruart, A., & Moratalla, R. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa354 · Cited by 49 · see citing works
“Strong evidence supports the important role that dopamine plays in associative learning and memory tasks (Groessi et al. 2018; Handler et al. 2019; Iino et al. 2020).”
BackgroundFu, 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
Bruzsik, B., Bíró, L., Zelena, D., Sipos, E., Szebik, H., Sarosdi, K. R., Horváth, O., Farkas, I., Csillag, V., Finszter, C. K., et al. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.1944-20.2020 · Cited by 40 · see citing works
Schleyer, M. H., Weiglein, A., Thoener, J., Strauch, M., Hartenstein, V., Weigelt, M. K., Schuller, S., Saumweber, T., Eichler, K., Rohwedder, A., et al. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.0290-20.2020 · Cited by 40 · see citing works
“…et al., 2006; Rohwedder et al., 2016; Saumweber et al., 2018; Eschbach et al., 2020; adult flies: Schwaerzel et al., 2003; Claridge-Chang et al., 2009; Liu et al., 2012) (a similar scenario may be emerging in vertebrates, too: Lammel et al., 2012; Groessl et al., 2018; Menegas et al., 2018).”
BackgroundDesmaison, J. D. U., Sala, R. W., Ayyaz, A., Nondhalee, P., Popa, D., & Léna, C. (2023) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2023.1176668 · Cited by 38 · see citing works
“A reciprocal pathway connects ventrolateral periaqueductal grey and the central nucleus of the amygdala in which dopaminergic neurons from the ventrolateral periaqueductal grey seem to encode prediction error during fear conditioning (Groessl et al., 2018).”
BackgroundAn active inference perspective for the amygdala complex
Sladky, R., Kargl, D., Haubensak, W. E., & Lamm, C. (2023) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2023.11.004 · Cited by 37 · see citing works
“Changes in (somatic) arousal are also detected by the brainstem, closing the regulation loop via direct [57,67] and indirect neural connections (e.g., via insula [44]) and neuromodulatory effects [25] on the amygdala.”
InfluentialSelf-citationIncreased anxiety-like behavior following circuit-specific catecholamine denervation in mice
Ferrazzo, S., Gunduz-Cinar, O., Stefanova, N., Pollack, G. A., Holmes, A., Schmuckermair, C., & Ferraguti, F. (2019) · Neurobiology of Disease · doi:10.1016/j.nbd.2019.01.009 · Cited by 36 · see citing works
“vPAG DAergic neurons markedly impairs cued fear conditioning without leading to overt effects in the elevated plus-maze or light dark exploration tests (Groessl et al., 2018).”
Neurotrophin signalling in amygdala-dependent cued fear learning
Meis, S., Endres, T., & Leßmann, V. (2020) · Cell and Tissue Research · doi:10.1007/s00441-020-03260-3 · Cited by 36 · see citing works
Self-citationThe Raphe Dopamine System: Roles in Salience Encoding, Memory Expression, and Addiction
Lin, R., Liang, J., & Luo, M. (2021) · Trends in Neurosciences · doi:10.1016/j.tins.2021.01.002 · Cited by 36 · see citing works
Tinbergen’s challenge for the neuroscience of behavior
Pfaff, D. W., Tabansky, I., & Haubensak, W. E. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1903589116 · Cited by 32 · see citing works
Self-citationLi, M., Yang, X., Yang, J., Li, T., Cui, C., Peng, X., Lei, J., Ren, K., Ming, J., Zhang, P., et al. (2024) · Neuron · doi:10.1016/j.neuron.2024.06.026 · Cited by 33 · see citing works
Dopaminergic circuits controlling threat and safety learning
Duvarci, S. (2024) · Trends in Neurosciences · doi:10.1016/j.tins.2024.10.001 · Cited by 31 · see citing works
“By contrast, dopamine projections from periaqueductal gray/dorsal raphe (PAG/DR) to central nucleus of the amygdala (CEA) encode a threat prediction error signal that is crucial for driving associative threat learning [38].”
BackgroundA possible evolutionary function of phenomenal conscious experience of pain
Kolodny, O., Moyal, R., & Edelman, S. (2021) · Neuroscience of Consciousness · doi:10.1093/nc/niab012 · Cited by 31 · see citing works
“Although the representations of bidding strength must be distinct from those of dopamine-mediated reinforcement learning credit, they may still involve dopamine, as suggested by the recent finding that in the dorsal tegmentum, dopamine neurons gate associative learning of fear (Groessl et al. 2018).”
ResultThreat and Bidirectional Valence Signaling in the Nucleus Accumbens Core
Ray, M. H., Moaddab, M., & McDannald, M. A. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.1107-21.2021 · Cited by 29 · see citing works
“This network includes traditional “ reward ” regions (Reynolds and Berridge, 2002; Pauli et al., 2015; Bouchet et al., 2018; Groessl et al., 2018; Cai et al., 2020; Piantadosi et al., 2020; Stephenson-Jones et al., 2020; Moaddab et al., 2021; Moaddab and McDannald, 2021).”
BackgroundWright, K. M., Jhou, T. C., Pimpinelli, D., & McDannald, M. A. (2019) · eLife · doi:10.7554/elife.50054 · Cited by 25 · see citing works
The amygdala instructs insular feedback for affective learning
Kargl, D., Kaczanowska, J., Ulonska, S., Groessl, F., Piszczek, Ł., Lazović, J., Buehler, K., & Haubensak, W. E. (2020) · eLife · doi:10.7554/elife.60336 · Cited by 25 · see citing works
“For neural recording experiments, three to five animals were required (effect size 0.3; Groessl et al., 2018).”
BackgroundMethodInfluentialSelf-citationChoi, J. E., Choi, D. I., Lee, J., Kim, J., Kim, M. J., Hong, I., Jung, H., Sung, Y., Kim, J., Kim, T., et al. (2022) · Science Advances · doi:10.1126/sciadv.abo7527 · Cited by 23 · see citing works
Dopaminergic circuits underlying associative aversive learning
Zafiri, D., & Duvarci, S. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.1041929 · Cited by 23 · see citing works
“Notably, PAG/DR DA neurons projecting to CEA encode a positive prediction error (PE) signal for aversive stimuli that drives associative aversive learning in CEA (Groessl et al., 2018).”
BackgroundMeCP2 in cholinergic interneurons of nucleus accumbens regulates fear learning
Zhang, Y., Zhu, Y., Cao, S.-X., Sun, P., Yang, J.-M., Xia, Y., Xie, S., Yu, X.-D., Fu, J., Shen, C.-J., et al. (2020) · eLife · doi:10.7554/elife.55342 · Cited by 20 · see citing works
How do stupendous cannabinoids modulate memory processing via affecting neurotransmitter systems?
Vaseghi, S., Nasehi, M., & Zarrindast, M. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.10.018 · Cited by 21 · see citing works
Milton, A. L. (2019) · F1000Research · doi:10.12688/f1000research.20053.1 · Cited by 15 · see citing works
Retrorubral field is a hub for diverse threat and aversive outcome signals
Moaddab, M., & McDannald, M. A. (2021) · Current Biology · doi:10.1016/j.cub.2021.02.055 · Cited by 15 · see citing works
Thoener, J., König, C., Weiglein, A., Toshima, N., Mancini, N., Amin, F., & Schleyer, M. H. (2021) · Biology Open · doi:10.1242/bio.058198 · Cited by 20 · see citing works
“A similar dichotomy of appetitive and aversive reinforcement signals carried by different sets of dopaminergic neurons may also be emerging in vertebrates (Groessl et al., 2018; Lammel et al., 2012; Menegas et al., 2018).”
Aksoy-Aksel, A., Gall, A., Seewald, A., Ferraguti, F., & Ehrlich, I. (2021) · eLife · doi:10.7554/elife.63708 · Cited by 17 · see citing works
He, Z., Jiang, Y., Gu, S., Wu, D., Qin, D., Feng, G., Ma, X., Huang, J. H., & Wang, F. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.713762 · Cited by 17 · see citing works
Wang, W., Wang, D., Zhao, D., Xu, L., Jiang, S., Zhang, Y., Cui, M., Liu, J., Meng, F., Liu, C., et al. (2024) · Translational Psychiatry · doi:10.1038/s41398-024-03093-6 · Cited by 16 · see citing works
Gray areas: Neuropeptide circuits linking the Edinger-Westphal and Dorsal Raphe nuclei in addiction
Pomrenze, M. B., Walker, L. C., & Giardino, W. J. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108769 · Cited by 14 · see citing works
Zhao, Q. J., Ito, T., Soko, C., Hori, Y., Furuyama, T., Hioki, H., Konno, K., Yamasaki, M., Watanabe, M., Ohtsuka, S., et al. (2022) · eNeuro · doi:10.1523/eneuro.0121-22.2022 · Cited by 14 · see citing works
“projections onto the CeA or BNST are glutamatergic It has been suggested that the DA neurons corelease glutamate as well as dopamine (Matthews et al., 2016; Groessl et al., 2018).”
BackgroundResultInfluentialHamati, R., Ahrens, J., Shvetz, C., Holahan, M. R., & Tuominen, L. J. (2023) · European Journal of Neuroscience · doi:10.1111/ejn.16157 · Cited by 14 · see citing works
“Thus, SNpc and DRN DA neurons have some overlapping role with VTA DA neurons in the encoding of fear conditioning and extinction.”
BackgroundMethodInfluentialKirouac, G. J. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105989 · Cited by 16 · see citing works
Zafiri, D., Salinas-Hernández, X. I., Biasi, E. S. D., Rebelo, L., & Duvarci, S. (2025) · Nature Communications · doi:10.1038/s41467-025-58382-5 · Cited by 14 · see citing works
“Notably, inhibitoryresponses to aversive USomissionswerealsoabsentinthedorsaltegmentalDAneuronsthat have been shown to encode PE signals to gate fear learning 29 , further supporting the notion of a general lack of negative PE signaling in DA neurons encoding PEs for aversive stimuli.”
Rebusi, R., Olorocisimo, J. P., Briones, J. C., Ohta, Y., Haruta, M., Takehara, H., Tashiro, H., Sasagawa, K., & Ohta, J. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.667708 · Cited by 14 · see citing works
Forebrain-Midbrain Circuits and Peptides Involved in Hyperalgesia After Chronic Alcohol Exposure
Gilpin, N. W. (2021) · Alcohol research · doi:10.35946/arcr.v41.1.13 · Cited by 14 · see citing works
Modulation of aversive value coding in the vertebrate and invertebrate brain
Perisse, E., Miranda, M., & Trouche, S. G. (2023) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2023.102696 · Cited by 12 · see citing works
Pati, D., & Kash, T. L. (2021) · Journal of Neurophysiology · doi:10.1152/jn.00251.2021 · Cited by 13 · see citing works
Reevaluating the ability of cerebellum in associative motor learning
Li, D., Yao, J., Sun, L., Wu, B., Li, X., Liu, S., Hou, J., Liu, H., Sui, J.-F., & Wu, G. (2019) · Scientific Reports · doi:10.1038/s41598-019-42413-5 · Cited by 13 · see citing works
Asymmetric representation of aversive prediction errors in Pavlovian threat conditioning
Ojala, K. E., Tzovara, A., Poser, B. A., Lutti, A., & Bach, D. R. (2022) · NeuroImage · doi:10.1016/j.neuroimage.2022.119579 · Cited by 12 · see citing works
Casey, E., Avale, M. E., Kravitz, A. V., & Rubinstein, M. (2023) · Brain Structure and Function · doi:10.1007/s00429-023-02614-1 · Cited by 12 · see citing works
“We found that the indirect mixed D1/ D2R DA agonist cocaine (20 mg/kg, i.p.) increased the number of c-FOS + nuclei only in the caudal part of the CeL and the caudal and frontoventral regions of the CeC (Fig.”
BackgroundInfluentialDissociation of impulsive traits by subthalamic metabotropic glutamate receptor 4
Piszczek, L., Constantinescu, A., Kargl, D., Lazović, J., Pekcec, A., Nicholson, J. R., & Haubensak, W. E. (2022) · eLife · doi:10.7554/elife.62123 · Cited by 11 · see citing works
Self-citationOleson, E. B., & Roberts, J. B. (2018) · Brain Research · doi:10.1016/j.brainres.2018.11.043 · Cited by 11 · see citing works
“And, recent evidence suggests dopamine release events arising from non-canonical dopamine populations in the periaqueductal gray and in the dorsal raphe interact with the amygdala to influence behavioral responses to fear (Groessl et al., 2018).”
BackgroundWank, I., Pliota, P., Badurek, S., Kraitsy, K., Kaczanowska, J., Griessner, J., Kreitz, S., Heß, A., & Haubensak, W. E. (2021) · Communications Biology · doi:10.1038/s42003-021-02262-3 · Cited by 11 · see citing works
Self-citationComyn, T., Préat, T., Pavlowsky, A., & Plaçais, P.-Y. (2024) · eLife · doi:10.7554/elife.92085 · Cited by 11 · see citing works
“…phasic activation in response to an aversive unconditioned stimulus (US) and to a conditioned stimulus (CS) associated with the aversive US ( Groessl et al., 2018 ; Zafiri and Duvarci, 2022 ), which could preferentially activate the D1 receptor-expressing CeA neurons during aversive…”
BackgroundLiu, M., Tian, X.-Y., Fang, T., Wu, N., Li, H., & Li, J. (2023) · Molecular Neurobiology · doi:10.1007/s12035-023-03312-z · Cited by 10 · see citing works
“This group of cells constitutes the mesolimbic and mesocortical pathways, which is known to be involved in reward-related reinforcement, incentive salience, aversion-related cognition, and decision-making [45, 46].”
BackgroundRules for aversive learning and decision-making
Yau, J. O.-Y., & McNally, G. P. (2018) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2018.08.006 · Cited by 10 · see citing works
Fear expression is suppressed by tyrosine administration
Soranzo, A., & Aquili, L. (2019) · Scientific Reports · doi:10.1038/s41598-019-52610-x · Cited by 9 · see citing works
Yan, Y., Aierken, A., Wang, C., Jin, W., Quan, Z., Wang, Z., Qing, H., Ni, J., & Zhao, J. (2022) · The Neuroscientist · doi:10.1177/10738584211069977 · Cited by 8 · see citing works
Comyn, T., Préat, T., Pavlowsky, A., & Plaçais, P.-Y. (2024) · eLife · doi:10.7554/elife.92085.3 · Cited by 8 · see citing works
Four individually identified paired dopamine neurons signal taste punishment in larval DrosophilaPreprint
Weber, D., Vogt, K., Miroschnikow, A., Pankratz, M. J., & Thum, A. S. (2023) · eLife · doi:10.7554/elife.91387 · Cited by 14 · see citing works
Separable dorsal raphe dopamine projections mimic the facets of a loneliness-like statePreprint
Lee, C. R., Matthews, G. A., Lemieux, M., Wasserlein, E. M., Borio, M., Miranda, R. L., Keyes, L. R., Schneider, G. P., Jia, C., Tran, A., et al. (2025) · eLife · doi:10.7554/elife.105955 · Cited by 8 · see citing works
Neuromodulation of Memory Formation and Extinction
Bostancıklıoğlu, M. (2020) · Current Neurovascular Research · doi:10.2174/1567202617999200421202818 · Cited by 7 · see citing works
Regulation of stress-induced sleep perturbations by dorsal raphe VGLUT3 neurons in male mice
Henderson, F., Dumas, S., Gangarossa, G., Bernard, V., Pujol, M., Poirel, O., Pietrancosta, N., Mestikawy, S. E., Daumas, S., & Fabre, V. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114411 · Cited by 7 · see citing works
Cell type specificity for circuit output in the midbrain dopaminergic system
Blaess, S., & Krabbe, S. (2023) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2023.102811 · Cited by 6 · see citing works
“The ventral periaqueductal grey (vPAG) is the primary source of innervation of the central AMY (C-AMY) [25,99] and the bed nucleus of the stria terminalis (BNST) [25,100].”
Experience-dependent changes in affective valence of taste in male mice
Hamada, S., Mikami, K., Ueda, S., Nagase, M., Nagashima, T., Yamamoto, M., Bito, H., Takemoto‐Kimura, S., Ohtsuka, T., & Watabe, A. M. (2023) · Molecular Brain · doi:10.1186/s13041-023-01017-x · Cited by 6 · see citing works
“In fact, Sst- and Prkcd-positive neurons exhibit contradictory responses in fear learning and pain-like behavior [41, 42].”
BackgroundXie, H., Wu, D., Gao, X., Wang, N., & Xiao, Z. (2020) · Neuroscience · doi:10.1016/j.neuroscience.2020.05.038 · Cited by 5 · see citing works
Four individually identified paired dopamine neurons signal taste punishment in larval Drosophila
Weber, D., Vogt, K., Miroschnikow, A., Pankratz, M. J., & Thum, A. S. (2025) · eLife · doi:10.7554/elife.91387.4 · Cited by 4 · see citing works
Plasticity of amygdala neurons underlying fear learning and extinction
Morozov, A., & Ito, W. (2020) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-815134-1.00006-4 · Cited by 4 · see citing works
Khairuddin, S., Lim, W. L., Aquili, L., Tsui, K. C., Tse, A. C.-K., Jayalath, S., Varma, R., Sharp, T., Benazzouz, A., Steinbusch, H. W. M., et al. (2023) · Cells · doi:10.3390/cells12111449 · Cited by 3 · see citing works
“Recent studies suggest that DA neurons in the DRN are involved in social interaction [17], reward memories [55], arousal, wakefulness [56], and fear response [57].”
BackgroundDefining circuit-specific roles for G protein-coupled receptors in aversive learning
Gowrishankar, R., & Bruchas, M. R. (2019) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2019.01.002 · Cited by 3 · see citing works
Four Individually Identified Paired Dopamine Neurons Signal Taste Punishment in Larval DrosophilaPreprint
Weber, D., Vogt, K., Miroschnikow, A., Pankratz, M. J., & Thum, A. S. (2023) · eLife · doi:10.7554/elife.91387.1 · Cited by 4 · see citing works
Li, E., Niu, W., Lu, C., Wang, M., Xu, X., Xu, K., & Xu, P. (2025) · Ageing Research Reviews · doi:10.1016/j.arr.2025.102743 · Cited by 2 · see citing works
García-Verdugo, M., Rodríguez-Martín, P., Gustincich, S., Lanciego, J. L., Murer, M. G., Jercog, P. E., & Moratalla, R. (2025) · Neurobiology of Disease · doi:10.1016/j.nbd.2025.107173 · Cited by 2 · see citing works
Zhang, X., Xu, J., Ren, S., Yang, Q., Liu, M., Chang, X., Sun, Y., Gao, X., Zhong, Y., Liu, Y., et al. (2022) · Advanced Electronic Materials · doi:10.1002/aelm.202200610 · Cited by 2 · see citing works
Roberta, C., Schluessel, V., Hofmann, H. A., & Hofmann, M. H. (2023) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2023.102342 · Cited by 2 · see citing works
Xie, H., Tian, Y., Li, Z., Wang, K., Li, R., Yi, S., Chen, A., Chen, J., Liu, J., Wei, X., et al. (2023) · Molecular Neurobiology · doi:10.1007/s12035-023-03667-3 · Cited by 2 · see citing works
Moaddab, M., Wright, K. M., & McDannald, M. A. (2020) · Scientific Reports · doi:10.1038/s41598-020-74457-3 · Cited by 2 · see citing works
Asymmetric representation of aversive prediction errors in Pavlovian threat conditioningPreprint
Ojala, K. E., Tzovara, A., Poser, B. A., Lutti, A., & Bach, D. R. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.07.10.197665 · Cited by 2 · see citing works
“US occurrence have not been shown to be responsive to US omission (Groessl et al., 2018; Walker et al., 2020); as such this remains a speculative interpretation.”
BackgroundToshima, N., Behrad, A., Behnke, F., Kaushik, G., Weiglein, A., Strauch, M., Thoener, J., Kobler, O., Wang, M. L. M., Dörr, M., et al. (2025) · eLife · doi:10.7554/elife.106148.1 · Cited by 2 · see citing works
Paci, E., Lumb, B. M., Apps, R., Lawrenson, C. L., & Moran, R. (2023) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2023.1148604 · Cited by 1 · see citing works
Separable dorsal raphe dopamine projections mimic the facets of a loneliness-like state
Lee, C. R., Matthews, G. A., Lemieux, M., Wasserlein, E. M., Borio, M., Miranda, R. L., Keyes, L. R., Schneider, G. P., Jia, C., Tran, A., et al. (2025) · eLife · doi:10.1101/2025.02.03.636224 · Cited by 4 · see citing works
“…DRN DAT circuit attributes we describe above may further enable this system to modulate other diverse forms of behavior (e.g. arousal Cho et al., 2017 , fear/reward associations Lin et al., 2020 ; Groessl et al., 2018 , and antinociception Li et al., 2016 ; Meyer et al., 2009 ; Yu et al., 2021 ).”
Heuermann, R. J., & Gereau, R. W. (2025) · Journal of Neurophysiology · doi:10.1152/jn.00135.2025 · Cited by 1 · see citing works
Bijoch, Ł., Wiśniewska, J., & Beroun, A. (2025) · European Journal of Neuroscience · doi:10.1111/ejn.70292 · Cited by 1 · see citing works
“Ablation or chemogenetic blocking of these neurons reduced fear learning (Groessl et al. 2018).”
Distinct threat and valence signals in rat nucleus accumbens corePreprint
Ray, M. H., Moaddab, M., & McDannald, M. A. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.05.27.446063 · Cited by 1 · see citing works
Comyn, T., Préat, T., Pavlowsky, A., & Plaçais, P.-Y. (2024) · eLife · doi:10.7554/elife.92085.1 · Cited by 1 · see citing works
Comyn, T., Préat, T., Pavlowsky, A., & Plaçais, P.-Y. (2024) · eLife · doi:10.7554/elife.92085.2 · Cited by 1 · see citing works
Separable Dorsal Raphe Dopamine Projections Mimic the Facets of a Loneliness-like StatePreprint
Lee, C. R., Matthews, G. A., Lemieux, M., Wasserlein, E. M., Borio, M., Miranda, R. L., Keyes, L. R., Schneider, G. P., Jia, C., Tran, A., et al. (2025) · eLife · doi:10.7554/elife.105955.2 · Cited by 1 · see citing works
- Authors
- Groessl, F., Munsch, T., Meis, S., Griessner, J., Kaczanowska, J., Pliota, P., Kargl, D., Badurek, S., Kraitsy, K., Rassoulpour, A., Zuber, J., Lessmann, V., & Haubensak, W.
- Affiliations
- Research Institute of Molecular Pathology (AT)
- Center for Behavioral Brain Sciences (DE)
- Vienna BioCenter Core Facilities (AT)
- Charles River Laboratories (United States) (US)
- Corresponding author
- Haubensak, Wulf
- ORCID
- Venue
- Nature Neuroscience
- Published
- 2018-06-27
- Volume
- 21
- Issue
- 7
- Pages
- 952-962
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC6166775
- OpenAlex
- W2811303733
- Cited by
- 118
- References
- 61
- Citations by year
- 2026: 6 · 2025: 15 · 2024: 10 · 2023: 16 · 2022: 9 · 2021: 18 · 2020: 23 · 2019: 16 · 2018: 5
- FWCI
- 9.23
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- fear conditioning, ventral periaqueductal gray, dorsal raphe nucleus, central amygdala, long-term potentiation, associative learning, Hebbian plasticity, fear memory
- MeSH terms
- Animals, Association Learning, Behavior, Animal, Conditioning, Classical, Fear, Male, Neural Pathways, Periaqueductal Gray, Tegmentum Mesencephali, Long-Term Potentiation, Mice, Dopaminergic Neurons
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