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Input-specific control of reward and aversion in the ventral tegmental area
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Ventral tegmental area (VTA) dopamine neurons have important roles in adaptive and pathological brain functions related to reward and motivation. However, it is unknown whether subpopulations of VTA dopamine neurons participate in distinct circuits that encode different motivational signatures, and whether inputs to the VTA differentially modulate such circuits. Here we show that, because of differences in synaptic connectivity, activation of inputs to the VTA from the laterodorsal tegmentum and the lateral habenula elicit reward and aversion in mice, respectively. Laterodorsal tegmentum neurons preferentially synapse on dopamine neurons projecting to the nucleus accumbens lateral shell, whereas lateral habenula neurons synapse primarily on dopamine neurons projecting to the medial prefrontal cortex as well as on GABAergic (γ-aminobutyric-acid-containing) neurons in the rostromedial tegmental nucleus. These results establish that distinct VTA circuits generate reward and aversion, and thereby provide a new framework for understanding the circuit basis of adaptive and pathological motivated behaviours.
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“In support of the latter result, habenula stimulation elicits inhibitory electrophysiological dopamine responses139–141 through an intermediate reticular nucleus138, rather than the excitatory responses required for a postulated aversive dopamine influence on place preferences137.”
From Dopamine reward prediction-error signalling: A two-component response (2016) · cites this paper as [137]
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“Anatomically, this subpopulation of DA neurons projects to the medial prefrontal cortex and the medial shell of the nucleus accumbens (Lammel et al., 2011; Lammel et al., 2012).”
From Dopamine regulates aversive contextual learning and associated in vivo synaptic plasticity in the Hippocampus (2016) · cites this paper as Lammel et al., 2012
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Cites
The Mouse Brain in Stereotaxic Coordinates
Paxinos, G. (2001) · Cited by 12,859
Wickersham, I. R., Sullivan, H., & Seung, H. (2010) · Nature Protocols · doi:10.1038/nprot.2009.248 · Cited by 4,905
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
Dissecting components of reward: ‘liking’, ‘wanting’, and learning
Berridge, K. C., Robinson, T. E., & Aldridge, J. W. (2009) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2008.12.014 · Cited by 1,942
Dopamine neuron systems in the brain: An update
Björklund, A., & Dunnett, S. B. (2007) · Trends in Neurosciences · doi:10.1016/j.tins.2007.03.006 · Cited by 1,777
Multiple dopamine functions at different time courses
Schultz, W. (2007) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.28.061604.135722 · Cited by 1,415
Two types of dopamine neuron distinctly convey positive and negative motivational signals
Matsumoto, M., & Hikosaka, O. (2009) · Nature · doi:10.1038/nature08028 · Cited by 1,378
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
Whole-Brain Mapping of Direct Inputs to Midbrain Dopamine Neurons
Watabe‐Uchida, M., Zhu, L., Ogawa, S. K., Vamanrao, A., & Uchida, N. (2012) · Neuron · doi:10.1016/j.neuron.2012.03.017 · Cited by 1,277
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
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Projection-Target-Defined Effects of Orexin and Dynorphin on VTA Dopamine Neurons
Baimel, C., Lau, B. K., Qiao, M., & Borgland, S. L. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.01.030 · Cited by 137
Overriding Phasic Dopamine Signals Redirects Action Selection during Risk/Reward Decision Making
Stopper, C. M., Tse, M. T. L., Montes, D. R., Wiedman, C. R., & Floresco, S. B. (2014) · Neuron · doi:10.1016/j.neuron.2014.08.033 · Cited by 136
Nicotine inhibits the VTA-to-amygdala dopamine pathway to promote anxiety
Nguyen, C., Mondoloni, S., Le Borgne, T., Centeno, I., Come, M., Jehl, J., Solié, C., Reynolds, L. M., Durand-de Cuttoli, R., Tolu, S., et al. (2021) · Neuron · doi:10.1016/j.neuron.2021.06.013 · Cited by 136
Meta-analysis of human prediction error for incentives, perception, cognition, and action
Corlett, P. R., Mollick, J. A., & Kober, H. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-021-01264-3 · Cited by 135
Ellwood, I. T., Patel, T., Wadia, V., Lee, A. T., Liptak, A. T., Bender, K. J., & Sohal, V. S. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.1221-17.2017 · Cited by 132
Neurobiological Mechanisms of Nicotine Reward and Aversion
Wills, L. P., Ables, J. L., Braunscheidel, K. M., Caligiuri, S. P. B., Elayouby, K. S., Fillinger, C., Ishikawa, M., Moen, J. K., & Kenny, P. J. (2022) · Pharmacological Reviews · doi:10.1124/pharmrev.121.000299 · Cited by 134
Wenzel, J. M., Rauscher, N. A., Cheer, J. F., & Oleson, E. B. (2015) · ACS Chemical Neuroscience · doi:10.1021/cn500255p · Cited by 131
Tang, W., Kochubey, O., Kintscher, M., & Schneggenburger, R. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.1796-19.2020 · Cited by 131
Reward processing by the dorsal raphe nucleus: 5-HT and beyondPreprint
Luo, M., Zhou, J., & Liu, Z. (2015) · Learning & Memory · doi:10.1101/lm.037317.114 · Cited by 131
Ikemoto, S., & Bonci, A. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.04.031 · Cited by 129
Stress effects on the neural substrates of motivated behavior
Hollon, N. G., Burgeno, L. M., & Phillips, P. E. M. (2015) · Nature Neuroscience · doi:10.1038/nn.4114 · Cited by 129
Development, wiring and function of dopamine neuron subtypes
Garritsen, O., van Battum, E. Y., Grossouw, L. M., & Pasterkamp, R. J. (2023) · Nature reviews. Neuroscience · doi:10.1038/s41583-022-00669-3 · Cited by 128
Distinct Midbrain and Habenula Pathways Are Involved in Processing Aversive Events in Humans
Hennigan, K., D’Ardenne, K., & McClure, S. M. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.0927-14.2015 · Cited by 127
Laterodorsal tegmentum interneuron subtypes oppositely regulate olfactory cue-induced innate fear
Yang, H., Yang, J., Wang, X., Hao, S., Luo, B., He, X., Zhu, L., Lou, H., Yu, Y., Xu, F., et al. (2016) · Nature Neuroscience · doi:10.1038/nn.4208 · Cited by 127
Breton, J., Charbit, A. R., Snyder, B. J., Fong, P. T. K., Dias, E. V., Himmels, P., Lock, H., & Margolis, E. B. (2018) · The Journal of Comparative Neurology · doi:10.1002/cne.24572 · Cited by 126
Beier, K. T., Gao, X. J., Xie, S. C., DeLoach, K. E., Malenka, R. C., & Luo, L. (2019) · Cell Reports · doi:10.1016/j.celrep.2018.12.040 · Cited by 126
Self-citationRole of nicotinic acetylcholine receptors in regulating dopamine neuron activity
Faure, P., Tolu, S., Valverde, S., & Naudé, J. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.05.040 · Cited by 125
Xiao, C., Zhou, C., Jiang, J., & Cui, Y. (2019) · Acta Pharmacologica Sinica · doi:10.1038/s41401-019-0299-4 · Cited by 124
The molecular pathophysiology of depression and the new therapeutics
Tian, H., Hu, Z., Xu, J., & Wang, C. (2022) · MedComm · doi:10.1002/mco2.156 · Cited by 122
GDNF–Ret signaling in midbrain dopaminergic neurons and its implication for Parkinson disease
Kramer, E. R., & Liss, B. (2015) · FEBS Letters · doi:10.1016/j.febslet.2015.11.006 · Cited by 121
Pistillo, F., Clementi, F., Zoli, M., & Gotti, C. (2014) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2014.10.002 · Cited by 120
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 119
Hsu, Y. A., Wang, S. D., Wang, S., Morton, G., Zariwala, H. A., de la Iglesia, H. O., & Turner, E. E. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1861-14.2014 · Cited by 119
Paraventricular Thalamus Balances Danger and Reward
Choi, E. A., & McNally, G. P. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.3320-16.2017 · Cited by 120
The antero-posterior heterogeneity of the ventral tegmental area
Sánchez-Catalán, M. J., Kaufling, J., Georges, F. E., Veinante, P., & Barrot, M. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.09.025 · Cited by 118
In situ electrochemical generation of nitric oxide for neuronal modulation
Park, J., Jin, K., Sahasrabudhe, A., Chiang, P., Maalouf, J. H., Koehler, F., Rosenfeld, D., Rao, S., Tanaka, T., Khudiyev, T., et al. (2020) · Nature Nanotechnology · doi:10.1038/s41565-020-0701-x · Cited by 118
Pain modulates dopamine neurons via a spinal–parabrachial–mesencephalic circuit
Yang, H., de Jong, J. W., Cerniauskas, I., Peck, J. R., Lim, B. K., Gong, H., Fields, H. L., & Lammel, S. (2021) · Nature Neuroscience · doi:10.1038/s41593-021-00903-8 · Cited by 120
Self-citationRemotely controlled chemomagnetic modulation of targeted neural circuits
Rao, S., Chen, R., LaRocca, A. A., Christiansen, M. G., Senko, A. W., Shi, C. H., Chiang, P., Varnavides, G., Xue, J., Zhou, Y., et al. (2019) · Nature Nanotechnology · doi:10.1038/s41565-019-0521-z · Cited by 116
The dopamine transporter gene SLC6A3: multidisease risks
Reith, M. E. A., Kortagere, S., Wiers, C. E., Sun, H., Kurian, M. A., Galli, A., Volkow, N. D., & Lin, Z. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01341-5 · Cited by 116
Anatomical and single-cell transcriptional profiling of the murine habenular complex
Wallace, M. L., Huang, K. W., Hochbaum, D., Hyun, M., Radeljic, G., & Sabatini, B. L. (2020) · eLife · doi:10.7554/elife.51271 · Cited by 113
Self-citationRabies screen reveals GPe control of cocaine-triggered plasticity
Beier, K. T., Kim, C. K., Hoerbelt, P., Hung, L. W., Heifets, B. D., DeLoach, K. E., Mosca, T. J., Neuner, S., Deisseroth, K. A., Luo, L., et al. (2017) · Nature · doi:10.1038/nature23888 · Cited by 113
Self-citationGuan, Y., Huang, G., Xu, M.-D., Gao, F., Lin, S., Huang, J., Wang, J., Li, Y., Wu, C.-H., Yao, S., et al. (2020) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2020.05.032 · Cited by 113
Role of Mesolimbic Brain-Derived Neurotrophic Factor in Depression
Koo, J. W., Chaudhury, D., Han, M.-H., & Nestler, E. J. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2019.05.020 · Cited by 112
Dopamine Neurons Reflect the Uncertainty in Fear Generalization
Jo, Y. S., Heymann, G., & Zweifel, L. S. (2018) · Neuron · doi:10.1016/j.neuron.2018.09.028 · Cited by 108
Lateral Habenular Burst Firing as a Target of the Rapid Antidepressant Effects of Ketamine
Cui, Y., Hu, S., & Hu, H. (2019) · Trends in Neurosciences · doi:10.1016/j.tins.2018.12.002 · Cited by 111
Topography of Reward and Aversion Encoding in the Mesolimbic Dopaminergic System
Yuan, L., Dou, Y., & Sun, Y.-G. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.0271-19.2019 · Cited by 110
A distinct D1-MSN subpopulation down-regulates dopamine to promote negative emotional state
Liu, Z., Le, Q., Lv, Y., Chen, X., Cui, J., Zhou, Y., Cheng, D., Ma, C., Su, X., Xiao, L., et al. (2021) · Cell Research · doi:10.1038/s41422-021-00588-5 · Cited by 110
The heterogeneity of ventral tegmental area neurons: Projection functions in a mood-related context
Walsh, J. J., & Han, M. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.06.006 · Cited by 108
Kawai, T., Yamada, H., Sato, N., Takada, M., & Matsumoto, M. (2015) · Neuron · doi:10.1016/j.neuron.2015.09.030 · Cited by 108
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Rizzi, G., & Tan, K. R. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00110 · Cited by 109
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Roelfsema, P. R., Denys, D., & Klink, P. C. (2018) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2018.04.001 · Cited by 107
Central Processing of Itch in the Midbrain Reward Center
Su, X., Chen, M., Yuan, Y., Li, Y., Guo, S.-S., Luo, H., Huang, C., Sun, W., Li, Y., Zhu, M. X., et al. (2019) · Neuron · doi:10.1016/j.neuron.2019.03.030 · Cited by 107
Anhedonia in depression symptomatology: appetite dysregulation and defective brain reward processing
Coccurello, R. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.112041 · Cited by 106
Glutamate neurons are intermixed with midbrain dopamine neurons in nonhuman primates and humans
Root, D. H., Wang, H., Liu, B., Barker, D. J., Mód, L., Szocsics, P., Silva, A. C., Maglóczky, Z., & Morales, M. (2016) · Scientific Reports · doi:10.1038/srep30615 · Cited by 106
Direct Bidirectional μ-Opioid Control of Midbrain Dopamine Neurons
Margolis, E. B., Hjelmstad, G. O., Fujita, W., & Fields, H. L. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.2144-14.2014 · Cited by 106
Does the kappa opioid receptor system contribute to pain aversion?
Cahill, C. M., Taylor, A. M. W., Cook, C., Ong, E., Morón, J. A., & Evans, C. J. (2014) · Frontiers in Pharmacology · doi:10.3389/fphar.2014.00253 · Cited by 105
Multiplexed neurochemical signaling by neurons of the ventral tegmental area
Barker, D. J., Root, D. H., Zhang, S., & Morales, M. (2016) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2015.12.016 · Cited by 105
Gardon, O., Faget, L. C., Chung, P. C. S., Matifas, A., Massotte, D., & Kieffer, B. L. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.07.053 · Cited by 105
Nakanishi, S., Hikida, T., & Yawata, S. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.04.026 · Cited by 103
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Benekareddy, M., Stachniak, T. J., Bruns, A., Knoflach, F., von Kienlin, M., Künnecke, B., & Ghosh, A. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.10.032 · Cited by 103
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Hayes, D. J., Duncan, N. W., Xu, J., & Northoff, G. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.06.018 · Cited by 102
Teles, M. C., Cardoso, S. D., & Oliveira, R. F. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2016.00016 · Cited by 102
Yetnikoff, L., Cheng, A. Y., Lavezzi, H. N., Parsley, K. P., & Zahm, D. S. (2015) · Journal of Comparative Neurology · doi:10.1002/cne.23797 · Cited by 101
The role of the habenula in the transition from reward to misery in substance use and mood disorders
Batalla, A., Homberg, J. R., Lipina, T. V., Sescousse, G., Luijten, M., Ivanova, S. А., Schellekens, A., & LOONEN, A. J. M. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.03.019 · Cited by 101
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Cai, J., & Tong, Q. (2022) · Frontiers in Neural Circuits · doi:10.3389/fncir.2022.867053 · Cited by 101
The role of the hippocampus in the consolidation of emotional memories during sleep
Pronier, É., Morici, J. F., & Girardeau, G. (2023) · Trends in Neurosciences · doi:10.1016/j.tins.2023.08.003 · Cited by 101
HCN2 channels in the ventral tegmental area regulate behavioral responses to chronic stress
Zhong, P., Vickstrom, C. R., Liu, X., Hu, Y., Yu, L., Yu, H.-G., & Liu, Q.-S. (2018) · eLife · doi:10.7554/elife.32420 · Cited by 99
“…targeted the lateral PBP, which is a more lateral subdivision of the VTA where dopamine neurons predominantly project to the lateral shell of the NAc (Lammel et al., 2008; Lammel et al., 2011) and play a primary role in reward and motivated behavior (Lammel et al., 2011; Lammel et al., 2012).”
BackgroundInfluentialDiversity and Homogeneity in Responses of Midbrain Dopamine Neurons
Fiorillo, C. D., Yun, S. R., & Song, M. R. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.3886-12.2013 · Cited by 99
Onaolapo, A. Y., & Onaolapo, O. J. (2018) · Pathophysiology · doi:10.1016/j.pathophys.2018.04.002 · Cited by 102
Yoshida, J., Oñate, M., Khatami, L., Vera, J. R., Nadim, F., & Khodakhah, K. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.1535-22.2022 · Cited by 102
Progress in understanding mood disorders: optogenetic dissection of neural circuits
Lammel, S., Tye, K. M., & Warden, M. R. (2014) · Genes, Brain and Behavior · doi:10.1111/gbb.12049 · Cited by 98
Self-citationDopamine tunes prefrontal outputs to orchestrate aversive processing
Weele, C. M. V., Siciliano, C. A., & Tye, K. M. (2018) · Brain Research · doi:10.1016/j.brainres.2018.11.044 · Cited by 98
Self-citationHuang, S., Zhang, Z., Gambeta, E., Xu, S. C., Thomas, C. S., Godfrey, N., Chen, L., M’Dahoma, S., Borgland, S. L., & Zamponi, G. W. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107812 · Cited by 98
Arulpragasam, A. R., Cooper, J. A., Nuutinen, M. R., & Treadway, M. T. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1800444115 · Cited by 99
Functional neuroanatomical review of the ventral tegmental area
Trutti, A. C., Mulder, M., Hommel, B., & Forstmann, B. U. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.01.062 · Cited by 97
Hypothalamic neuronal circuits regulating hunger-induced taste modification
Fu, O., Iwai, Y., Narukawa, M., Ishikawa, A. W., Ishii, K. K., Murata, K., Yoshimura, Y., Touhara, K., Misaka, T., Minokoshi, Y., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-12478-x · Cited by 97
VTA-projecting cerebellar neurons mediate stress-dependent depression-like behaviors
Baek, S. J., Park, J., Kim, J., Yamamoto, Y., & Tanaka, K. (2022) · eLife · doi:10.7554/elife.72981 · Cited by 97
The Dopamine Prediction Error: Contributions to Associative Models of Reward Learning
Nasser, H. M., Calu, D. J., Schoenbaum, G. M., & Sharpe, M. J. (2017) · Frontiers in Psychology · doi:10.3389/fpsyg.2017.00244 · Cited by 97
Ely, B. A., Xu, J., Goodman, W. K., Lapidus, K. A. B., Gabbay, V., & Stern, E. R. (2016) · Human Brain Mapping · doi:10.1002/hbm.23179 · Cited by 96
Review of the cytology and connections of the lateral habenula, an avatar of adaptive behaving
Zahm, D. S., & Root, D. H. (2017) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2017.06.004 · Cited by 96
Brown, P. L., Palacorolla, H., Brady, D. L., Riegger, K. E., Elmer, G. I., & Shepard, P. D. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.1353-16.2016 · Cited by 95
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Browne, C. A., Hammack, R. J., & Lucki, I. (2018) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2018.00046 · Cited by 95
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Lenz, J. D., & Lobo, M. K. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.04.018 · Cited by 95
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Zhang, G., Shen, L., Zhong, W., Xiong, Y., Zhang, L. I., & Tao, H. W. (2018) · Neuron · doi:10.1016/j.neuron.2018.07.023 · Cited by 95
In vivo functional diversity of midbrain dopamine neurons within identified axonal projections
Farassat, N., Costa, K. M., Stojanovic, S., Albert, S., Kovacheva, L., Shin, J., Egger, R., Somayaji, M., Duvarci, S., Schneider, G., et al. (2019) · eLife · doi:10.7554/elife.48408 · Cited by 96
Consolidating the Circuit Model for Addiction
Lüscher, C., & Janak, P. H. (2021) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-092920-123905 · Cited by 94
Mirrione, M. M., Schulz, D., Lapidus, K. A. B., Zhang, S., Goodman, W. K., & Henn, F. A. (2014) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2014.00029 · Cited by 94
Moreines, J. L., Owrutsky, Z. L., & Grace, A. A. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2016.249 · Cited by 93
Hong, S., & Hikosaka, O. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.07.002 · Cited by 92
Grillner, S. E., & Robertson, B. (2015) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2015.01.019 · Cited by 92
Psychosurgery Reduces Uncertainty and Increases Free Will? A Review
Ridder, D. D., Vanneste, S., Gillett, G. R., Manning, P. J., Glue, P., & Langguth, B. (2016) · Neuromodulation Technology at the Neural Interface · doi:10.1111/ner.12405 · Cited by 92
Synaptic and cellular profile of neurons in the lateral habenula
Meye, F. J., Lecca, S., Valentinova, K., & Mameli, M. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00860 · Cited by 92
Dudman, J. T., & Gerfen, C. R. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-374245-2.00017-6 · Cited by 92
Heterogeneity in striatal dopamine circuits: Form and function in dynamic reward seeking
Collins, A. L., & Saunders, B. T. (2020) · Journal of Neuroscience Research · doi:10.1002/jnr.24587 · Cited by 93
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Dautan, D., Huerta-Ocampo, I., Gut, N. K., Valencia, M., Kondabolu, K., Kim, Y., Gerdjikov, T. V., & Mena‐Segovia, J. (2020) · Nature Communications · doi:10.1038/s41467-020-15514-3 · Cited by 91
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Mizumori, S. J. Y., & Baker, P. M. (2017) · Trends in Neurosciences · doi:10.1016/j.tins.2017.06.001 · Cited by 91
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Covey, D. P., Roitman, M. F., & Garris, P. A. (2014) · Trends in Neurosciences · doi:10.1016/j.tins.2014.02.002 · Cited by 90
The Challenge of Understanding the Brain: Where We Stand in 2015
Lisman, J. E. (2015) · Neuron · doi:10.1016/j.neuron.2015.03.032 · Cited by 92
Aversion or Salience Signaling by Ventral Tegmental Area Glutamate Neurons
Root, D. H., Estrin, D. J., & Morales, M. (2018) · iScience · doi:10.1016/j.isci.2018.03.008 · Cited by 90
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Metadata
- Authors
- Lammel, S., Lim, B. K., Ran, C., Huang, K. W., Betley, M. J., Tye, K. M., Deisseroth, K., & Malenka, R. C.
- Affiliations
- Stanford Medicine (US)
- Massachusetts Institute of Technology (US)
- Stanford University (US)
- Corresponding author
- Malenka, Robert C.
- Venue
- Nature
- Published
- 2012-10-14
- Volume
- 491
- Issue
- 7423
- Pages
- 212-217
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC3493743
- OpenAlex
- W2140986639
- Cited by
- 1,300
- References
- 43
- Citations by year
- 2026: 55 · 2025: 69 · 2024: 78 · 2023: 73 · 2022: 84 · 2021: 101 · 2020: 91 · 2019: 105 · 2018: 118 · 2017: 105 · 2016: 113 · 2015: 101 · 2014: 115 · 2013: 82 · 2012: 6
- FWCI
- 40.06
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- PMC
- Funders
- National Institute of Mental Health (P50MH086403)
- National Institute of Diabetes and Digestive and Kidney Diseases (DP2DK102256)
- National Institute of Neurological Disorders and Stroke (NS069375, P30NS069375)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Keywords
- ventral tegmental area, dopaminergic neurons, reward, aversion, laterodorsal tegmentum, lateral habenula, synaptic connectivity, medial prefrontal cortex, rostromedial tegmental nucleus, GABAergic neurons
- MeSH terms
- Animals, Avoidance Learning, Axons, Dopamine, Male, Mice, Inbred C57BL, Models, Neurological, Neural Pathways, Receptors, Dopamine, Reward, Synapses, Ventral Tegmental Area, Dopamine Antagonists, Habenula, Mice, Dopaminergic Neurons, GABAergic Neurons
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