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Input-specific control of reward and aversion in the ventral tegmental area

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Lammel, Stephan, Lim, Byung Kook, Ran, Chen, Huang, Kee Wui, Betley, Michael J., Tye, Kay M., Deisseroth, Karl, Malenka, Robert C.·2012·Nature

DOI 10.1038/nature11527PMC PMC3493743

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Abstract

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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Cui, J., Qian, J., Wang, J., & Shi, L. (2025) · Neurobiology of Disease · doi:10.1016/j.nbd.2025.107049 · Cited by 6
Awe is characterized as an ambivalent affect in the human behavior and cortex
Lee, J., Han, D. D., Oh, S.-Y., & Cha, J. (2025) · Communications Psychology · doi:10.1038/s44271-025-00299-2 · Cited by 5
Biological substrates of structure-function coupling in brain networks
Fotiadis, P., Arnsten, A. F. T., Parkes, L., Satterthwaite, T. D., Shinohara, R. T., & Bassett, D. S. (2026) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2026.106581 · Cited by 5
Early-life Stress Modifies the Reactivity of Neurons in the Ventral Tegmental Area and Lateral Hypothalamus to Acute Stress in Female Rats
Guguła, A., Trenk, A., Celary, A., Cizio, K., Tylko, G., Błasiak, A., & Hess, G. (2022) · Neuroscience · doi:10.1016/j.neuroscience.2022.02.017 · Cited by 5
Recruitment of inhibitory neuronal pathways regulating dopaminergic activity for the control of cocaine seeking
Wilczkowski, M., Karwowska, K., Kiełbiński, M., Zajda, K., Pradel, K., Drwiȩga, G., Rajfur, Z., Błasiak, T., Przewłocki, R., & Solecki, W. (2022) · European Journal of Neuroscience · doi:10.1111/ejn.15885 · Cited by 5
A novel small molecule, AS1, reverses the negative hedonic valence of noxious stimuli
Esancy, K., Conceicao, L. L., Curtright, A., Tran, T., Condon, L. F., Lecamp, B., & Dhaka, A. (2023) · BMC Biology · doi:10.1186/s12915-023-01573-7 · Cited by 5
Exploring the link between functional connectivity of ventral tegmental area and physical fitness in schizophrenia and healthy controls
Hamzehpour, L., Bohn, T., Jaspers, L., & Grimm, O. (2023) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2023.07.009 · Cited by 5
Interactions of sex and stress in modulation of ventral tegmental area dopaminergic activity
Price, K. M., & Polter, A. M. (2024) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2024.101477 · Cited by 5
Effect of electrolytic lesions of the dorsal diencephalic conduction system on the distribution of Fos-like immunoreactivity induced by rewarding electrical stimulation
Fakhoury, M., Voyer, D., Lévesque, D., & Rompré, P.-P. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.08.002 · Cited by 5
Enhanced psychostimulant response, but not social avoidance, depends on GluA1 AMPA receptors in VTA dopamine neurons following intermittent social defeat stress in rats
Rudolph, M. L., Neve, R. L., Hammer, R. P., & Nikulina, E. M. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.14884 · Cited by 5
Neuropeptide Y modifies a part of diencephalic catecholamine but not indolamine metabolism in chicks depending on feeding status
Tran, P. V., Tamura, Y., Pham, C. V., Elhussiny, M. Z., Han, G., Chowdhury, V. S., & Furuse, M. (2021) · Neuropeptides · doi:10.1016/j.npep.2021.102169 · Cited by 5
Habenula bibliometrics: Thematic development and research fronts of a resurgent field
Chen, S., Sun, X., Zhang, Y., Mu, Y., & Su, D. (2022) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2022.949162 · Cited by 5
Nicotinic Acetylcholine Receptors in the Ventral Tegmental Area are Important Targets for Nicotine and Ethanol Co-dependence
Taylor, D. H. (2013) · Biochemistry & Pharmacology Open Access · doi:10.4172/2167-0501.s1-002 · Cited by 5
Ventral Tegmental Area Microinjected-SKF38393 Increases Regular Chow Intake in 18 Hours Food-Deprived Rats
Rad, F. S., Haghparast, A., & Eliassi, A. (2020) · Basic and Clinical Neuroscience Journal · doi:10.32598/bcn.11.6.2226.1 · Cited by 5
An ongoing saga of nicotine complexity and dopamine heterogeneity: Nicotine activation and inhibition mediating reward and anxiety
Addy, N. (2021) · Neuron · doi:10.1016/j.neuron.2021.07.016 · Cited by 5
Fos response of the tail of the ventral tegmental area to food restriction entails a prediction error processing
Sánchez-Catalán, M. J., & Barrot, M. (2022) · Behavioural Brain Research · doi:10.1016/j.bbr.2022.113826 · Cited by 5
Involvement of GABAA receptors of lateral habenula in the acquisition and expression phases of morphine-induced place preference in male rats
Amohashemi, E., Reisi, P., & Alaei, H. (2022) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000695 · Cited by 5
Training recurrent neural networks with sparse, delayed rewards for flexible decision tasksPreprint
Miconi, T. (2015) · arXiv (Cornell University) · doi:10.48550/arxiv.1507.08973 · Cited by 5
Influence of Population Densities of Heterodera schachtii on Sugar Beets Grown in Microplots.
Olthof, T. H. A. (1978) · PubMed · Cited by 5
Firing patterns of serotonin neurons underlying cognitive flexibilityPreprint
Matias, S., Lottem, E., Dugué, G. P., & Mainen, Z. F. (2016) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/059758 · Cited by 5
Context-dependent multiplexing by individual VTA dopamine neuronsPreprint
Kremer, Y., Flakowski, J., Rohner, C., & Lüscher, C. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/408062 · Cited by 5
Mu Opioid Receptor mRNA and Protein Localization Across the Rat and Mouse Habenula
Popat, A., Simon, R. C., Aoyama, B. B., Wokhlu, A., Ehrlich, A. T., Harwell, C. C., & Margolis, E. B. (2026) · The Journal of Comparative Neurology · doi:10.1002/cne.70175 · Cited by 4
Social stress and affiliative touch: A tale of two affective states
Papantoniou, L. P., Vityk, O., & Tzanoulinou, S. (2026) · iScience · doi:10.1016/j.isci.2026.114833 · Cited by 4

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.
ORCID: Lammel, Stephan
Lim, Byung Kook
Huang, Kee Wui
Tye, Kay M.
Deisseroth, Karl
Malenka, Robert C.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2012-10-14
Volume: 491
Issue: 7423
Pages: 212-217
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature11527
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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Input-specific control of reward and aversion in the ventral tegmental area

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