Similar roles of substantia nigra and ventral tegmental dopamine neurons in reward and aversion
Open accessAbstract
Dopamine neurons in the ventral tegmental area (VTA) are implicated in affective functions. However, it is unclear to what extent dopamine neurons in substantia nigra pars compacta (SNc) play such roles. TH-Cre transgenic mice received adeno-associated viral vectors encoding channelrhodopsin2 (ChR2), halorhodopsin (NpHR), or control vector into the VTA or SNc, resulting in selective expression of these opsins in dopamine neurons. Mice with ChR2 learned instrumental responding to deliver photostimulation into the VTA or SNc and also sought for the compartment where they received photostimulation (i.e., operant place preference). Operant place preference scores were highly correlated with self-stimulation responses. In contrast, mice with NpHR avoided the compartment where they received photostimulation into the VTA, SNc, or dorsal striatum, whereas control mice did not. These observations suggest that the excitation and inhibition of SNc dopamine neurons elicit positive and negative affective effects, respectively, similar to those of VTA dopamine neurons.
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VTA-DA neurons play a central role in modulating the pleasurable and aversive aspects of social interactions.
“Dopaminergic neurons, arising from both the ventral tegmental area (VTA) and substantia nigra (SN), have attracted significant scientific interest regarding social behaviour, particularly VTA-DA neurons, owing to their central role in modulating the pleasurable and aversive aspects of social interactions (Gunaydin et al., 2014; Ilango et al., 2014; Merrer et al., 2024; Soli ´ e et al., 2022).”
From Convergence of oxytocin and dopamine signalling in neuronal circuits: Insights into the neurobiology of social interactions across species (2024) · cites this paper as Ilango et al., 2014
The Introduction and Discussion (pp. 817–822) support a role for VTA dopamine neurons in reward and aversion. They do not establish that these neurons modulate the pleasurable and aversive aspects of social interactions; the Discussion mentions social stress only in connection with a reported effect on later depression-like behavior. (LLM, conf=0.88)
Experimental — accuracy not yet measuredSNc-DA neurons play a pivotal role in motor function, goal-directed behaviour and reward.
“SNc-DA neurons play a pivotal role in motor function, goal-directed behaviour and reward (Ilango et al., 2014; Kim et al., 2015).”
From Convergence of oxytocin and dopamine signalling in neuronal circuits: Insights into the neurobiology of social interactions across species (2024) · cites this paper as Ilango et al., 2014
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Cites
A guided tour into subcellular colocalization analysis in light microscopy
Bolte, S., & Cordelières, F. (2006) · Journal of Microscopy · doi:10.1111/j.1365-2818.2006.01706.x · Cited by 5,238 · see citing works
Drugs of abuse: anatomy, pharmacology and function of reward pathways
Koob, G. F. (1992) · Trends in Pharmacological Sciences · doi:10.1016/0165-6147(92)90060-j · Cited by 2,070 · see citing works
Non-motor symptoms of Parkinson's disease: dopaminergic pathophysiology and treatment
Chaudhuri, К. R., & Schapira, A. H. V. (2009) · The Lancet Neurology · doi:10.1016/s1474-4422(09)70068-7 · Cited by 1,739 · see citing works
The primate basal ganglia: Parallel and integrative networks
Haber, S. N. (2003) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2003.10.003 · Cited by 1,479 · see citing works
Ikemoto, S. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.05.004 · Cited by 1,477 · see citing works
Input-specific control of reward and aversion in the ventral tegmental area
Lammel, S., Lim, B. K., Ran, C., Huang, K. W., Betley, M. J., Tye, K. M., Deisseroth, K., & Malenka, R. C. (2012) · Nature · doi:10.1038/nature11527 · Cited by 1,300 · 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
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 1,221 · see citing works
Neurobehavioural mechanisms of reward and motivation
Robbins, T. W., & Everitt, B. J. (1996) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(96)80077-8 · Cited by 1,187 · see citing works
Fallon, J. H., & Moore, R. Y. (1978) · The Journal of Comparative Neurology · doi:10.1002/cne.901800310 · Cited by 1,172 · see citing works
Cocaine cues and dopamine in dorsal striatum: mechanism of craving in cocaine addiction
Volkow, N. D., Wang, G.-J., Telang, F., Fowler, J. S., Logan, J., Childress, A.-R., Jayne, M., Ma, Y., & Wong, C. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.1544-06.2006 · Cited by 1,164 · see citing works
Rapid regulation of depression-related behaviours by control of midbrain dopamine neurons
Chaudhury, D., Walsh, J. J., Friedman, A. K., Juarez, B., Ku, S. M., Koo, J. W., Ferguson, D., Tsai, H.-C., Pomeranz, L., Christoffel, D. J., et al. (2013) · Nature · doi:10.1038/nature11713 · Cited by 1,156 · see citing works
Dopamine neurons modulate neural encoding and expression of depression-related behaviour
Tye, K. M., Mirzabekov, J. J., Warden, M. R., Ferenczi, E. A., Tsai, H.-C., Finkelstein, J., Kim, S.-Y., Adhikari, A., Thompson, K. R., Andalman, A. S., et al. (2013) · Nature · doi:10.1038/nature11740 · Cited by 1,073 · see citing works
Distinct roles for direct and indirect pathway striatal neurons in reinforcement
Kravitz, A. V., Tye, L. D., & Kreitzer, A. C. (2012) · Nature Neuroscience · doi:10.1038/nn.3100 · Cited by 972 · see citing works
Witten, I. B., Steinberg, E. E., Lee, S. Y., Davidson, T. J., Zalocusky, K. A., Brodsky, M., Yizhar, O., Cho, S. L., Gong, S., Ramakrishnan, C., et al. (2011) · Neuron · doi:10.1016/j.neuron.2011.10.028 · Cited by 680 · see citing works
GABA 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
Activation of lateral habenula inputs to the ventral midbrain promotes behavioral avoidance
Stamatakis, A. M., & Stuber, G. D. (2012) · Nature Neuroscience · doi:10.1038/nn.3145 · Cited by 564 · see citing works
Roles for nigrostriatal—not just mesocorticolimbic—dopamine in reward and addiction
Wise, R. A. (2009) · Trends in Neurosciences · doi:10.1016/j.tins.2009.06.004 · Cited by 500 · see citing works
Construction of implantable optical fibers for long-term optogenetic manipulation of neural circuits
Sparta, D. R., Stamatakis, A. M., Phillips, J. L., Hovelsø, N., van Zessen, R., & Stuber, G. D. (2012) · Nature Protocols · doi:10.1038/nprot.2011.413 · Cited by 394 · see citing works
Adamantidis, A. R., Tsai, H.-C., Boutrel, B., Zhang, F., Stuber, G. D., Budygin, E. A., Tourino, C., Bonci, A., Deisseroth, K., & de Lecea, L. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.2246-11.2011 · Cited by 357 · see citing works
Increased Occupancy of Dopamine Receptors in Human Striatum during Cue-Elicited Cocaine Craving
Wong, D. F., Kuwabara, H., Schretlen, D. J., Bonson, K. R., Zhou, Y., Nandi, A., Brašić, J. R., Kimes, A. S., Maris, M. A., Kumar, A., et al. (2006) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301194 · Cited by 311 · see citing works
Drui, G., Carnicella, S., Carcenac, C., Favier, M., Bertrand, A., Boulet, S., & Savasta, M. (2013) · Molecular Psychiatry · doi:10.1038/mp.2013.3 · Cited by 211 · see citing works
Transgenic expression of Cre recombinase from the tyrosine hydroxylase locus
Lindeberg, J., Usoskin, D., Bengtsson, H., Gustafsson, A., Kylberg, A., Söderström, S., & Ebendal, T. (2004) · genesis · doi:10.1002/gene.20065 · Cited by 211 · see citing works
Reward, Motivation, Cognition: Psychobiology of Mesotelencephalic Dopamine Systems
Fibiger, H. C., & Phillips, A. G. (1986) · Comprehensive physiology · doi:10.1002/cphy.cp010412 · Cited by 204 · see citing works
Jhou, T. C., Good, C. H., Rowley, C. S., Xu, S., Wang, H., Burnham, N. W., Hoffman, A. F., Lupica, C. R., & Ikemoto, S. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.3634-12.2013 · Cited by 198 · see citing works
Kim, K. M., Baratta, M. V., Yang, A., Lee, D., Boyden, E. S., & Fiorillo, C. D. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033612 · Cited by 144 · see citing works
Operant self-stimulation of dopamine neurons in the substantia nigra
Rossi, M. A., Sukharnikova, T., Hayrapetyan, V. Y., Yang, L., & Yin, H. H. (2013) · PLoS ONE · doi:10.1371/journal.pone.0065799 · Cited by 119 · see citing works
Neuroanatomical substrates mediating the aversive effects of D-1 dopamine receptor antagonists
Shippenberg, T. S., Bals-Kubik, R., Huber, A., & Herz, A. (1991) · Psychopharmacology · doi:10.1007/bf02244205 · Cited by 74 · see citing works
Dual Role of Medial A10 Dopamine Neurons in Affective Encoding
Liu, Z., Shin, R. S., & Ikemoto, S. (2008) · Neuropsychopharmacology · doi:10.1038/npp.2008.4 · Cited by 73 · see citing works
Operant place conditioning measures examined using two nondrug reinforcers
Crowder, W. F., & Hutto, C. W. (1992) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(92)90233-6 · Cited by 67 · see citing works
Shin, R. S., Cao, J., Webb, S. M., & Ikemoto, S. (2010) · PLoS ONE · doi:10.1371/journal.pone.0008741 · Cited by 35 · see citing works
Horiuchi, N. (2012) · Nature Photonics · doi:10.1038/nphoton.2012.356 · Cited by 34 · see citing works
Keller, K. L., Vollrath-Smith, F. R., Jafari, M., & Ikemoto, S. (2013) · Psychopharmacology · doi:10.1007/s00213-013-3300-9 · Cited by 14 · see citing works
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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
Ventral tegmental area: cellular heterogeneity, connectivity and behaviour
Morales, M., & Margolis, E. B. (2017) · Nature reviews. Neuroscience · doi:10.1038/nrn.2016.165 · Cited by 1,108 · see citing works
Dopamine reward prediction-error signalling: A two-component response
Schultz, W. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2015.26 · Cited by 1,036 · see citing works
Motivation and cognitive control: from behavior to neural mechanism
Botvinick, M., & Braver, T. (2015) · Annual Review of Psychology · doi:10.1146/annurev-psych-010814-015044 · Cited by 909 · see citing works
Intact-brain analyses reveal distinct information carried by SNc dopamine subcircuits
Lerner, T. N., Shilyansky, C., Davidson, T. J., Evans, K. E., Beier, K. T., Zalocusky, K. A., Crow, A. K., Malenka, R. C., Luo, L., Tomer, R., et al. (2015) · Cell · doi:10.1016/j.cell.2015.07.014 · Cited by 794 · see citing works
“In fact, SNc DA neurons could in principle even be similar to VTA DA neurons in terms of the valence of information represented because mice will self-stimulate for SNc DA neuron activity just as for VTA DA neuron activity (Ilango et al., 2014; Rossi et al., 2013).”
BackgroundCerebellar modulation of the reward circuitry and social behavior
Carta, I., Chen, C. H., Schott, A. L., Dorizan, S., & Khodakhah, K. (2019) · Science · doi:10.1126/science.aav0581 · Cited by 601 · see citing works
Striatal circuits for reward learning and decision-making
Cox, J., & Witten, I. B. (2019) · Nature reviews. Neuroscience · doi:10.1038/s41583-019-0189-2 · Cited by 554 · see citing works
Apathy in Parkinson's disease: clinical features, neural substrates, diagnosis, and treatment
Pagonabarraga, J., Kulisevsky, J., Strafella, A. P., & Krack, P. (2015) · The Lancet Neurology · doi:10.1016/s1474-4422(15)00019-8 · Cited by 556 · see citing works
Wise, R. A., & Robble, M. A. (2020) · Annual Review of Psychology · doi:10.1146/annurev-psych-010418-103337 · Cited by 418 · see citing works
Overlapping Brain Circuits for Homeostatic and Hedonic Feeding
Rossi, M. A., & Stuber, G. D. (2018) · Cell Metabolism · doi:10.1016/j.cmet.2017.09.021 · Cited by 415 · see citing works
Dopamine neurons projecting to the posterior striatum reinforce avoidance of threatening stimuli
Menegas, W., Akiti, K., Amo, R., Uchida, N., & Watabe‐Uchida, M. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0222-1 · Cited by 384 · see citing works
Dopamine Prediction Errors in Reward Learning and Addiction: From Theory to Neural Circuitry
Keiflin, R., & Janak, P. H. (2015) · Neuron · doi:10.1016/j.neuron.2015.08.037 · Cited by 370 · see citing works
Dopamine neurons create Pavlovian conditioned stimuli with circuit-defined motivational properties
Saunders, B. T., Richard, J. M., Margolis, E. B., & Janak, P. H. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0191-4 · Cited by 365 · see citing works
Diversity of Transgenic Mouse Models for Selective Targeting of Midbrain Dopamine Neurons
Lammel, S., Steinberg, E. E., Földy, C., Wall, N. R., Beier, K. T., Luo, L., & Malenka, R. C. (2015) · Neuron · doi:10.1016/j.neuron.2014.12.036 · Cited by 345 · see citing works
Reward and choice encoding in terminals of midbrain dopamine neurons depends on striatal target
Parker, N. F., Cameron, C. M., Taliaferro, J. P., Lee, J., Choi, J. Y., Davidson, T. J., Daw, N. D., & Witten, I. B. (2016) · Nature Neuroscience · doi:10.1038/nn.4287 · Cited by 340 · see citing works
Sufficiency of Mesolimbic Dopamine Neuron Stimulation for the Progression to Addiction
Pascoli, V., Terrier, J. E., Hiver, A., & Lüscher, C. (2015) · Neuron · doi:10.1016/j.neuron.2015.10.017 · Cited by 291 · see citing works
Dopamine transients are sufficient and necessary for acquisition of model-based associations
Sharpe, M. J., Chang, C. Y., Liu, M. A., Batchelor, H. M., Mueller, L. E., Jones, J. L., Niv, Y., & Schoenbaum, G. M. (2017) · Nature Neuroscience · doi:10.1038/nn.4538 · Cited by 284 · see citing works
Hu, H. (2016) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-070815-014106 · Cited by 253 · 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
Reward deficiency and anti-reward in pain chronification
Borsook, D., Linnman, C., Faria, V., Strassman, A. M., Becerra, L. R., & Elman, I. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.05.033 · Cited by 227 · see citing works
Basal ganglia circuit loops, dopamine and motivation: a review and enquiry
Ikemoto, S., Yang, C., & Tan, A. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.04.018 · Cited by 226 · see citing works
“Moreover, as discussed above, inhibition of DA release in the DStr with an optogenetic procedure induces aversion [16], and stimulation of DStr neurons are rewarding [87–89].”
InfluentialStructural foundations of optogenetics: Determinants of channelrhodopsin ion selectivity
Berndt, A., Lee, S. Y., Wietek, J., Ramakrishnan, C., Steinberg, E. E., Rashid, A. J., Kim, H., Park, S., Santoro, A., Frankland, P. W., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1523341113 · Cited by 214 · see citing works
Brief optogenetic inhibition of dopamine neurons mimics endogenous negative reward prediction errors
Chang, C. Y., Esber, G. R., Marrero-Garcia, Y., Yau, H., Bonci, A., & Schoenbaum, G. M. (2015) · Nature Neuroscience · doi:10.1038/nn.4191 · Cited by 211 · see citing works
Puig, M. V., Rose, J., Schmidt, R., & Freund, N. (2014) · Frontiers in Neural Circuits · doi:10.3389/fncir.2014.00093 · Cited by 182 · see citing works
Dopamine, Updated: Reward Prediction Error and Beyond
Lerner, T. N., Holloway, A. L., & Seiler, J. L. (2020) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2020.10.012 · Cited by 178 · see citing works
Schultz, W., Stauffer, W. R., & Lak, A. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.03.013 · Cited by 164 · see citing works
Generating bursts (and pauses) in the dopamine midbrain neurons
Paladini, C. A., & Roeper, J. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.07.032 · Cited by 158 · see citing works
Cell-type-specific asynchronous modulation of PKA by dopamine in learning
Lee, S. J., Lodder, B., Chen, Y., Patriarchi, T., Tian, L., & Sabatini, B. L. (2021) · Nature · doi:10.1038/s41586-020-03050-5 · Cited by 160 · see citing works
Behavioral and neurobiological mechanisms of punishment: implications for psychiatric disorders
Jean-Richard-Dit-Bressel, P., Killcross, S., & McNally, G. P. (2018) · Neuropsychopharmacology · doi:10.1038/s41386-018-0047-3 · Cited by 160 · see citing works
Learning from Action: Reconsidering Movement Signaling in Midbrain Dopamine Neuron Activity
Coddington, L. T., & Dudman, J. T. (2019) · Neuron · doi:10.1016/j.neuron.2019.08.036 · Cited by 150 · see citing works
Mechanisms of Action and Persistent Neuroplasticity by Drugs of Abuse
Korpi, E. R., den Hollander, B., Farooq, U., Vashchinkina, E., Rajkumar, R., Nutt, D. J., Hyytiä, P., & Dawe, G. S. (2015) · Pharmacological Reviews · doi:10.1124/pr.115.010967 · Cited by 148 · see citing works
What Is the Relationship between Dopamine and Effort?
Walton, M. E., & Bouret, S. (2018) · Trends in Neurosciences · doi:10.1016/j.tins.2018.10.001 · Cited by 150 · see citing works
Nesfatin-1: functions and physiology of a novel regulatory peptide
Dore, R., Levata, L., Lehnert, H., & Schulz, C. (2016) · Journal of Endocrinology · doi:10.1530/joe-16-0361 · Cited by 146 · see citing works
Ventral Tegmental Dopamine Neurons Participate in Reward Identity Predictions
Keiflin, R., Pribut, H. J., Shah, N. B., & Janak, P. H. (2018) · Current Biology · doi:10.1016/j.cub.2018.11.050 · Cited by 142 · see citing works
Prefrontal dopamine in associative learning and memory
Puig, M. V., Antzoulatos, E. G., & Miller, E. K. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.09.026 · Cited by 138 · see citing works
Architectural Representation of Valence in the Limbic System
Namburi, P., Al‐Hasani, R., Calhoon, G. G., Bruchas, M. R., & Tye, K. M. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.358 · Cited by 133 · see citing works
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 · see citing works
Dopamine, behavior, and addiction
Wise, R. A., & Jordan, C. J. (2021) · Journal of Biomedical Science · doi:10.1186/s12929-021-00779-7 · Cited by 138 · see citing works
GURNEY, K. N., Humphries, M. D., & Redgrave, P. (2015) · PLoS Biology · doi:10.1371/journal.pbio.1002034 · Cited by 123 · see citing works
Rewarding Effects of Optical Stimulation of Ventral Tegmental Area Glutamatergic Neurons
Wang, H., Qi, J., Zhang, S. S., Wang, H., & Morales, M. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.3428-15.2015 · Cited by 119 · see citing works
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 118 · see citing works
Midbrain dopamine neurons signal aversion in a reward-context-dependent manner
Matsumoto, H., Tian, J., Uchida, N., & Watabe‐Uchida, M. (2016) · eLife · doi:10.7554/elife.17328 · Cited by 109 · see citing works
Wenzel, J. M., Oleson, E. B., Gove, W. N., Cole, A. B., Gyawali, U., Dantrassy, H. M., Bluett, R. J., Dryanovski, D. I., Stuber, G. D., Deisseroth, K. A., et al. (2018) · Current Biology · doi:10.1016/j.cub.2018.03.037 · Cited by 103 · see citing works
Dopamine and Acetylcholine, a Circuit Point of View in Parkinson’s Disease
Rizzi, G., & Tan, K. R. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00110 · Cited by 101 · see citing works
Tsutsui‐Kimura, I., Matsumoto, H., Akiti, K., Yamada, M. M., Uchida, N., & Watabe‐Uchida, M. (2020) · eLife · doi:10.7554/elife.62390 · Cited by 91 · see citing works
Dissecting the Role of GABA Neurons in the VTA versus SNr in Opioid Reward
Galaj, E., Han, X., Shen, H., Jordan, C. J., He, Y., Humburg, B. A., Bi, G., & Xi, Z. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.0988-20.2020 · Cited by 97 · see citing works
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 87 · see citing works
Han, X., Jing, M.-Y., Zhao, T.-Y., Wu, N., Song, R., & Li, J. (2017) · Metabolic Brain Disease · doi:10.1007/s11011-017-0023-3 · Cited by 93 · see citing works
Salehpour, F., Gholipour-Khalili, S., Farajdokht, F., Kamari, F., Walski, T., Hamblin, M. R., DiDuro, J. O., & Cassano, P. (2019) · Reviews in the Neurosciences · doi:10.1515/revneuro-2019-0063 · Cited by 116 · see citing works
Temporally restricted dopaminergic control of reward-conditioned movements
Lee, K., Claar, L. D., Hachisuka, A., Bakhurin, K. I., Nguyen, J., Trott, J. M., Gill, J. L., & Masmanidis, S. C. (2020) · Nature Neuroscience · doi:10.1038/s41593-019-0567-0 · Cited by 77 · see citing works
Satiation state-dependent dopaminergic control of foraging in Drosophila
Landayan, D., Feldman, D. S., & Wolf, F. W. (2018) · Scientific Reports · doi:10.1038/s41598-018-24217-1 · Cited by 77 · see citing works
Flores-Dourojeanni, J. P., van Rijt, C., van den Munkhof, M. H., Boekhoudt, L., Luijendijk, M. C. M., Vanderschuren, L. J. M. J., & Adan, R. A. H. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.0477-20.2020 · Cited by 78 · see citing works
Associative and sensorimotor cortico‐basal ganglia circuit roles in effects of abused drugs
Gremel, C. M., & Lovinger, D. M. (2016) · Genes Brain & Behavior · doi:10.1111/gbb.12309 · Cited by 72 · see citing works
Neurochemical and behavioural indices of exercise reward are independent of exercise controllability
Herrera, J. J., Fedynska, S., Ghasem, P. R., Wieman, T., Clark, P., Gray, N. A., Loetz, E. C., Campeau, S., Fleshner, M., & Greenwood, B. N. (2016) · European Journal of Neuroscience · doi:10.1111/ejn.13193 · Cited by 75 · see citing works
Magnard, R., Vachez, Y. M., Carcenac, C., Krack, P., Olivier David, A., Savasta, M., Boulet, S., & Carnicella, S. (2016) · Translational Psychiatry · doi:10.1038/tp.2016.17 · Cited by 75 · see citing works
Arrigoni, E., & Saper, C. B. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.07.016 · Cited by 71 · see citing works
Fritz, M., Klawonn, A. M., Nilsson, A., Singh, A. K., Zajdel, J., Wilhelms, D., Lazarus, M., Löfberg, A., Jaarola, M., Kugelberg, U. Ö., et al. (2015) · Journal of Clinical Investigation · doi:10.1172/jci83844 · Cited by 72 · see citing works
Pristerà, A., Lin, W., Kaufmann, A.-K., Brimblecombe, K. R., Threlfell, S., Dodson, P. D., Magill, P. J., Fernandes, C., Cragg, S. J., & Ang, S. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1503911112 · Cited by 71 · see citing works
van Elzelingen, W., Warnaar, P., de Matos, J. M. S., Bastet, W., Jonkman, R., Smulders, D., Goedhoop, J. N., Denys, D. A. J. P., Arbab, T., & Willuhn, I. (2022) · Current Biology · doi:10.1016/j.cub.2021.12.027 · Cited by 63 · see citing works
On the Modulatory Roles of Neuregulins/ErbB Signaling on Synaptic Plasticity
Ledonne, A., & Mercuri, N. B. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms21010275 · Cited by 69 · see citing works
Ventral pallidal modulation of aversion processing
Wulff, A. B., Tooley, J. R., Marconi, L. J., & Creed, M. C. (2018) · Brain Research · doi:10.1016/j.brainres.2018.10.010 · Cited by 67 · see citing works
The substantia nigra and ventral tegmental dopaminergic neurons from development to degeneration
Fu, Y., Paxinos, G., WATSON, C. R. R., & Halliday, G. M. (2016) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2016.02.001 · Cited by 66 · see citing works
Components and characteristics of the dopamine reward utility signal
Stauffer, W. R., Lak, A., Kobayashi, S., & Schultz, W. (2015) · The Journal of Comparative Neurology · doi:10.1002/cne.23880 · Cited by 62 · see citing works
Ventral Tegmental Area Afferents and Drug-Dependent Behaviors
Oliva, I., & Wanat, M. J. (2016) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2016.00030 · Cited by 62 · see citing works
Clock Speed as a Window into Dopaminergic Control of Emotion and Time Perception
Cheng, R., Tipples, J., Narayanan, N. S., & Meck, W. H. (2016) · Timing & Time Perception · doi:10.1163/22134468-00002064 · Cited by 62 · see citing works
Lee, J., Finkelstein, J., Choi, J. Y., & Witten, I. B. (2016) · Neuron · doi:10.1016/j.neuron.2016.05.001 · Cited by 58 · see citing works
Activation of Pedunculopontine Glutamate Neurons Is Reinforcing
Yoo, J. H., Zell, V., Wu, J., Punta, C., Ramajayam, N., Shen, X., Faget, L. C., Lilascharoen, V., Lim, B. K., & Hnasko, T. S. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.3082-16.2016 · Cited by 59 · see citing works
Toward sophisticated basal ganglia neuromodulation: Review on basal ganglia deep brain stimulation
Cunha, C. D., Boschen, S. L., Gómez‐A, A., Ross, E. K., Gibson, W. S. J., Min, H.-K. P., Lee, K. H., & Blaha, C. D. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.02.003 · Cited by 58 · see citing works
Seeking motivation and reward: Roles of dopamine, hippocampus, and supramammillo-septal pathway
Kesner, A. J., Calva, C. B., & Ikemoto, S. (2022) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2022.102252 · Cited by 56 · see citing works
Curcumin improves neurofunctions of 6-OHDA-induced parkinsonian rats
Song, S., Nie, Q., Li, Z., & Du, G. (2015) · Pathology - Research and Practice · doi:10.1016/j.prp.2015.11.012 · Cited by 55 · see citing works
Dopamine-independent effect of rewards on choices through hidden-state inference
Blanco-Pozo, M., Akam, T. E., & Walton, M. E. (2024) · Nature Neuroscience · doi:10.1038/s41593-023-01542-x · Cited by 70 · see citing works
Ilango, A., Kesner, A. J., Broker, C. J., Wang, D. V., & Ikemoto, S. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00155 · Cited by 50 · see citing works
Gadziola, M. A., Stetzik, L. A., Wright, K. N., Milton, A. J., Arakawa, K., Cortijo, M. D. M., & Wesson, D. W. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107919 · Cited by 50 · see citing works
Cannabis use, abuse, and withdrawal: Cannabinergic mechanisms, clinical, and preclinical findings
Kesner, A. J., & Lovinger, D. (2021) · Journal of Neurochemistry · doi:10.1111/jnc.15369 · Cited by 41 · see citing works
Rappeneau, V., & Castillo Díaz, F. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105675 · Cited by 51 · see citing works
“…have attracted significant scientific interest regarding social behaviour, particularly VTA-DA neurons, owing to their central role in modulating the pleasurable and aversive aspects of social interactions (Gunaydin et al., 2014; Ilango et al., 2014; Merrer et al., 2024; Soli ´ e et al., 2022).”
BackgroundChen, Y., Hu, Y., Talishinsky, A., Potter, C. T., Calva, C. B., Ramsey, L. A., Kesner, A. J., Don, R. F., Junn, S., Tan, A., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-28892-7 · Cited by 50 · see citing works
Effects of alternating current stimulation on the healthy and diseased brain
Hamid, A. I. A., Gall, C., Speck, O., Antal, A., & Sabel, B. A. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00391 · Cited by 50 · see citing works
Takakuwa, N., Kato, R., Redgrave, P., & Isa, T. (2017) · eLife · doi:10.7554/elife.24459 · Cited by 47 · see citing works
Boekhoudt, L., Wijbrans, E. C., Man, J. H. K., Luijendijk, M. C. M., de Jong, J. W., Plasse, G., Vanderschuren, L. J. M. J., & Adan, R. A. H. (2017) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2017.11.005 · Cited by 49 · see citing works
Kesner, A. J., Shin, R. S., Calva, C. B., Don, R. F., Junn, S., Potter, C. T., Ramsey, L. A., Abouelnaga, A., Cover, C. G., Wang, D. V., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-23040-z · Cited by 48 · see citing works
Gadziola, M. A., & Wesson, D. W. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.3328-15.2016 · Cited by 47 · see citing works
Kuo, H., & Liu, F. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00422 · Cited by 46 · see citing works
Auerbach, R. P., Pagliaccio, D., & Kirshenbaum, J. S. (2022) · Current topics in behavioral neurosciences · doi:10.1007/7854_2022_358 · Cited by 47 · see citing works
Fischbach-Weiss, S., Reese, R. M., & Janak, P. H. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.12.003 · Cited by 44 · see citing works
Kuo, H., & Liu, F. (2022) · Biomedicines · doi:10.3390/biomedicines10030560 · Cited by 45 · see citing works
Cornejo, M. P., Mustafá, E. R., Barrile, F., Cassano, D., Francesco, P. N. D., Raingo, J., & Perelló, M. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.10.017 · Cited by 43 · see citing works
A dopamine mechanism for reward maximization
Schultz, W. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2316658121 · Cited by 44 · see citing works
Cre-driven optogenetics in the heterogeneous genetic panorama of the VTA
Pupe, S., & Wallén‐Mackenzie, Å. (2015) · Trends in Neurosciences · doi:10.1016/j.tins.2015.04.005 · Cited by 41 · see citing works
Yamaguchi, T., Goto, A., NAKAHARA, I., Yawata, S., Hikida, T., Matsuda, M., Funabiki, K., & Nakanishi, S. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1514731112 · Cited by 42 · see citing works
Wang, D. V., Viereckel, T., Zell, V., Konradsson‐Geuken, Å., Broker, C. J., Talishinsky, A., Yoo, J. H., Galinato, M. H., Arvidsson, E., Kesner, A. J., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.02.062 · Cited by 40 · see citing works
Contributions of nucleus accumbens dopamine to cognitive flexibility
Radke, A. K., Kocharian, A., Covey, D. P., Lovinger, D. M., Cheer, J. F., Mateo, Y., & Holmes, A. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.14152 · Cited by 42 · see citing works
Steidl, S., O’Sullivan, S., Pilat, D., Bubula, N., Brown, J., & Vezina, P. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.06.045 · Cited by 40 · see citing works
Drive and Reinforcement Circuitry in the Brain: Origins, Neurotransmitters, and Projection Fields
Wise, R. A., & McDevitt, R. A. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2017.228 · Cited by 40 · see citing works
Pagonabarraga, J., & Kulisevsky, J. (2017) · International review of neurobiology · doi:10.1016/bs.irn.2017.05.025 · Cited by 40 · see citing works
Neurochemicals, Behaviours and Psychiatric Perspectives of Neurological Diseases
Choudhury, A., Sahu, T., Ramanujam, P. L., Banerjee, A. K., Chakraborty, I., Arun Kumar, R., & Arora, N. (2018) · Neuropsychiatry · doi:10.4172/neuropsychiatry.1000361 · Cited by 41 · see citing works
Optogenetic excitation of LDTg axons in the VTA reinforces operant responding in rats
Steidl, S., & Veverka, K. K. (2015) · Brain Research · doi:10.1016/j.brainres.2015.04.021 · Cited by 39 · see citing works
Wei, J., Lambert, T. Y., Valada, A., Patel, N. C., Walker, K., Lenders, J., Schmidt, C. J., Iskhakova, M., Alazizi, A., Mair-Meijers, H. E., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-41455-8 · Cited by 38 · see citing works
Contemporary approaches to neural circuit manipulation and mapping: focus on reward and addiction
Saunders, B. T., Richard, J. M., & Janak, P. H. (2015) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2014.0210 · Cited by 38 · see citing works
Wei, L., Hu, X., Yuan, Y., Liu, W., & Chen, H. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.03.011 · Cited by 37 · see citing works
β2* nAChRs on VTA dopamine and GABA neurons separately mediate nicotine aversion and reward
Grieder, T. E., Besson, M., Maal‐Bared, G., Pons, S., Maskos, U., & van der Kooy, D. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1908724116 · Cited by 36 · see citing works
- Authors
- Ilango, A., Kesner, A. J., Keller, K. L., Stuber, G. D., Bonci, A., & Ikemoto, S.
- Affiliations
- University of North Carolina at Chapel Hill (US)
- National Institutes of Health (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2014-01-15
- Volume
- 34
- Issue
- 3
- Pages
- 817-822
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3891961
- OpenAlex
- W1964812893
- Cited by
- 255
- References
- 33
- Citations by year
- 2026: 2 · 2025: 18 · 2024: 14 · 2023: 16 · 2022: 14 · 2021: 23 · 2020: 20 · 2019: 24 · 2018: 28 · 2017: 20 · 2016: 28 · 2015: 33 · 2014: 15
- FWCI
- 14.62
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
- UNC Libraries
- Funders
- National Institutes of Health
- National Institute on Drug Abuse (R01DA032750)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- substantia nigra pars compacta, ventral tegmental area, dopaminergic neurons, reward, aversion, self-stimulation, photostimulation, halorhodopsin, emotional behavior, dorsal striatum
- MeSH terms
- Animals, Avoidance Learning, Conditioning, Operant, Male, Mice, Inbred C57BL, Reward, Substantia Nigra, Ventral Tegmental Area, Mice, Gene Knock-In Techniques, Dopaminergic Neurons
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