Reward and aversion in a heterogeneous midbrain dopamine system

Lammel, Stephan; Lim, Byung Kook; Malenka, Robert C.

doi:10.1016/j.neuropharm.2013.03.019

Cited by 804Neurotransmitter Receptor Influence on BehaviorNeuroscience and Neuropharmacology ResearchNeural and Behavioral Psychology Studies

Reward and aversion in a heterogeneous midbrain dopamine system

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Lammel, Stephan, Lim, Byung Kook, Malenka, Robert C.·2014·Neuropharmacology

DOI 10.1016/j.neuropharm.2013.03.019PMC PMC3778102

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Abstract

The ventral tegmental area (VTA) is a heterogeneous brain structure that serves a central role in motivation and reward processing. Abnormalities in the function of VTA dopamine (DA) neurons and the targets they influence are implicated in several prominent neuropsychiatric disorders including addiction and depression. Recent studies suggest that the midbrain DA system is composed of anatomically and functionally heterogeneous DA subpopulations with different axonal projections. These findings may explain a number of previously confusing observations that suggested a role for DA in processing both rewarding as well as aversive events. Here we will focus on recent advances in understanding the neural circuits mediating reward and aversion in the VTA and how stress as well as drugs of abuse, in particular cocaine, alter circuit function within a heterogeneous midbrain DA system. This article is part of a Special Issue entitled 'NIDA 40th Anniversary Issue'.

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Midbrain dopamine neurons constitute the mesocorticolimbic pathway critical for creating rewards and signaling aversive outcomes.
“Furthermore, midbrain DA neurons constitute the mesocorticolimbic pathway critical for creating rewards and signaling aversive outcomes (55, 56).”
From Emotional Blunting in Patients With Major Depressive Disorder: A Brief Non-systematic Review of Current Research (2021) · cites this paper as [56]
The Introduction and section 3 describe midbrain dopamine neurons as involved in reward signaling and responses to aversive events; section 4 also links particular VTA projections to reward and aversion-related behavior. But the Introduction describes a heterogeneous midbrain system that includes substantia nigra and VTA neurons, so the paper does not support identifying all midbrain dopamine neurons with the mesocorticolimbic pathway. Its account of reward-related signaling and reinforcement is also narrower than saying these neurons create rewards. (LLM, conf=0.81)
Experimental — accuracy not yet measured
Prefrontal cortex and hippocampus decode stimulus and environmental features to guide adaptive reward responses, while lateral hypothalamus-lateral habenula circuits encode negative valence; both are integrated in nucleus accumbens and ventral tegmental area to regulate dopamine.
“A grossly oversimplified overview of these circuits is that the prefrontal cortices and hippocampus are devoted to detecting and decoding specific features of stimuli and the environment, including the social environment, to guide decision-making and ensure adaptive, flexible, and predictive responses to rewarding stimuli, whereas the lateral hypothalamus-lateral habenula circuits predominantly En”
From Plasticity of synapses and reward circuit function in the genesis and treatment of depression (2023) · cites this paper as [52]

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Laterodorsal tegmental stimulation elicits dopamine efflux in the rat nucleus accumbens by activation of acetylcholine and glutamate receptors in the ventral tegmental area
Forster, G. L., & Blaha, C. D. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.00250.x · Cited by 271 · see citing works
Activation of dopamine neurons is critical for aversive conditioning and prevention of generalized anxiety
Zweifel, L. S., Fadok, J. P., Argilli, E., Garelick, M. G., Jones, G. L., Dickerson, T. M. K., Allen, J. M., Mizumori, S. J. Y., Bonci, A., & Palmiter, R. D. (2011) · Nature Neuroscience · doi:10.1038/nn.2808 · Cited by 256 · see citing works
Corticotropin‐releasing factor increases mouse ventral tegmental area dopamine neuron firing through a protein kinase C‐dependent enhancement ofIh
Wanat, M. J., Hopf, F. W., Stuber, G. D., Phillips, P. E. M., & Bonci, A. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2007.150078 · Cited by 256 · see citing works
Laterodorsal tegmental projections to identified cell populations in the rat ventral tegmental area
Omelchenko, N., & Sesack, S. R. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20417 · Cited by 252 · see citing works
Mechanism and Time Course of Cocaine-Induced Long-Term Potentiation in the Ventral Tegmental Area
Argilli, E., Sibley, D. R., Malenka, R. C., England, P. M., & Bonci, A. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1001-08.2008 · Cited by 243 · see citing works
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Glutamate Receptors on Dopamine Neurons Control the Persistence of Cocaine Seeking
Engblom, D., Bilbao, A., Sanchis‐Segura, C., Dahan, L., Perreau‐Lenz, S., Balland, B., Parkitna, J. M. R., Luján, R., Halbout, B., Mameli, M., et al. (2008) · Neuron · doi:10.1016/j.neuron.2008.07.010 · Cited by 241 · see citing works
Afferent modulation of dopamine neuron firing patterns
Kitai, S. T., Shepard, P. D., Callaway, J. C., & Scroggs, R. S. (1999) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(99)00040-9 · Cited by 234 · see citing works
Midbrain Dopamine Neurons: Projection Target Determines Action Potential Duration and Dopamine D 2 Receptor Inhibition
Margolis, E. B., Mitchell, J., Ishikawa, J., Hjelmstad, G. O., & Fields, H. L. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1526-08.2008 · Cited by 232 · see citing works
Preferential Enhancement of Dopamine Transmission within the Nucleus Accumbens Shell by Cocaine Is Attributable to a Direct Increase in Phasic Dopamine Release Events
Aragona, B. J., Cleaveland, N. A., Stuber, G. D., Day, J. J., Carelli, R. M., & Wightman, R. M. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.2225-08.2008 · Cited by 225 · see citing works
K-ATP channels in dopamine substantia nigra neurons control bursting and novelty-induced exploration
Schiemann, J. M., Schlaudraff, F., Klose, V., Bingmer, M., Seino, S., Magill, P. J., Zaghloul, K. A., Schneider, G., Liss, B., & Roeper, J. (2012) · Nature Neuroscience · doi:10.1038/nn.3185 · Cited by 215 · see citing works
Collateralization of monoamine neurons: mesotelencephalic dopamine projections to caudate, septum, and frontal cortex
Jh, F. (1981) · Journal of Neuroscience · doi:10.1523/jneurosci.01-12-01361.1981 · Cited by 206 · see citing works
Identification of Rat Ventral Tegmental Area GABAergic Neurons
Margolis, E. B., Toy, B. C., Himmels, P., Morales, M., & Fields, H. L. (2012) · PLoS ONE · doi:10.1371/journal.pone.0042365 · Cited by 202 · see citing works
An electrophysiological characterization of ventral tegmental area dopaminergic neurons during differential pavlovian fear conditioning in the awake rabbit
Guarraci, F. A., & Kapp, B. S. (1999) · Behavioural Brain Research · doi:10.1016/s0166-4328(98)00102-8 · Cited by 201 · see citing works
Calcium-permeable AMPA receptors in the VTA and nucleus accumbens after cocaine exposure: when, how, and why?
Wolf, M. E., & Tseng, K. Y. (2012) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2012.00072 · Cited by 199 · see citing works
Event timing turns punishment to reward
Tanimoto, H., Heisenberg, M., & Gerber, B. (2004) · Nature · doi:10.1038/430983a · Cited by 197 · see citing works
Ultrastructural analysis of local collaterals of rat ventral tegmental area neurons: GABA phenotype and synapses onto dopamine and GABA cells
Omelchenko, N., & Sesack, S. R. (2009) · Synapse · doi:10.1002/syn.20668 · Cited by 194 · see citing works
Restraint increases dopaminergic burst firing in awake rats
Anstrom, K. K., & Woodward, D. J. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300730 · Cited by 181 · see citing works
Cocaine inverts rules for synaptic plasticity of glutamate transmission in the ventral tegmental area
Mameli, M., Bellone, C., Brown, M. T. C., & Lüscher, C. (2011) · Nature Neuroscience · doi:10.1038/nn.2763 · Cited by 177 · see citing works
Effect of noxious tail pinch on the discharge rate of mesocortical and mesolimbic dopamine neurons: selective activation of the mesocortical system
Mantz, J., Thierry, A. M., & Glowinski, J. (1989) · Brain Research · doi:10.1016/0006-8993(89)91263-8 · Cited by 168 · see citing works
A subset of ventral tegmental area neurons is inhibited by dopamine, 5-hydroxytryptamine and opioids
Cameron, D., Wessendorf, M. W., & Williams, J. T. (1997) · Neuroscience · doi:10.1016/s0306-4522(96)00444-7 · Cited by 163 · see citing works
Dynamics of the dopaminergic system as a key component to the understanding of depression
Yadid, G., & Friedman, A. (2008) · Progress in brain research · doi:10.1016/s0079-6123(08)00913-8 · Cited by 160 · see citing works
Cocaine-induced potentiation of synaptic strength in dopamine neurons: Behavioral correlates in GluRA(–/–) mice
Dong, Y., Saal, D., Thomas, M., Faust, R., Bonci, A., Robinson, T., & Malenka, R. C. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0401553101 · Cited by 158 · see citing works
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Effects of stress and aversion on dopamine neurons: Implications for addiction
Ungless, M. A., Argilli, E., & Bonci, A. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.04.006 · Cited by 145 · see citing works
Structural correlates of heterogeneous in vivo activity of midbrain dopaminergic neurons
Henny, P., Brown, M. T. C., Northrop, A., Faunes, M., Ungless, M. A., Magill, P. J., & Bolam, J. P. (2012) · Nature Neuroscience · doi:10.1038/nn.3048 · Cited by 139 · see citing works
Brain Systems Underlying Susceptibility to Helplessness and Depression
Shumake, J., & Gonzalez-Lima, F. (2003) · Behavioral and Cognitive Neuroscience Reviews · doi:10.1177/1534582303259057 · Cited by 135 · see citing works
Organization of the ascending projections from the ventral tegmental area: A multiple fluorescent retrograde tracer study in the rat
Albanese, A., & Minciacchi, D. (1983) · The Journal of Comparative Neurology · doi:10.1002/cne.902160406 · Cited by 130 · see citing works
Heterogeneous composition of dopamine neurons of the rat A10 region: molecular evidence for diverse signaling properties
Li, X., Qi, J., Yamaguchi, T., Wang, H., & Morales, M. (2012) · Brain Structure and Function · doi:10.1007/s00429-012-0452-z · Cited by 129 · see citing works
Increased extracellular dopamine in nucleus accumbens in response to unconditioned and conditioned aversive stimuli: studies using 1 min microdialysis in rats
Young, A. M. J. (2004) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2004.03.003 · Cited by 123 · see citing works
Regional specificity in the real‐time development of phasic dopamine transmission patterns during acquisition of a cue–cocaine association in rats
Aragona, B. J., Day, J. J., Roitman, M. F., Cleaveland, N. A., Wightman, R. M., & Carelli, R. M. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.07027.x · Cited by 120 · see citing works
Long-lasting Modulation of Glutamatergic Transmission in VTA Dopamine Neurons after a Single Dose of Benzodiazepine Agonists
Panhelainen, A. E., Möykkynen, T. P., & Korpi, E. R. (2008) · Neuropsychopharmacology · doi:10.1038/npp.2008.89 · Cited by 108 · see citing works
Activity of Neurochemically Heterogeneous Dopaminergic Neurons in the Substantia Nigra during Spontaneous and Driven Changes in Brain State
Brown, M. T. C., Henny, P., Bolam, J. P., & Magill, P. J. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.4423-08.2009 · Cited by 106 · see citing works
Amphetamine Depresses Excitatory Synaptic Transmission via Serotonin Receptors in the Ventral Tegmental Area
Jones, S., & Kauer, J. A. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-22-09780.1999 · Cited by 102 · see citing works
In vitro identification and electrophysiological characterization of dopamine neurons in the ventral tegmental area
Zhang, T. A., Placzek, A. N., & Dani, J. A. (2010) · Neuropharmacology · doi:10.1016/j.neuropharm.2010.06.004 · Cited by 100 · see citing works
Dopamine neuron glutamate cotransmission: frequency-dependent modulation in the mesoventromedial projection
Chuhma, N., Choi, W., Mingote, S., & Rayport, S. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.08.057 · Cited by 83 · see citing works
Functional Diversity of Ventral Midbrain Dopamine and GABAergic Neurons
Korotkova, T. M., Ponomarenko, A. A., Brown, R. E., & Haas, H. L. (2004) · Molecular Neurobiology · doi:10.1385/mn:29:3:243 · Cited by 79 · see citing works
Increased phasic activity of VTA dopamine neurons in mice 3 weeks after repeated social defeat
Razzoli, M., Andreoli, M., Michielin, F., Quarta, D., & Sokal, D. M. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.11.050 · Cited by 76 · see citing works
VTA Dopamine Neuron Bursting is Altered in an Animal Model of Depression and Corrected by Desipramine
Friedman, A., Friedman, Y., Dremencov, E., & Yadid, G. (2008) · Journal of Molecular Neuroscience · doi:10.1007/s12031-007-9016-8 · Cited by 63 · see citing works
Effect of amphetamine on extrastriatal D2 dopamine receptor binding in the primate brain: A PET study
Chou, Y.-H., Halldin, C., & Farde, L. (2000) · Synapse · doi:10.1002/1098-2396(200011)38:2 · Cited by 57 · see citing works
Establishing causality for dopamine in neural function and behavior with optogenetics
Steinberg, E. E., & Janak, P. H. (2012) · Brain Research · doi:10.1016/j.brainres.2012.09.036 · Cited by 52 · see citing works
Medial Prefrontal Cortex Inversely Regulates Toluene-Induced Changes in Markers of Synaptic Plasticity of Mesolimbic Dopamine Neurons
Beckley, J. T., Evins, C. E., Fedarovich, H., Gilstrap, M. J., & Woodward, J. J. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.3729-12.2013 · Cited by 42 · see citing works
Species Differences in Somatodendritic Dopamine Transmission Determine D2-Autoreceptor-Mediated Inhibition of Ventral Tegmental Area Neuron Firing
Courtney, N. A., Mamaligas, A. A., & Ford, C. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.2745-12.2012 · Cited by 40 · see citing works
Dopaminergic axons in different divisions of the adult rat striatal complex do not express vesicular glutamate transporters
Moss, J., Ungless, M. A., & Bolam, J. P. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07594.x · Cited by 31 · see citing works
Cocaine must enter the brain to evoke unconditioned dopamine release within the nucleus accumbens shell
Porter‐Stransky, K. A., Wescott, S. A., Hershman, M., Badrinarayan, A., Weele, C. M. V., Lovic, V., & Aragona, B. J. (2011) · Neuroscience Letters · doi:10.1016/j.neulet.2011.08.028 · Cited by 11 · see citing works

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The brain on drugs: from reward to addiction
Volkow, N. D., & Morales, M. (2015) · Cell · doi:10.1016/j.cell.2015.07.046 · Cited by 1,306 · see citing works
The dopamine motive system: implications for drug and food addiction
Volkow, N. D., Wise, R. A., & Baler, R. (2017) · Nature Reviews Neuroscience · doi:10.1038/nrn.2017.130 · Cited by 939 · 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
“However, not all midbrain DA neurons appear to encode similar information in their activity patterns (Bromberg-Martin et al., 2010; Lammel et al., 2014; Roeper, 2013).”
Background
Gating of social reward by oxytocin in the ventral tegmental area
Hung, L. W., Neuner, S., Polepalli, J. S., Beier, K. T., Wright, M., Walsh, J. J., Lewis, E. M., Luo, L., Deisseroth, K., Dölen, G., et al. (2017) · Science · doi:10.1126/science.aan4994 · Cited by 578 · see citing works
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Coordinated and compartmentalized neuromodulation shapes sensory processing in Drosophila
Cohn, R., Morantte, I., & Ruta, V. (2015) · Cell · doi:10.1016/j.cell.2015.11.019 · Cited by 430 · see citing works
Mapping projections of molecularly defined dopamine neuron subtypes using intersectional genetic approaches
Poulin, J.-F., Caronia, G., Hofer, C., Cui, Q., Helm, B., Ramakrishnan, C., Chan, C. S., Dombeck, D. A., Deisseroth, K., & Awatramani, R. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0203-4 · Cited by 423 · see citing works
Nucleus Accumbens Subnuclei Regulate Motivated Behavior via Direct Inhibition and Disinhibition of VTA Dopamine Subpopulations
Yang, H., de Jong, J. W., Tak, Y., Peck, J., Bateup, H. S., & Lammel, S. (2018) · Neuron · doi:10.1016/j.neuron.2017.12.022 · Cited by 407 · see citing works
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Model-based and model-free Pavlovian reward learning: Revaluation, revision, and revelation
Dayan, P., & Berridge, K. C. (2014) · Cognitive, Affective, & Behavioral Neuroscience · doi:10.3758/s13415-014-0277-8 · Cited by 357 · see citing works
Neuromodulation of Attention
Thiele, A., & Bellgrove, M. A. (2018) · Neuron · doi:10.1016/j.neuron.2018.01.008 · Cited by 350 · see citing works
Neurobiology of Resilience: Interface Between Mind and Body
Cathomas, F., Murrough, J. W., Nestler, E. J., Han, M.-H., & Russo, S. J. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2019.04.011 · Cited by 296 · see citing works
Single-cell RNA sequencing reveals midbrain dopamine neuron diversity emerging during mouse brain development
Tiklová, K., Björklund, Å. K., Lahti, L., Fiorenzano, A., Nolbrant, S., Gillberg, L., Volakakis, N., Yokota, C., Hilscher, M. M., Hauling, T., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-08453-1 · Cited by 276 · 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
Ventral tegmental area dopamine revisited: effects of acute and repeated stress
Holly, E. N., & Miczek, K. A. (2016) · Psychopharmacology · doi:10.1007/s00213-015-4151-3 · Cited by 265 · see citing works
Reward and aversion
Hu, H. (2016) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-070815-014106 · Cited by 253 · see citing works
5-HT release in nucleus accumbens rescues social deficits in mouse autism model
Walsh, J. J., Christoffel, D. J., Heifets, B. D., Ben-Dor, G. A., Selimbeyoglu, A., Hung, L. W., Deisseroth, K., & Malenka, R. C. (2018) · Nature · doi:10.1038/s41586-018-0416-4 · Cited by 256 · see citing works
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Organization of monosynaptic inputs to the serotonin and dopamine neuromodulatory systems
Ogawa, S. K., Cohen, J. Y., Hwang, D., Uchida, N., & Watabe-Uchida, M. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.06.042 · Cited by 249 · 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
Essential Role of Mesolimbic Brain-Derived Neurotrophic Factor in Chronic Social Stress–Induced Depressive Behaviors
Wook Koo, J., Labonté, B., Engmann, O., Calipari, E. S., Juarez, B., Lorsch, Z., Walsh, J. J., Friedman, A. K., Yorgason, J. T., Han, M.-H., et al. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.12.009 · Cited by 231 · see citing works
Distributed and Mixed Information in Monosynaptic Inputs to Dopamine Neurons
Tian, J., Huang, R., Cohen, J. Y., Osakada, F., Kobak, D., Machens, C. K., Callaway, E. M., Uchida, N., & Watabe-Uchida, M. (2016) · Neuron · doi:10.1016/j.neuron.2016.08.018 · Cited by 224 · see citing works
Glutamate neurons within the midbrain dopamine regions
Morales, M., & Root, D. H. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.05.032 · Cited by 218 · see citing works
Mesolimbic Dopamine and the Regulation of Motivated Behavior
Salamone, J. D., Pardo, M., Yohn, S. E., López-Cruz, L., SanMiguel, N., & Correa, M. (2015) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2015_383 · Cited by 204 · see citing works
Dopamine regulates aversive contextual learning and associated in vivo synaptic plasticity in the Hippocampus
Broussard, J. I., Yang, K., Levine, A. T., Tsetsenis, T., Jenson, D., Cao, F., Garcia, I., Arenkiel, B. R., Zhou, F.-M., De Biasi, M., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.01.070 · Cited by 180 · see citing works
“Recent studies indicate that a DA neuron’s response to negative or positive stimuli is largely dependent upon the neuron’s presynaptic inputs, and the dopaminergic signal influences separate brain regions depending on valence (Lammel et al., 2011, 2012, 2014).”
BackgroundResult
New insights into the specificity and plasticity of reward and aversion encoding in the mesolimbic system
Volman, S. F., Lammel, S., Margolis, E. B., Kim, Y., Richard, J. M., Roitman, M. F., & Lobo, M. K. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.3250-13.2013 · Cited by 168 · see citing works
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Role of VTA dopamine neurons and neuroligin 3 in sociability traits related to nonfamiliar conspecific interaction
Bariselli, S., Hörnberg, H., Prévost-Solié, C., Musardo, S., Hatstatt-Burklé, L., Scheiffele, P., & Bellone, C. (2018) · Nature Communications · doi:10.1038/s41467-018-05382-3 · Cited by 171 · see citing works
Nucleus Accumbens Modulation in Reward and Aversion
Klawonn, A. M., & Malenka, R. C. (2018) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2018.83.037457 · Cited by 163 · see citing works
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Deep Brain Stimulation of the Human Reward System for Major Depression—Rationale, Outcomes and Outlook
Schlaepfer, T. E., Bewernick, B. H., Kayser, S., Hurlemann, R., & Coenen, V. A. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.28 · Cited by 160 · see citing works
Neural mechanisms regulating different forms of risk-related decision-making: Insights from animal models
Orsini, C. A., Moorman, D. E., Young, J. W., Setlow, B., & Floresco, S. B. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.04.009 · Cited by 153 · 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
Mesocorticolimbic Dopamine Pathways Across Adolescence: Diversity in Development
Reynolds, L. M., & Flores, C. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.735625 · Cited by 137 · see citing works
Multiphasic modulation of cholinergic interneurons by nigrostriatal afferents
Straub, C., Tritsch, N. X., Hagan, N. A., Gu, C., & Sabatini, B. L. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0589-14.2014 · Cited by 130 · see citing works
Reward-centricity and attenuated aversions: an adolescent phenotype emerging from studies in laboratory animals
Doremus-Fitzwater, T. L., & Spear, L. P. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.08.015 · Cited by 125 · see citing works
Deep brain stimulation of the medial forebrain bundle: Distinctive responses in resistant depression
Fenoy, A. J., Schulz, P., Selvaraj, S., Burrows, C., Spiker, D., Cao, B., Zunta-Soares, G., Gajwani, P., Quevedo, J., & Soares, J. (2016) · Journal of Affective Disorders · doi:10.1016/j.jad.2016.05.064 · Cited by 125 · see citing works
Mapping social reward and punishment processing in the human brain: A voxel-based meta-analysis of neuroimaging findings using the social incentive delay task
Martins, D., Rademacher, L., Gabay, A. S., Taylor, R., Richey, J. A., Smith, D. V., Goerlich, K. S., Nawijn, L., Cremers, H. R., Wilson, R., et al. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.12.034 · Cited by 119 · see citing works
A longitudinal study on deep brain stimulation of the medial forebrain bundle for treatment-resistant depression
Fenoy, A. J., Schulz, P. E., Selvaraj, S., Burrows, C. L., Zunta-Soares, G., Durkin, K., Zanotti-Fregonara, P., Quevedo, J., & Soares, J. C. (2018) · Translational Psychiatry · doi:10.1038/s41398-018-0160-4 · Cited by 118 · see citing works
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 · see citing works
Role of the Brain's Reward Circuitry in Depression
Nestler, E. J. (2015) · International review of neurobiology · doi:10.1016/bs.irn.2015.07.003 · Cited by 108 · see citing works
Sources of input to the rostromedial tegmental nucleus, ventral tegmental area, and lateral habenula compared: A study in rat
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 · see citing works
Developmental Exposure to Perfluorooctane Sulfonate (PFOS) and Perfluorooctanoic Acid (PFOA) Selectively Decreases Brain Dopamine Levels in Northern Leopard Frogs
Foguth, R. M., Flynn, R. W., de Perre, C., Iacchetta, M., Lee, L. S., Sepúlveda, M. S., & Cannon, J. R. (2019) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2019.114623 · Cited by 103 · see citing works
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 · see citing works
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Illuminating circuitry relevant to psychiatric disorders with optogenetics
Steinberg, E. E., Christoffel, D. J., Deisseroth, K., & Malenka, R. C. (2015) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.08.004 · Cited by 92 · see citing works
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A framework for understanding the emerging role of corticolimbic-ventral striatal networks in OCD-associated repetitive behaviors
Wood, J., & Ahmari, S. E. (2015) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2015.00171 · Cited by 85 · see citing works
“Dysregulation of this circuit in OCD could potentially contribute to compulsive behavior. basolateral nuclei to the central nucleus of the amygdala, which functions as an output to numerous brain regions (LeDoux, 2007; Janak and Tye, 2015).”
Background
Dopamine Circuit Mechanisms of Addiction-Like Behaviors
Poisson, C. L., Engel, L., & Saunders, B. T. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.752420 · Cited by 75 · see citing works
Combinatorial Expression of Grp and Neurod6 Defines Dopamine Neuron Populations with Distinct Projection Patterns and Disease Vulnerability
Kramer, D. J., Risso, D., Kosillo, P., Ngai, J., & Bateup, H. S. (2018) · eNeuro · doi:10.1523/eneuro.0152-18.2018 · Cited by 70 · see citing works
Neural circuits regulating prosocial behaviors
Walsh, J. J., Christoffel, D. J., & Malenka, R. C. (2023) · Neuropsychopharmacology · doi:10.1038/s41386-022-01348-8 · Cited by 72 · see citing works
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The Formation and Function of the VTA Dopamine System
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Authors: Lammel, S., Lim, B. K., & Malenka, R. C.
Affiliations: Stanford Medicine (US)
Corresponding author: Malenka, Robert C.
ORCID: Lammel, Stephan
Lim, Byung Kook
Malenka, Robert C.
Venue: Neuropharmacology
Publisher: Elsevier BV
Published: 2014-01
Volume: 76
Pages: 351-359
ISSN: 0028-3908 (ISSN-L)
DOI: 10.1016/j.neuropharm.2013.03.019
PMC: PMC3778102
OpenAlex: W2045821490
Cited by: 804
References: 126
Citations by year: 2026: 47 · 2025: 59 · 2024: 61 · 2023: 56 · 2022: 61 · 2021: 83 · 2020: 71 · 2019: 83 · 2018: 73 · 2017: 47 · 2016: 55 · 2015: 64 · 2014: 36 · 2013: 8
FWCI: 5.42
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Neuropharmacology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: Simons Foundation Autism Research Initiative
National Institutes of Health
National Institute of Mental Health (P50MH086403)
National Institute on Drug Abuse (R21DA032955, P01DA008227)
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, midbrain dopamine system, reward processing, aversion, stress, cocaine, drugs of abuse, neural circuits, motivation, addiction, depression
MeSH terms: Animals, Dopamine, Humans, Nerve Net, Reward, Ventral Tegmental Area

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Reward and aversion in a heterogeneous midbrain dopamine system

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