Properties and opioid inhibition of mesolimbic dopamine neurons vary according to target location
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The mesolimbic dopamine system, which mediates the rewarding properties of nearly all drugs of abuse, originates in the ventral tegmental area (VTA) and sends major projections to both the nucleus accumbens (NAc) and the basolateral amygdala (BLA). To address whether differences occur between neurons that project to these separate areas, retrograde microspheres were injected to either the BLA or the NAc of DBA/2J mice. Whole-cell recordings were made from labeled VTA dopamine neurons. We found that identified neurons that projected to the BLA and NAc originated within different quadrants of the VTA with neither group exhibiting large-amplitude h-currents. Neurons that projected to the NAc exhibited a greater outward current in response to the kappa-opioid agonist (5alpha,7alpha,8alpha)-(+)-N-methyl-N-[7-(pyrrolidinyl)-1-oxaspiro [4,5]dec-8-yl]-benzeneacetamide (U69593; 200 nM), whereas neurons that projected to the BLA exhibited greater inhibition to the mu/delta opioid agonist [Met5] enkephalin (ME; 3 microM). In addition, we found that the presynaptic inhibition of GABAergic transmission at both GABAA and GABAB receptors was differentially regulated by U69593 between the two groups. When dopamine IPSCs were examined, U69593 caused a greater inhibition in NAc- than BLA-projecting neurons. ME had no effect on either. Finally, the regulation of extracellular dopamine by dopamine uptake transporters was equal across the VTA. These results suggest that opioids differentially inhibit mesolimbic neurons depending on their target projections. Identifying the properties of projecting mesolimbic VTA dopamine neurons is crucial to understanding the action of drugs of abuse.
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Species-related quantitative differences in dopamine function between rats and mice may account for differences in results.
“Species related quantitative differences in DA function between rats and mice may account for the differences in the results (42, 43).”
From Withdrawal from Chronic Nicotine Exposure Alters Dopamine Signaling Dynamics in the Nucleus Accumbens (2012) · cites this paper as [42]
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Cites
The Mouse Brain in Stereotaxic Coordinates
Paxinos, G. (2001) · Cited by 12,859 · 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
Swanson, L. W. (1982) · Brain Research Bulletin · doi:10.1016/0361-9230(82)90145-9 · Cited by 1,718 · see citing works
Opioids excite dopamine neurons by hyperpolarization of local interneurons
Johnson, S., & North, R. (1992) · The Journal of Neuroscience · doi:10.1523/jneurosci.12-02-00483.1992 · Cited by 1,637 · see citing works
Ikemoto, S., & Panksepp, J. (1999) · Brain Research Reviews · doi:10.1016/s0165-0173(99)00023-5 · Cited by 1,450 · see citing works
Mesocorticolimbic dopaminergic network: functional and regulatory roles
Moal, M. L., & Simon, H. (1991) · Physiological Reviews · doi:10.1152/physrev.1991.71.1.155 · Cited by 1,096 · see citing works
Wise, R. A. (1996) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(96)80079-1 · Cited by 1,072 · see citing works
Cellular and Synaptic Adaptations Mediating Opioid Dependence
Williams, J. T., Christie, M. J., & Manzoni, O. J. (2001) · Physiological Reviews · doi:10.1152/physrev.2001.81.1.299 · Cited by 852 · see citing works
The neuropsychological basis of addictive behaviour
Everitt, B. J., Dickinson, A., & Robbins, T. W. (2001) · Brain Research Reviews · doi:10.1016/s0165-0173(01)00088-1 · Cited by 808 · see citing works
Addictive Drugs and Brain Stimulation Reward
Wise, R. A. (1996) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.19.030196.001535 · Cited by 792 · see citing works
Uniform Inhibition of Dopamine Neurons in the Ventral Tegmental Area by Aversive Stimuli
Ungless, M. A., Magill, P. J., & Bolam, J. P. (2004) · Science · doi:10.1126/science.1093360 · Cited by 782 · see citing works
Grace, A., & Onn, S. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-10-03463.1989 · Cited by 720 · see citing works
Two types of neurone in the rat ventral tegmental area and their synaptic inputs.
Johnson, S. W., & NORTH, R. A. (1992) · The Journal of Physiology · doi:10.1113/jphysiol.1992.sp019136 · Cited by 672 · see citing works
Release of dopamine from dendrites in rat substantia nigra
Geffen, L. B., Jessell, T. M., Cuello, A. C., & Iversen, L. L. (1976) · Nature · doi:10.1038/260258a0 · Cited by 650 · see citing works
Joel, D., & Weiner, I. (2000) · Neuroscience · doi:10.1016/s0306-4522(99)00575-8 · Cited by 614 · see citing works
Hatfield, T., Han, J.-S., Conley, M., Gallagher, M., & Holland, P. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-16-05256.1996 · Cited by 555 · see citing works
Bals-Kubik, R., Ableitner, A., Herz, A., & Shippenberg, T. S. (1993) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)10296-6 · Cited by 525 · see citing works
Morphine-induced activation of A10 dopamine neurons in the rat
Gysling, K., & Wang, R. Y. (1983) · Brain Research · doi:10.1016/0006-8993(83)90913-7 · Cited by 493 · see citing works
Neuhoff, H., Neu, A. D., Liss, B., & Roeper, J. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-04-01290.2002 · Cited by 400 · see citing works
Vesicular Dopamine Release Elicits an Inhibitory Postsynaptic Current in Midbrain Dopamine Neurons
Beckstead, M. J., Grandy, D. K., Wickman, K. D., & Williams, J. T. (2004) · Neuron · doi:10.1016/j.neuron.2004.05.019 · Cited by 368 · see citing works
Membrane properties of rat locus coeruleus neurones
Williams, J. T., North, R. A., Shefner, S. A., Nishi, S., & Egan, T. M. (1984) · Neuroscience · doi:10.1016/0306-4522(84)90265-3 · Cited by 341 · see citing works
Reinforcing effects of morphine microinjection into the ventral tegmental area
Phillips, A. G., & LePiane, F. G. (1980) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(80)90460-8 · Cited by 339 · see citing works
Whitelaw, R. B., Markou, A., Robbins, T. W., & Everitt, B. J. (1996) · PubMed · Cited by 306 · see citing works
Hasue, R. H., & Shammah‐Lagnado, S. J. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10420 · Cited by 306 · see citing works
K-ATP channels promote the differential degeneration of dopaminergic midbrain neurons
Liss, B., Haeckel, O., Wildmann, J., Miki, T., Seino, S., & Roeper, J. (2005) · Nature Neuroscience · doi:10.1038/nn1570 · Cited by 300 · see citing works
Synaptic regulation of mesocorticolimbic dopamine neurons
White, F. J. (1996) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.19.030196.002201 · Cited by 289 · see citing works
Increased probability of GABA release during withdrawal from morphine
Bonci, A., & Williams, J. T. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-02-00796.1997 · Cited by 286 · see citing works
Self-citationκ-Opioid Agonists Directly Inhibit Midbrain Dopaminergic Neurons
Margolis, E. B., Hjelmstad, G. O., Bonci, A., & Fields, H. L. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-31-09981.2003 · Cited by 276 · see citing works
Dopamine D1 receptors facilitate transmitter release
Cameron, D. L., & Williams, J. T. (1993) · Nature · doi:10.1038/366344a0 · Cited by 263 · see citing works
5-hydroxytryptamine1B receptors block the GABAB synaptic potential in rat dopamine neurons
Johnson, S., Mercuri, N. B., & North, R. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-05-02000.1992 · Cited by 249 · see citing works
μ-Opposing actions of the κ-opioid receptor
Pan, Z. Z. (1998) · Trends in Pharmacological Sciences · doi:10.1016/s0165-6147(98)01169-9 · Cited by 238 · see citing works
Whitelaw, R. B., Markou, A., Robbins, T. W., & Everitt, B. J. (1996) · Psychopharmacology · doi:10.1007/bf02805996 · Cited by 228 · see citing works
See, R. E., Kruzich, P. J., & Grimm, J. W. (2001) · Psychopharmacology · doi:10.1007/s002130000636 · Cited by 222 · see citing works
Synaptic inputs to GABAA and GABAB receptors originate from discrete afferent neurons
Sugita, S., Johnson, S. W., & North, R. A. (1992) · Neuroscience Letters · doi:10.1016/0304-3940(92)90518-c · Cited by 220 · see citing works
Adell, A., & Artigas, F. (2004) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.05.001 · Cited by 190 · see citing works
Altered Dopamine Release and Uptake Kinetics in Mice Lacking D2Receptors
Schmitz, Y., Schmauss, C., & Sulzer, D. L. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-18-08002.2002 · Cited by 176 · see citing works
A Comparison of Axonal and Somatodendritic Dopamine Release Using In Vivo Dialysis
Kalivas, P. W., & Duffy, P. (1991) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1991.tb02015.x · Cited by 165 · 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
Chefer, V. I., Czyzyk, T. A., Bolan, E. A., Morón, J. A., Pintar, J. E., & Shippenberg, T. S. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0854-05.2005 · Cited by 155 · see citing works
Bachtell, R. K., Whisler, K., Karanian, D., & Self, D. W. (2005) · Psychopharmacology · doi:10.1007/s00213-005-0133-1 · Cited by 154 · see citing works
Cragg, S. J., Nicholson, C., Kume‐Kick, J., Tao, L., & Rice, M. E. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.85.4.1761 · Cited by 150 · see citing works
Albanese, A., & Minciacchi, D. (1983) · The Journal of Comparative Neurology · doi:10.1002/cne.902160406 · Cited by 130 · see citing works
Cragg, S. J., Rice, M. E., & Greenfield, S. A. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.77.2.863 · Cited by 118 · see citing works
A Specific Limbic Circuit Underlies Opiate Withdrawal Memories
Frenois, F., Stinus, L., Blasi, F. D., Cador, M., & Moine, C. L. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.3090-04.2005 · Cited by 117 · see citing works
Garzón, M., & Pickel, V. M. (2001) · Synapse · doi:10.1002/syn.1088 · Cited by 107 · see citing works
Brinley-Reed, M., & McDonald, A. J. (1999) · Brain Research · doi:10.1016/s0006-8993(99)02112-5 · Cited by 84 · see citing works
Infrared-Guided Laser Stimulation of Neurons in Brain Slices
Dodt, H., Eder, M., Schierloh, A., & Zieglgänsberger, W. (2002) · Science s STKE · doi:10.1126/stke.2002.120.pl2 · Cited by 75 · see citing works
Shoji, Y., Delfs, J. M., & Williams, J. T. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-06-02347.1999 · Cited by 65 · see citing works
Maurin, Y., Banrezes, B., Menetrey, A., Mailly, P., & Deniau, J. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00681-2 · Cited by 53 · see citing works
κ-Opioid Tolerance and Dependence in Cultures of Dopaminergic Midbrain Neurons
Dalman, F. C., & O’Malley, K. L. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-14-05750.1999 · Cited by 21 · see citing works
Senatorov, V. V., & Renaud, L. P. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00268-1 · Cited by 15 · see citing works
Unidirectional axonal transport in in vitro adult rat brain explants
Senatorov, V. V., & Hu, B. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)00278-9 · Cited by 3 · see citing works
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Sorted by citations
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
Unique properties of mesoprefrontal neurons within a dual mesocorticolimbic dopamine system
Lammel, S., Hetzel, A., Häckel, O., Jones, I., Liss, B., & Roeper, J. (2008) · Neuron · doi:10.1016/j.neuron.2008.01.022 · Cited by 976 · see citing works
Cortico-Basal Ganglia Reward Network: Microcircuitry
Sesack, S. R., & Grace, A. A. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.93 · Cited by 985 · see citing works
Reward and aversion in a heterogeneous midbrain dopamine system
Lammel, S., Lim, B. K., & Malenka, R. C. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.03.019 · Cited by 804 · see citing works
Phasic excitation of dopamine neurons in ventral VTA by noxious stimuli
Brischoux, F., Chakraborty, S., Brierley, D. I., & Ungless, M. A. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0811507106 · Cited by 801 · see citing works
Projection-specific modulation of dopamine neuron synapses by aversive and rewarding stimuli
Lammel, S., Ion, D. I., Roeper, J., & Malenka, R. C. (2011) · Neuron · doi:10.1016/j.neuron.2011.03.025 · Cited by 766 · see citing works
Jhou, T. C., Fields, H. L., Baxter, M. G., Saper, C. B., & Holland, P. C. (2009) · Neuron · doi:10.1016/j.neuron.2009.02.001 · Cited by 696 · see citing works
Margolis, E. B., Lock, H., Hjelmstad, G. O., & Fields, H. L. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2006.117069 · Cited by 527 · see citing works
Nobili, A., Latagliata, E. C., Viscomi, M. T., Cavallucci, V., Cutuli, D., Giacovazzo, G., Krashia, P., Rizzo, F. R., Marino, R., Federici, M., et al. (2017) · Nature Communications · doi:10.1038/ncomms14727 · Cited by 514 · see citing works
The neurobiology and genetics of impulse control disorders: Relationships to drug addictions
Brewer, J. A., & Potenza, M. N. (2007) · Biochemical Pharmacology · doi:10.1016/j.bcp.2007.06.043 · Cited by 515 · see citing works
Courtney, K. E., & Ray, L. A. (2014) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2014.08.003 · Cited by 502 · see citing works
Cellular neuroadaptations to chronic opioids: tolerance, withdrawal and addiction
Christie, M. J. (2008) · British Journal of Pharmacology · doi:10.1038/bjp.2008.100 · Cited by 481 · see citing works
Are you or aren’t you? Challenges associated with physiologically identifying dopamine neurons
Ungless, M. A., & Grace, A. A. (2012) · Trends in Neurosciences · doi:10.1016/j.tins.2012.02.003 · Cited by 431 · see citing works
Fields, H. L., & Margolis, E. B. (2015) · Trends in Neurosciences · doi:10.1016/j.tins.2015.01.002 · Cited by 432 · see citing works
Stamatakis, A. M., Jennings, J. H., Ung, R. L., Blair, G. A., Weinberg, R. J., Neve, R. L., Boyce, F., Mattis, J., Ramakrishnan, C., Deisseroth, K., et al. (2013) · Neuron · doi:10.1016/j.neuron.2013.08.023 · Cited by 364 · see citing works
Nashmi, R., Xiao, C., Deshpande, P., McKinney, S., Grady, S. R., Whiteaker, P., Huang, Q., McClure-Begley, T., Lindstrom, J. M., Labarca, C., et al. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2199-07.2007 · Cited by 274 · see citing works
Khaliq, Z. M., & Bean, B. P. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.0143-10.2010 · Cited by 261 · 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
Role of kappa-opioid receptors in stress and anxiety-related behavior
Veer, A. V., & Carlezon, W. A. (2013) · Psychopharmacology · doi:10.1007/s00213-013-3195-5 · Cited by 254 · see citing works
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
Blednov, Y. A., Benavidez, J. M., Geil, C., Perra, S., Morikawa, H., & Harris, R. A. (2011) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2011.01.008 · Cited by 240 · see citing works
Calculating utility: preclinical evidence for cost–benefit analysis by mesolimbic dopamine
Phillips, P. E. M., Walton, M. E., & Jhou, T. C. (2007) · Psychopharmacology · doi:10.1007/s00213-006-0626-6 · Cited by 237 · see citing works
Matsui, A., Jarvie, B. C., Robinson, B. G., Hentges, S. T., & Williams, J. T. (2014) · Neuron · doi:10.1016/j.neuron.2014.04.030 · Cited by 237 · see citing works
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
Stress-induced plasticity and functioning of ventral tegmental dopamine neurons
Douma, E. H., & de Kloet, E. R. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.10.015 · Cited by 226 · see citing works
VTA GABA Neurons at the Interface of Stress and Reward
Bouarab, C., Thompson, B. V., & Polter, A. M. (2019) · Frontiers in Neural Circuits · doi:10.3389/fncir.2019.00078 · 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
Dopamine is necessary for cue-dependent fear conditioning
Fadok, J. P., Dickerson, T. M. K., & Palmiter, R. D. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.1616-09.2009 · Cited by 213 · see citing works
Labouèbe, G., Lomazzi, M., Cruz, H. G., Creton, C., Luján, R., Li, M., Yanagawa, Y., Obata, K., Watanabe, M., Wickman, K. D., et al. (2007) · Nature Neuroscience · doi:10.1038/nn2006 · Cited by 208 · see citing works
Rogers, J. L., Ghee, S. M., & See, R. E. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.10.012 · Cited by 204 · 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
Matsui, A., & Williams, J. T. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.4570-11.2011 · Cited by 191 · see citing works
Kappa Opioid Receptor-Induced Aversion Requires p38 MAPK Activation in VTA Dopamine Neurons
Ehrich, J. M., Messinger, D. I., Knakal, C. R., Kuhar, J. R., Schattauer, S. S., Bruchas, M. R., Zweifel, L. S., Kieffer, B. L., Phillips, P. E. M., & Chavkin, C. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.2444-15.2015 · Cited by 187 · see citing works
Lecca, S., Melis, M., Luchicchi, A., Muntoni, A. L., & Pistis, M. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.302 · Cited by 185 · see citing works
Mietlicki‐Baase, E. G., Ortinski, P. I., Rupprecht, L. E., Olivos, D. R., Alhadeff, A. L., Pierce, R. C., & Hayes, M. R. (2013) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00413.2013 · Cited by 175 · see citing works
An update on the connections of the ventral mesencephalic dopaminergic complex
Yetnikoff, L., Lavezzi, H. N., Reichard, R. A., & Zahm, D. S. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.04.010 · Cited by 172 · see citing works
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
Morel, C., Montgomery, S. E., Li, L., Cuttoli, R. D.-D., Teichman, E. M., Juarez, B., Tzavaras, N., Ku, S. M., Flanigan, M. E., Cai, M., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-29155-1 · Cited by 167 · see citing works
Diversity of Dopaminergic Neural Circuits in Response to Drug Exposure
Juarez, B., & Han, M. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2016.32 · Cited by 165 · see citing works
Dopamine Signaling Differences in the Nucleus Accumbens and Dorsal Striatum Exploited by Nicotine
Zhang, T., Zhang, L., Liang, Y., Siapas, A. G., Zhou, F.-M., & Dani, J. A. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0261-09.2009 · Cited by 165 · see citing works
The dynorphin/κ-opioid receptor system and its role in psychiatric disorders
Tejeda, H. A., Shippenberg, T. S., & Henriksson, R. (2011) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-011-0844-x · Cited by 155 · see citing works
Kappa-opioid ligands in the study and treatment of mood disorders
Carlezon, W. A., Béguin, C., Knoll, A. T., & Cohen, B. M. (2009) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2009.05.008 · Cited by 156 · see citing works
Opioid Receptor-Mediated Regulation of Neurotransmission in the Brain
Reeves, K. C., Shah, N., Muñoz, B., & Atwood, B. K. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.919773 · Cited by 156 · see citing works
Morikawa, H., & Paladini, C. A. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.08.023 · Cited by 150 · see citing works
Heterogeneity of dopamine neuron activity across traits and states
Marinelli, M., & McCutcheon, J. E. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.07.034 · Cited by 141 · see citing works
Stress and VTA synapses: implications for addiction and depression
Polter, A. M., & Kauer, J. A. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12490 · Cited by 141 · see citing works
Orexin B/hypocretin 2 increases glutamatergic transmission to ventral tegmental area neurons
Borgland, S. L., Storm, E. E., & Bonci, A. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06397.x · Cited by 141 · see citing works
Ethanol Action on Dopaminergic Neurons in the Ventral Tegmental Area
Morikawa, H., & Morrisett, R. A. (2010) · International review of neurobiology · doi:10.1016/s0074-7742(10)91008-8 · Cited by 139 · see citing works
Zhang, L., Dong, Y., Doyon, W. M., & Dani, J. A. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.07.024 · Cited by 135 · see citing works
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 135 · see citing works
Sex Differences in Kappa Opioid Receptor Function and Their Potential Impact on Addiction
Chartoff, E. H., & Mavrikaki, M. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00466 · Cited by 134 · see citing works
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 · see citing works
Control of Extracellular Dopamine at Dendrite and Axon Terminals
Ford, C., Gantz, S. C., Phillips, P. E. M., & Williams, J. T. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1020-10.2010 · Cited by 135 · see citing works
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
Jarjour, S., Bai, L., & Gianoulakis, C. (2009) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2009.00924.x · Cited by 130 · see citing works
Kokane, S. S., & Perrotti, L. I. (2020) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2020.00074 · Cited by 123 · see citing works
Kappa Opioid Receptors Regulate Stress-Induced Cocaine Seeking and Synaptic Plasticity
Graziane, N. M., Polter, A. M., Briand, L. A., Pierce, R. C., & Kauer, J. A. (2013) · Neuron · doi:10.1016/j.neuron.2012.12.034 · Cited by 121 · see citing works
Role 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 · see citing works
Chieng, B. C. H., Azriel, Y., Mohammadi, S. A., & Christie, M. J. (2011) · The Journal of Physiology · doi:10.1113/jphysiol.2011.210807 · Cited by 120 · see citing works
Oxycodone in the Opioid Epidemic: High ‘Liking’, ‘Wanting’, and Abuse Liability
Kibaly, C., Alderete, J. A., Liu, S. H., Nasef, H., Law, P., Evans, C. J., & Cahill, C. M. (2020) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-020-01013-y · Cited by 116 · see citing works
Piecing together the puzzle of acetaldehyde as a neuroactive agent
Correa, M., Salamone, J. D., Segovia, K. N., Pardo, M., Longoni, R., Spina, L., Peana, A. T., Vinci, S., & Acquas, E. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.07.009 · Cited by 118 · see citing works
Mazei‐Robison, M. S., & Nestler, E. J. (2012) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a012070 · Cited by 113 · see citing works
Karkhanis (2017) · doi:10.1016/bs.irn.2017.08.001 · Cited by 113 · see citing works
Energy regulatory signals and food reward
Figlewicz, D. P., & Sipols, A. J. (2010) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2010.03.002 · Cited by 111 · see citing works
Brain Reward Circuits in Morphine Addiction
Kim, J., Ham, S., Hong, H., Moon, C., & Im, H. (2016) · Molecules and Cells · doi:10.14348/molcells.2016.0137 · Cited by 113 · see citing works
Tejeda, H. A., & Bonci, A. (2018) · Brain Research · doi:10.1016/j.brainres.2018.09.023 · Cited by 112 · see citing works
Differential Activation and Trafficking of μ-Opioid Receptors in Brain Slices
Arttamangkul, S., Quillinan, N., Low, M. J., von Zastrow, M., Pintar, J. E., & Williams, J. T. (2008) · Molecular Pharmacology · doi:10.1124/mol.108.048512 · Cited by 112 · see citing works
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 · see citing works
Acetaldehyde mediates alcohol activation of the mesolimbic dopamine system
Melis, M., Enrico, P., Peana, A. T., & Diana, M. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05887.x · Cited by 107 · see citing works
Dopamine neurons in the ventral tegmental area fire faster in adolescent rats than in adults
McCutcheon, J. E., Conrad, K. L., Carr, S. B., Ford, K. A., McGehee, D. S., & Marinelli, M. (2012) · Journal of Neurophysiology · doi:10.1152/jn.00077.2012 · Cited by 106 · see citing works
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 106 · see citing works
Riegel, A. C., Zapata, A. G., Shippenberg, T. S., & French, E. D. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301273 · Cited by 105 · see citing works
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 104 · see citing works
Evans, R. C., Zhu, M., & Khaliq, Z. M. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.0117-17.2017 · Cited by 101 · see citing works
Regulation of the mesolimbic dopamine circuit by feeding peptides
Liu, S., & Borgland, S. L. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2014.12.046 · Cited by 100 · see citing works
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
Theile, J. W., Morikawa, H., Gonzales, R. A., & Morrisett, R. A. (2008) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2008.00665.x · Cited by 100 · see citing works
Diversity 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 · 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
CRF Facilitates Calcium Release from Intracellular Stores in Midbrain Dopamine Neurons
Riegel, A. C., & Williams, J. T. (2008) · Neuron · doi:10.1016/j.neuron.2007.12.029 · Cited by 97 · see citing works
Robinson, D. L., Howard, E. C., McConnell, S., Gonzales, R. A., & Wightman, R. M. (2009) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2009.00942.x · Cited by 97 · see citing works
Conversano, C., Marazziti, D., Carmassi, C., Baldini, S., Barnabei, G., & Dell'Osso, L. (2012) · Harvard Review of Psychiatry · doi:10.3109/10673229.2012.694318 · Cited by 110 · see citing works
Sheng, Z., Santiago, A. M., Thomas, M. P., & Routh, V. H. (2014) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2014.08.001 · Cited by 95 · see citing works
Endogenous opiates and behavior: 2006
Bodnar, R. J. (2007) · Peptides · doi:10.1016/j.peptides.2007.09.002 · Cited by 91 · see citing works
Fadok, J. P., Darvas, M., Dickerson, T. M. K., & Palmiter, R. D. (2010) · PLoS ONE · doi:10.1371/journal.pone.0012751 · Cited by 90 · see citing works
Role of Mu- and Delta-Opioid Receptors in the Nucleus Accumbens in Cocaine-Seeking Behavior
Simmons, D. L., & Self, D. W. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2009.28 · Cited by 89 · see citing works
Nicotine Potentiation of Excitatory Inputs to Ventral Tegmental Area Dopamine Neurons
Mao, D., Gallagher, K., & McGehee, D. S. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.5671-10.2011 · Cited by 90 · see citing works
Chen, M., Zhao, Y., Yang, H., Luan, W., Song, J., Cui, D., Dong, Y. W., Lai, B., Ma, L., & Zheng, P. (2015) · eLife · doi:10.7554/elife.09275 · Cited by 88 · see citing works
Spontaneous Inhibitory Synaptic Currents Mediated by a G Protein-Coupled Receptor
Gantz, S. C., Bunzow, J. R., & Williams, J. T. (2013) · Neuron · doi:10.1016/j.neuron.2013.04.013 · Cited by 88 · see citing works
Enhanced serotonin and mesolimbic dopamine transmissions in a rat model of neuropathic pain
Sagheddu, C., Aroni, S., Felice, M. D., Lecca, S., Luchicchi, A., Melis, M., Muntoni, A. L., Romano, R., Palazzo, E., Guida, F., et al. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2015.06.003 · Cited by 86 · see citing works
Kappa Opioid Inhibition of Somatodendritic Dopamine Inhibitory Postsynaptic Currents
Ford, C., Beckstead, M. J., & Williams, J. T. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00963.2006 · Cited by 84 · see citing works
Lintas, A., Chi, N., Lauzon, N. M., Bishop, S. F., Gholizadeh, S., Sun, N., Tan, H., & Laviolette, S. R. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.1781-11.2011 · Cited by 84 · see citing works
The Time Course of Dopamine Transmission in the Ventral Tegmental Area
Ford, C., Phillips, P. E. M., & Williams, J. T. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.3546-09.2009 · Cited by 84 · see citing works
Food Restriction Increases Glutamate Receptor-Mediated Burst Firing of Dopamine Neurons
Branch, S. Y., Goertz, R. B., Sharpe, A. L., Pierce, J., Roy, S., Ko, D., Paladini, C. A., & Beckstead, M. J. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.5099-12.2013 · Cited by 81 · see citing works
Jordan, C. J., Humburg, B. A., RICE, M. S., Bi, G., You, Z., Shaik, A. B., Cao, J., Bonifazi, A., Gadiano, A. J., Rais, R., et al. (2019) · Neuropharmacology · doi:10.1016/j.neuropharm.2019.04.003 · Cited by 82 · see citing works
Neuroinflammation—a co-occurring phenomenon linking chronic pain and opioid dependence
Cahill, C. M., & Taylor, A. M. W. (2017) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2016.12.003 · Cited by 82 · see citing works
Ray, L. A., Bujarski, S., Courtney, K. E., Moallem, N. R., Lunny, K. F., Roche, D., Leventhal, A. M., SHOPTAW, S. J., Heinzerling, K. G., London, E. D., et al. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.83 · Cited by 79 · see citing works
Branch, S. Y., Sharma, R. V., & Beckstead, M. J. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.4228-13.2014 · Cited by 79 · see citing works
Brown, P. L., & Shepard, P. D. (2016) · Journal of Neurophysiology · doi:10.1152/jn.00305.2016 · Cited by 75 · see citing works
Khaliq, Z. M., & Bean, B. P. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.2237-08.2008 · Cited by 77 · see citing works
- Authors
- Ford, C. P., Mark, G. P., & Williams, J. T.
- Affiliations
- Oregon Health & Science University (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2006-03-08
- Volume
- 26
- Issue
- 10
- Pages
- 2788-2797
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3623681
- OpenAlex
- W2012111567
- Cited by
- 339
- References
- 52
- Citations by year
- 2026: 12 · 2025: 9 · 2024: 7 · 2023: 14 · 2022: 14 · 2021: 8 · 2020: 14 · 2019: 14 · 2018: 10 · 2017: 24 · 2016: 22 · 2015: 26 · 2014: 25 · 2013: 28 · 2012: 21
- FWCI
- 7.20
- 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)
- Europe PMC (PubMed Central) (acceptedVersion)
- Funders
- Life Sciences Research Foundation
- Fondation pour la Recherche Médicale
- National Institutes of Health
- National Institute on Drug Abuse (DA04523, DA 014639, R01DA008163, DA-08163, R01DA014639, R01DA004523)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- mesolimbic dopamine system, ventral tegmental area, nucleus accumbens, basolateral amygdala, opioid inhibition, kappa opioid receptor, [Met5]enkephalin, presynaptic inhibition, GABAA receptor, GABAB receptors, retrograde tracing, drug reward
- MeSH terms
- Amygdala, Analgesics, Animals, Bicuculline, Biotin, Cell Count, Dopamine, Dose-Response Relationship, Radiation, Drug Interactions, Electric Stimulation, Female, Immunohistochemistry, Limbic System, Male, Membrane Potentials, Mice, Inbred DBA, Microinjections, Molecular Sequence Data, Naloxone, Narcotic Antagonists, Narcotics, Neural Inhibition, Neural Pathways, Synaptic Transmission, Neurons, Nucleus Accumbens, Reaction Time, Serotonin, Tyrosine 3-Monooxygenase, Serotonin Receptor Agonists, Ventral Tegmental Area, Patch-Clamp Techniques, GABA Antagonists, Mice, In Vitro Techniques
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