Rewarding and psychomotor stimulant effects of endomorphin-1: anteroposterior differences within the ventral tegmental area and lack of effect in nucleus accumbens
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Endomorphin-1 (EM-1) is a recently isolated endogenous peptide having potent analgesic activity and high affinity and selectivity for the mu-opioid receptor. The present study was designed to investigate the rewarding and psychomotor stimulant effects of EM-1 in specific brain regions. We found that rats would learn without priming or response shaping to lever-press for microinjections of EM-1 into the ventral tegmental area (VTA); responding was most vigorous for high-dose injections into the posterior VTA. Rats did not learn to lever-press for microinjections of EM-1 into the nucleus accumbens (NAS) or regions just dorsal to the VTA. Lever-pressing for EM-1 in the VTA was extinguished when vehicle was substituted for the peptide and was reinstated when EM-1 reinforcement was re-established. Conditioned place preference was established by EM-1 injections into the posterior but not the anterior VTA or the NAS. Injection of EM-1 (0.1-1.0 nmol) into the posterior VTA induced robust increases in locomotor activity, whereas injections into the anterior VTA had very weak locomotor-stimulating effects. When injected into the NAS, EM-1 (0.1-10.0 nmol) did not affect locomotor activity. The present findings implicate the posterior VTA as a highly specific and sensitive site for opioid reward and suggest a role for EM-1-containing projections to the posterior VTA in the rewarding effects of other reinforcers.
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Drugs such as nicotine and opiates are more rewarding when administered into the posterior VTA or the central linear nucleus than into the anterior VTA.
“Drugs such as nicotine and opiates are more rewarding when administered into the posterior VTA or the central linear nucleus than into the anterior VTA.”
From Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens–olfactory tubercle complex (2007) · cites this paper as Zangen et al., 2002
Rats learn to lever-press for administration of drugs such as nicotine, carbachol, opiates, cannabinoids, cocaine, ethanol and its metabolite acetaldehyde into the posterior VTA more readily than into the anterior VTA.
“Rats learn to lever-press for administration of drugs such as nicotine (Ikemoto et al., 2006), carbachol (Ikemoto and Wise, 2002), opiates (Zangen et al., 2002), cannabinoids (Zangen et al., 2006), cocaine (Rodd et al., 2005), ethanol (Rodd-Henricks et al., 2000) and its metabolite acetaldehyde (Rodd et al., 2004) into the posterior VTA more readily than into the anterior VTA.”
From Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens–olfactory tubercle complex (2007) · cites this paper as Zangen et al., 2002
Other drugs of abuse such as nicotine and opiates appear to act in the posteromedial VTA and central linear nucleus.
“Other drugs of abuse such as nicotine and opiates appear to act in the posteromedial VTA and central linear nucleus.”
From Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens–olfactory tubercle complex (2007) · cites this paper as Zangen et al., 2002
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Cites
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
A psychomotor stimulant theory of addiction.
Wise, R. A., & Bozarth, M. A. (1987) · Psychological Review · doi:10.1037/0033-295x.94.4.469 · Cited by 2,747 · 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
A potent and selective endogenous agonist for the µ-opiate receptor
Zadina, J. E., Hackler, L., Ge, L.-J., & Kastin, A. J. (1997) · Nature · doi:10.1038/386499a0 · Cited by 1,309 · 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
Neuroleptic-Induced "Anhedonia" in Rats: Pimozide Blocks Reward Quality of Food
Wise, R. A., Spindler, J., de Wit, H., & Gerberg, G. J. (1978) · Science · doi:10.1126/science.566469 · Cited by 636 · 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
Intracranial self-administration of morphine into the ventral tegmental area in rats
Bozarth, M. A., & Wise, R. A. (1981) · Life Sciences · doi:10.1016/0024-3205(81)90148-x · Cited by 503 · see citing works
A biological theory of reinforcement.
Glickman, S. E., & Schiff, B. B. (1967) · Psychological Review · doi:10.1037/h0024290 · Cited by 466 · see citing works
Three‐dimensional reconstruction of the antennal lobe in Drosophila melanogaster
Laissue, P. P., Reiter, C., Hiesinger, P. R., Halter, S., Fischbach, K. F., & Stocker, R. F. (1999) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19990322)405:4 · Cited by 421 · see citing works
Functional interaction between opioid and cannabinoid receptors in drug self-administration.
Navarro, M., Carrera, M. R. A., Fratta, W., Valverde, O., Cossu, G., Fattore, L., Chowen, J. A., Gómez, R., del Arco, I., Villanúa, M. A., et al. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-14-05344.2001 · Cited by 378 · see citing works
Immunohistochemical localization of the cloned μ opioid receptor in the rat CNS
Mansour, A., Fox, C. A., Burke, S., Akil, H., & Watson, S. J. (1995) · Journal of Chemical Neuroanatomy · doi:10.1016/0891-0618(95)00055-c · Cited by 370 · see citing works
Kalivas, P. W., Widerlöv, E., Stanley, D. A., Breese, G. R., & Prange, A. J. (1983) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)22000-6 · Cited by 358 · see citing works
Rewarding Actions of Phencyclidine and Related Drugs in Nucleus Accumbens Shell and Frontal Cortex
Carlezon, & Wise, R. A. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-09-03112.1996 · Cited by 327 · see citing works
Self-citationOpiate reward: Sites and substrates
Wise, R. A. (1989) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(89)80021-1 · Cited by 286 · see citing works
Suppression of deprivation-induced food and water intake in rats and mice by naloxone.
Brown, D. R., & Holtzman, S. (1979) · Pharmacology, Biochemistry and Behavior · doi:10.1016/0091-3057(79)90043-1 · Cited by 271 · see citing works
Reinforcing effects of morphine in the nucleus accumbens
OLDS, M. E. (1982) · Brain Research · doi:10.1016/0006-8993(82)90454-1 · Cited by 259 · see citing works
Self-administration of morphine, DAMGO, and DPDPE into the ventral tegmental area of rats
Devine, D. P., & Wise, R. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-04-01978.1994 · Cited by 256 · see citing works
Self-administration of methionine enkephalin into the nucleus accumbens
Goeders, N. E., Lane, J. D., & Smith, J. E. (1984) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(84)90284-3 · Cited by 245 · see citing works
Olmstead, M. C., & Franklin, K. B. J. (1997) · Behavioral Neuroscience · doi:10.1037/0735-7044.111.6.1324 · Cited by 231 · see citing works
Olmstead, M. C., & Franklin, K. B. J. (1997) · Behavioral Neuroscience · doi:10.1037//0735-7044.111.6.1324 · Cited by 216 · see citing works
Hoffman, A. F., & Lupica, C. R. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.85.1.72 · Cited by 194 · see citing works
Place Conditioning: A Simple and Effective Method for Assessing the Motivational Properties of Drugs
van der Kooy, D. (1987) · Springer eBooks · doi:10.1007/978-1-4612-4812-5_13 · Cited by 176 · see citing works
Sinclair, J. D. (2001) · Alcohol and Alcoholism · doi:10.1093/alcalc/36.1.2 · Cited by 175 · see citing works
Opiate antagonists reduce cocaine but not nicotine self-administration
Corrigall, W. A., & Coen, K. M. (1991) · Psychopharmacology · doi:10.1007/bf02244173 · Cited by 156 · see citing works
Bozarth, M. A. (1987) · Brain Research · doi:10.1016/0006-8993(87)91327-8 · Cited by 133 · see citing works
Nader, K., & van der Kooy, D. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-01-00383.1997 · Cited by 133 · see citing works
Negus, S. S., Henriksen, S. J., Mattox, A., Pasternak, G. W., Portoghese, P. S., Takemori, A. E., Weinger, M. B., & Koob, G. F. (1993) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)38246-7 · Cited by 130 · see citing works
Naloxone attenuation of sham feeding is modified by manipulation of sucrose concentration
Kirkham, T. C., & Cooper, S. J. (1988) · Physiology & Behavior · doi:10.1016/0031-9384(88)90310-1 · Cited by 125 · see citing works
Bardo, M. T., Valone, J. M., & Bevins, R. A. (1999) · Psychopharmacology · doi:10.1007/s002130050917 · Cited by 119 · see citing works
Ikemoto, S., Murphy, J. M., & McBride, W. J. H. (1997) · Behavioral Neuroscience · doi:10.1037//0735-7044.111.2.369 · Cited by 117 · see citing works
Arnt, J., & Scheel‐Krüger, J. (1979) · Life Sciences · doi:10.1016/0024-3205(79)90402-8 · Cited by 106 · see citing works
Regional Differences Within the Rat Ventral Tegmental Area for Muscimol Self-Infusions
Ikemoto, S., Murphy, J. M., & McBride, W. J. H. (1998) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(98)00086-0 · Cited by 104 · see citing works
Carlezon, W. A., Haile, C. N., Coppersmith, R., Hayashi, Y., Malinow, R., Neve, R. L., & Nestler, E. J. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-05-j0002.2000 · Cited by 98 · cited 2× · see citing works
“An additional line of evidence implicating functional heterogeneity of the VTA is that overexpression of the AMPA receptor subunit in the anterior VTA enhances the rewarding effects of systemic morphine, whereas overexpression in the posterior VTA establishes aversive effects of systemic morphine (Carlezon et al., 200…”
BackgroundJenck, F., Gratton, A. P., & Wise, R. A. (1987) · Brain Research · doi:10.1016/0006-8993(87)90821-3 · Cited by 85 · see citing works
Effects of naltrexone on food preference and concurrent behavioral responses in food-deprived rats
Cooper, S. J., & Turkish, S. (1989) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(89)90422-x · Cited by 80 · see citing works
Stinus, L., Winnock, M., & Kelley, A. E. (1985) · Psychopharmacology · doi:10.1007/bf00428196 · Cited by 79 · see citing works
Dissociation of analgesic and rewarding effects of endomorphin-1 in rats
Wilson, A. M., Soignier, R. D., Zadina, J. E., Kastin, A. J., Nores, W. L., Olson, R. D., & Olson, G. A. (2000) · Peptides · doi:10.1016/s0196-9781(00)00340-5 · Cited by 76 · see citing works
Welzl, H., Kuhn, H. G., & Huston, J. P. (1989) · Neuropharmacology · doi:10.1016/0028-3908(89)90112-3 · Cited by 70 · see citing works
Schildein, S., Ågmo, A., Huston, J. P., & Schwarting, R. K. W. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00062-6 · Cited by 68 · see citing works
Johnson, K., Churchill, L., Klitenick, M. A., Hooks, M. S., & Kalivas, P. W. (1996) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)12900-5 · Cited by 63 · see citing works
Péter, A., Tóth, G., Tömböly, C., Laus, G., & Tourwé, D. A. (1999) · Journal of Chromatography A · doi:10.1016/s0021-9673(99)00146-6 · Cited by 57 · see citing works
Involvement of Opioid μ1 Receptors in Morphine-Induced Conditioned Place Preference In Rats
Piepponen, P. T. (1997) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(96)00567-9 · Cited by 49 · see citing works
Ikemoto, S., & Sharpe, L. G. (2001) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(01)00428-9 · Cited by 46 · see citing works
Localization of the reward-relevant opiate receptors.
Bozarth, M. A., & Wise, R. A. (1982) · PsycEXTRA Dataset · doi:10.1037/e472782004-001 · Cited by 42 · see citing works
Churchill, L., & Kalivas, P. W. (1992) · Synapse · doi:10.1002/syn.890110107 · Cited by 38 · see citing works
Churchill, L., Klitenick, M. A., & Kalivas, P. W. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-19-08074.1998 · Cited by 28 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Ikemoto, S. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.05.004 · Cited by 1,477 · see citing works
Tzschentke, T. M. (2007) · Addiction Biology · doi:10.1111/j.1369-1600.2007.00070.x · Cited by 1,336 · see citing works
Reward Processing by the Opioid System in the Brain
Le Merrer, J., Becker, J. A. J., Befort, K., & Kieffer, B. L. (2009) · Physiological Reviews · doi:10.1152/physrev.00005.2009 · Cited by 1,013 · see citing works
Wise, R. A. (2002) · Neuron · doi:10.1016/s0896-6273(02)00965-0 · Cited by 881 · 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
Brain reward circuitry beyond the mesolimbic dopamine system: a neurobiological theory
Ikemoto, S. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.02.001 · Cited by 454 · see citing works
Role of brain dopamine in food reward and reinforcement
Wise, R. A. (2006) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2006.1854 · Cited by 436 · 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
Wise, R. A., & Robble, M. A. (2020) · Annual Review of Psychology · doi:10.1146/annurev-psych-010418-103337 · Cited by 418 · see citing works
The Ventral Pallidum and Hedonic Reward: Neurochemical Maps of Sucrose “Liking” and Food Intake
Smith, K. S., & Berridge, K. C. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1902-05.2005 · Cited by 391 · see citing works
Glutamatergic neurons are present in the rat ventral tegmental area
Yamaguchi, T., Sheen, W., & Morales, M. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05263.x · Cited by 367 · see citing works
Afferents to the GABAergic tail of the ventral tegmental area in the rat
Kaufling, J., Veinante, P., Pawlowski, S. A., Freund‐Mercier, M., & Barrot, M. (2009) · Journal of Comparative Neurology · doi:10.1002/cne.21983 · Cited by 347 · see citing works
Inactivation of the Interoceptive Insula Disrupts Drug Craving and Malaise Induced by Lithium
Contreras, M., Ceric, F., & Torrealba, F. (2007) · Science · doi:10.1126/science.1145590 · Cited by 297 · see citing works
Forebrain substrates of reward and motivation
Wise, R. A. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20689 · Cited by 292 · see citing works
The Endomorphin System and Its Evolving Neurophysiological Role
Fichna, J., Janecka, A. E., Costentin, J., & do-Rego, J.-C. (2007) · Pharmacological Reviews · doi:10.1124/pr.59.1.3 · Cited by 249 · see citing works
Lessons in exercise neurobiology: the case of endorphins.
Dishman, R. K., & O'Connor, P. J. (2009) · Mental health and physical activity · doi:10.1016/j.mhpa.2009.01.002 · Cited by 243 · 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
Critical assessment of how to study addiction and its treatment: Human and non-human animal models
O’Brien, C. P., & Gardner, E. L. (2005) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2005.06.018 · Cited by 221 · see citing works
Braking Dopamine Systems: A New GABA Master Structure for Mesolimbic and Nigrostriatal Functions
Barrot, M., Sesack, S. R., Georges, F. E., Pistis, M., Hong, S., & Jhou, T. C. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.3370-12.2012 · Cited by 215 · 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
Liechti, M. E., Lhuillier, L., Kaupmann, K., & Markou, A. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.1766-07.2007 · Cited by 193 · see citing works
Kritzer, M., & Creutz, L. M. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.2637-08.2008 · Cited by 180 · see citing works
Olson, V. G. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0345-05.2005 · Cited by 186 · see citing works
Two brain sites for cannabinoid reward
Zangen, A., Solinas, M., Ikemoto, S., Goldberg, S. R., & Wise, R. A. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.3554-05.2006 · Cited by 174 · 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
Topographical organization of GABAergic neurons within the ventral tegmental area of the rat
Olson, V. G., & Nestler, E. J. (2006) · Synapse · doi:10.1002/syn.20345 · Cited by 170 · see citing works
Ikemoto, S., Qin, M., & Liu, Z.-H. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.4542-05.2006 · Cited by 151 · see citing works
Mapping of chemical trigger zones for reward
Ikemoto, S., & Wise, R. A. (2004) · Neuropharmacology · doi:10.1016/j.neuropharm.2004.07.012 · Cited by 137 · see citing works
Ikemoto, S., & Bonci, A. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.04.031 · Cited by 122 · see citing works
Neurobiological Mechanisms of Nicotine Reward and Aversion
Wills, L. P., Ables, J. L., Braunscheidel, K. M., Caligiuri, S. P. B., Elayouby, K. S., Fillinger, C., Ishikawa, M., Moen, J. K., & Kenny, P. J. (2022) · Pharmacological Reviews · doi:10.1124/pharmrev.121.000299 · Cited by 126 · see citing works
Ikemoto, S., Qin, M., & Liu, Z. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0892-05.2005 · Cited by 120 · 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
Ikemoto, S., & Wise, R. A. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-22-09895.2002 · Cited by 116 · see citing works
Zhao-Shea, R., Liu, L., Soll, L. G., Improgo, M. R., Meyers, E. E., McIntosh, J. M., Grady, S. R., Marks, M. J., Gardner, P. D., & Tapper, A. R. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.240 · Cited by 113 · see citing works
The antero-posterior heterogeneity of the ventral tegmental area
Sánchez-Catalán, M. J., Kaufling, J., Georges, F. E., Veinante, P., & Barrot, M. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.09.025 · Cited by 112 · 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
Butovsky, E., Juknat, A., Goncharov, I., Elbaz, J., Eilam, R., Zangen, A., & Vogel, Z. (2005) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2005.03074.x · Cited by 105 · see citing works
Ferreira, J. G. P., Del-Fava, F., Hasue, R. H., & Shammah‐Lagnado, S. J. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.02.003 · Cited by 101 · see citing works
The role of motivation and reward neural systems in vocal communication in songbirds
Riters, L. V. (2012) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2012.04.002 · Cited by 100 · see citing works
Dual Roles of Dopamine in Food and Drug Seeking: The Drive-Reward Paradox
Wise, R. A. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.09.001 · Cited by 95 · 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
Persistent Adaptations in Afferents to Ventral Tegmental Dopamine Neurons after Opiate Withdrawal
Kaufling, J., & Aston‐Jones, G. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.0715-15.2015 · Cited by 89 · see citing works
Lorcaserin Suppresses Oxycodone Self-Administration and Relapse Vulnerability in Rats
Neelakantan, H., Holliday, E. D., Fox, R. G., Stutz, S. J., Comer, S. D., Haney, M., Anastasio, N. C., Moeller, F. G., & Cunningham, K. A. (2017) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.6b00413 · Cited by 90 · see citing works
Margolis, E. B., Fields, H. L., Hjelmstad, G. O., & Mitchell, J. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.4569-08.2008 · Cited by 87 · see citing works
Solinas, M., Zangen, A., Thiriet, N., & Goldberg, S. R. (2004) · European Journal of Neuroscience · doi:10.1111/j.0953-816x.2004.03420.x · Cited by 83 · see citing works
Nikulina, E. M., Arrillaga‐Romany, I., Miczek, K. A., & Hammer, R. P. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06176.x · Cited by 81 · 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
Rodd, Z. A., Bell, R. L., Kuc, K. A., Zhang, Y., Murphy, J. M., & McBride, W. J. (2005) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.104.075952 · Cited by 72 · see citing works
Steidl, S., Wasserman, D., Blaha, C. D., & Yeomans, J. S. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.09.022 · Cited by 72 · see citing works
Opioid–galanin receptor heteromers mediate the dopaminergic effects of opioids
Cai, N.-S., Quiroz, C., Bonaventura, J., Bonifazi, A., Cole, T. O., Purks, J., Billing, A. S., Massey, E. C., Wagner, M., Wish, E. D., et al. (2019) · Journal of Clinical Investigation · doi:10.1172/jci126912 · Cited by 71 · see citing works
Jordan, C. J., Cao, J., Newman, A. H., & Xi, Z. (2019) · Neuropharmacology · doi:10.1016/j.neuropharm.2019.04.015 · Cited by 70 · see citing works
Shabat-Simon, M., Levy, D. J., Amir, A., Rehavi, M., & Zangen, A. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1958-08.2008 · Cited by 70 · see citing works
Kaufling, J., Waltisperger, E., Bourdy, R., Valera, A. M., Veinante, P., Freund‐Mercier, M. J., & Barrot, M. (2010) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2010.00984.x · Cited by 66 · see citing works
Jhou, T. C., Xu, S., Lee, M. R., Gallen, C. L., & Ikemoto, S. (2012) · Psychopharmacology · doi:10.1007/s00213-012-2753-6 · Cited by 64 · see citing works
Smith, R. J., Vento, P. J., Chao, Y. S., Good, C. H., & Jhou, T. C. (2018) · Brain Structure and Function · doi:10.1007/s00429-018-1761-7 · Cited by 58 · see citing works
Galaj, E., Newman, A. H., & Xi, Z. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.04.024 · Cited by 56 · see citing works
Ikemoto, S., Witkin, B. M., Zangen, A., & Wise, R. A. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.5367-04.2004 · Cited by 56 · see citing works
Yang, C. H., Yoon, S. S., Hansen, D. M., Wilcox, J. D., Blumell, B. R., Park, J. J., & Steffensen, S. C. (2010) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2010.01310.x · Cited by 55 · see citing works
Sánchez-Catalán, M. J., Hipólito, L., Zornoza, T., Polache, A., & Granero, L. M. (2009) · Psychopharmacology · doi:10.1007/s00213-009-1495-6 · Cited by 48 · see citing works
McGovern, D. J., Polter, A. M., Prévost, E. D., Ly, A., McNulty, C. J., Rubinstein, B., & Root, D. H. (2023) · Neuropsychopharmacology · doi:10.1038/s41386-023-01637-w · Cited by 49 · see citing works
Functional μ-Opioid-Galanin Receptor Heteromers in the Ventral Tegmental Area
Moreno, E., Quiroz, C., Rea, W. P., Cai, N.-S., Mallol, J., Cortés, A., Lluı́s, C., Canela, E. I., Casadó, V., & Ferré, S. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.2442-16.2016 · Cited by 44 · see citing works
Endogenous opiates and behavior: 2002
Bodnar, R. J., & Hadjimarkou, M. M. (2003) · Peptides · doi:10.1016/j.peptides.2003.08.002 · Cited by 59 · see citing works
Motor skill learning and reward consumption differentially affect VTA activation
Leemburg, S., Canonica, T., & Luft, A. R. (2018) · Scientific Reports · doi:10.1038/s41598-017-18716-w · Cited by 38 · see citing works
Piray, P., Keramati, M., Dezfouli, A., Lucas, C., & Mokri, A. (2010) · Neural Computation · doi:10.1162/neco_a_00009 · Cited by 39 · see citing works
Gazit, T., Friedman, A., Lax, E., Bruchim-Samuel, M., Zahut, R., Katz, M., Abraham, L., Tischler, H., Teicher, M., & Yadid, G. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.12.003 · Cited by 39 · see citing works
David, V., Ségu, L., Buhot, M.-C., Ichaye, M., & Cazala, P. (2004) · Psychopharmacology · doi:10.1007/s00213-003-1767-5 · Cited by 39 · see citing works
Terashvili, M., Wu, H.-E., Leitermann, R. J., Hung, K.-C., Clithero, A. D., Schwasinger, E. T., & Tseng, L. F. (2004) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.103.059287 · Cited by 37 · see citing works
García‐Pérez, D., López-Bellido, R., Hidalgo, J. M., Rodrı́guez, R. E., Laorden, M. L., Núñez, C., & Milanés, M. V. (2013) · Addiction Biology · doi:10.1111/adb.12083 · Cited by 34 · see citing works
Greenwell, T. N., Martin‐Schild, S., Inglis, F. M., & Zadina, J. E. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21374 · Cited by 33 · see citing works
Potential for Kappa-Opioid Receptor Agonists to Engineer Nonaddictive Analgesics: A Narrative Review
Kaski, S. W., White, A., Gross, J., & Siderovski, D. P. (2020) · Anesthesia & Analgesia · doi:10.1213/ane.0000000000005309 · Cited by 32 · see citing works
Zangen, A., & Shalev, U. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02509.x · Cited by 32 · see citing works
Petzel, A., Bernard, R., Poller, W. C., & Veh, R. W. (2017) · The Journal of Comparative Neurology · doi:10.1002/cne.24200 · Cited by 31 · see citing works
Zhang, J., Song, C., Dai, J., Li, L., Yang, X., & Chen, Z. (2022) · MedComm · doi:10.1002/mco2.148 · Cited by 29 · see citing works
Ikemoto, S., Witkin, B. M., & Morales, M. (2003) · Brain Research · doi:10.1016/s0006-8993(03)02280-7 · Cited by 30 · see citing works
Levinstein, M. R., de Oliveira, P. A., Casajuana-Martín, N., Quiroz, C., Budinich, R. C., Rais, R., Rea, W. P., Ventriglia, E. N., Llopart, N., Casadó-Anguera, V., et al. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02353-z · Cited by 27 · see citing works
Operant self-administration of ethanol in C57BL/6 mice lacking ?-endorphin and enkephalin
HAYWARD, M., Hansen, S. T., Pintar, J. E., & Low, M. J. (2004) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2004.07.002 · Cited by 28 · see citing works
Progress in opioid reward research: From a canonical two-neuron hypothesis to two neural circuits
Galaj, E., & Xi, Z. (2020) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2020.173072 · Cited by 29 · see citing works
Somalwar, A. R., Shelkar, G. P., Subhedar, N. K., & Kokare, D. M. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.09.054 · Cited by 26 · see citing works
Beloate, L. N., & Coolen, L. M. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.10.024 · Cited by 25 · see citing works
Walker, B. M., & Ettenberg, A. (2005) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2005.10.002 · Cited by 25 · see citing works
Greenwell, T. N., Zangen, A., Martin‐Schild, S., Wise, R. A., & Zadina, J. E. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10464 · Cited by 24 · see citing works
García‐Pérez, D., López-Bellido, R., Rodrı́guez, R. E., Laorden, M. L., Núñez, C., & Milanés, M. V. (2014) · Brain Structure and Function · doi:10.1007/s00429-014-0761-5 · Cited by 23 · see citing works
Morzorati, S. L., Marunde, R. L., & Downey, D. (2010) · Alcohol · doi:10.1016/j.alcohol.2010.02.009 · Cited by 21 · see citing works
Terashvili, M., Wu, H.-E., Schwasinger, E. T., Hung, K.-C., Hong, J., & Tseng, L. F. (2008) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2008.03.020 · Cited by 19 · see citing works
Ding, Z., Liu, W., Engleman, E. A., Rodd, Z. A., & McBride, W. J. (2009) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2009.01.004 · Cited by 19 · see citing works
Wang, B., You, Z., & Wise, R. A. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2012.167 · Cited by 17 · see citing works
Chiurchiù, V., Izzi, V., D’Aquilio, F., Vismara, D., Carotenuto, F., Catanzaro, G., & Maccarrone, M. (2010) · Peptides · doi:10.1016/j.peptides.2010.09.024 · Cited by 18 · see citing works
Opposite conditioned place preference responses to endomorphin-1 and endomorphin-2 in the mouse
Wu, H.-E., MacDougall, R. S., Clithero, A. D., Leitermann, R. J., Terashvili, M., & Tseng, L. F. (2004) · Neuroscience Letters · doi:10.1016/j.neulet.2004.03.093 · Cited by 18 · see citing works
Off the Beaten Path: Drug Addiction and the Pontine Laterodorsal Tegmentum
Kohlmeier, K. A. (2013) · ISRN Neuroscience · doi:10.1155/2013/604847 · Cited by 17 · see citing works
Upadhyay, J., Verrico, C. D., Cay, M., Kodele, S., Yammine, L., Koob, G. F., & Schreiber, R. (2021) · The Lancet Psychiatry · doi:10.1016/s2215-0366(21)00008-0 · Cited by 17 · see citing works
Supraspinal anti-allodynic and rewarding effects of endomorphins in rats
Huang, E. Y., Chen, C.-M., & Tao, P. (2004) · Peptides · doi:10.1016/j.peptides.2004.02.009 · Cited by 16 · see citing works
Mu Opioid Receptor Mediated Analgesia and Reward
Fields, H. L. (2010) · Humana Press eBooks · doi:10.1007/978-1-60761-993-2_10 · Cited by 14 · see citing works
Huang, A. C. W., Shyu, B., & Hsiao, S. (2010) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2010.02.003 · Cited by 14 · see citing works
Steidl, S., Myal, S. E., & Wise, R. A. (2015) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2015.04.006 · Cited by 14 · see citing works
Ahmad, T., & Laviolette, S. R. (2017) · Psychopharmacology · doi:10.1007/s00213-017-4669-7 · Cited by 13 · see citing works
Stress, Opioid Peptides, and Their Receptors
Przewłocki, R. (2009) · Elsevier eBooks · doi:10.1016/b978-008088783-8.00008-5 · Cited by 13 · see citing works
The antitussive effects of endomorphin-1 and endomorphin-2 in mice
Kamei, J., Morita, K., Saitoh, A., & Nagase, H. (2003) · European Journal of Pharmacology · doi:10.1016/s0014-2999(03)01634-0 · Cited by 12 · see citing works
Ikemoto, S. (2004) · Psychopharmacology · doi:10.1007/s00213-003-1651-3 · Cited by 11 · see citing works
Bujdosó, E., Jászberényi, M., Gardi, J., Földesi, I., & Telegdy, G. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00241-0 · Cited by 11 · see citing works
- Authors
- Zangen, A., Ikemoto, S., Zadina, J. E., & Wise, R. A.
- Affiliations
- National Institutes of Health (US)
- Tulane University (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2002-08-15
- Volume
- 22
- Issue
- 16
- Pages
- 7225-7233
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6757872
- OpenAlex
- W1888155279
- Cited by
- 138
- References
- 47
- Citations by year
- 2026: 4 · 2025: 2 · 2023: 4 · 2022: 2 · 2021: 2 · 2020: 7 · 2019: 4 · 2018: 3 · 2017: 9 · 2016: 4 · 2015: 6 · 2014: 3 · 2013: 5 · 2012: 11
- FWCI
- 3.15
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute on Drug Abuse
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Keywords
- endomorphin-1, opioid reward, ventral tegmental area, nucleus accumbens, mu-opioid receptor, conditioned place preference, locomotor activity, reinstatement, opioid analgesia
- MeSH terms
- Animals, Behavior, Animal, Choice Behavior, Dose-Response Relationship, Drug, Drug Administration Routes, Male, Microinjections, Motor Activity, Nucleus Accumbens, Oligopeptides, Reinforcement, Psychology, Reward, Self Administration, Spatial Behavior, Rats, Sprague-Dawley, Receptors, Opioid, mu, Ventral Tegmental Area, Rats
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