Increased probability of GABA release during withdrawal from morphine
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Opioid receptors located on interneurons in the ventral tegmental area (VTA) inhibit GABA A -mediated synaptic transmission to dopamine projection neurons. The resulting disinhibition of dopamine cells in the VTA is thought to play a pivotal role in drug abuse; however, little is known about how this GABA A synapse is affected after chronic morphine treatment. The regulation of GABA release during acute withdrawal from morphine was studied in slices from animals treated for 6–7 d with morphine. Slices containing the VTA were prepared and maintained in morphine-free solutions, and GABA A IPSCs were recorded from dopamine cells. The amplitude of evoked IPSCs and the frequency of spontaneous miniature IPSCs measured in slices from morphine-treated guinea pigs were greater than placebo-treated controls. In addition, activation of adenylyl cyclase, with forskolin, and cAMP-dependent protein kinase, with Sp-cAMPS, caused a larger increase in IPSCs in slices from morphine-treated animals. Conversely, the kinase inhibitors staurosporine and Rp-CPT-cAMPS decreased GABA IPSCs to a greater extent after drug treatment. The results indicate that the probability of GABA release was increased during withdrawal from chronic morphine treatment and that this effect resulted from an upregulation of the cAMP-dependent cascade. Increased transmitter release from opioid-sensitive synapses during acute withdrawal may be one adaptive mechanism that results from prolonged morphine treatment.
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Chronic opioid-induced cAMP-dependent increase in the probability of GABA release in the VTA would inhibit dopamine neurons.
“A prominent observation is a chronic opioid-induced cAMP-dependent increase in the probability of GABA release in the VTA, which would inhibit dopamine neurons (Bonci and Williams, 1997).”
From Drug Addiction: Hyperkatifeia/Negative Reinforcement as a Framework for Medications Development (2021) · cites this paper as Bonci and Williams, 1997
Cites
Wise, R. A., & Rompre, P.-P. (1989) · Annual Review of Psychology · doi:10.1146/annurev.ps.40.020189.001203 · Cited by 1,968 · 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
Aghajanian, G. K. (1978) · Nature · doi:10.1038/276186a0 · Cited by 803 · see citing works
Local and diffuse synaptic actions of GABA in the hippocampus
Isaacson, J. S., Solis, J. M., & Nicoll, R. A. (1993) · Neuron · doi:10.1016/0896-6273(93)90308-e · Cited by 688 · 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
Dual regulation of adenylate cyclase accounts for narcotic dependence and tolerance.
Sharma, S. K., Klee, W. A., & Nirenberg, M. W. (1975) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.72.8.3092 · Cited by 671 · see citing works
Molecular Mechanisms of Drug Reinforcement and Addiction
Self, D. W., & Nestler, E. J. (1995) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.18.030195.002335 · Cited by 565 · see citing works
Drug addiction: A model for the molecular basis of neural plasticity
Nestler, E. J., Hope, B. T., & Widnell, K. L. (1993) · Neuron · doi:10.1016/0896-6273(93)90213-b · Cited by 544 · see citing works
Terwilliger, R. Z., Beitner‐Johnson, D., Sevarino, K. A., Crain, S. M., & Nestler, E. J. (1991) · Brain Research · doi:10.1016/0006-8993(91)91111-d · Cited by 534 · 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
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
Cyclic AMP Mediates a Presynaptic Form of LTP at Cerebellar Parallel Fiber Synapses
Salin, P. A., Malenka, R. C., & Nicoll, R. A. (1996) · Neuron · doi:10.1016/s0896-6273(00)80099-9 · Cited by 439 · see citing works
Rosenmund, C., Carr, D. W., Bergeson, S. E., Nilaver, G., Scott, J. D., & Westbrook, G. L. (1994) · Nature · doi:10.1038/368853a0 · Cited by 371 · see citing works
Enkephalin blocks inhibitory pathways in the vertebrate CNS
Nicoll, R. A., Alger, B. E., & Jahr, C. E. (1980) · Nature · doi:10.1038/287022a0 · Cited by 333 · see citing works
Enkephalin hyperpolarizes interneurones in the rat hippocampus.
Madison, D. V., & Nicoll, R. A. (1988) · The Journal of Physiology · doi:10.1113/jphysiol.1988.sp017033 · Cited by 292 · see citing works
Duman, R. S., Tallman, J. F., & Nestler, E. J. (1988) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)22179-6 · Cited by 282 · see citing works
Akaoka, H., & Aston‐Jones, G. (1991) · Journal of Neuroscience · doi:10.1523/jneurosci.11-12-03830.1991 · Cited by 266 · see citing works
Cellular mechanisms of opioid tolerance: studies in single brain neurons.
Christie, M. J., Williams, J. T., & NORTH, R. A. (1987) · Molecular Pharmacology · doi:10.1016/s0026-895x(25)13048-4 · Cited by 264 · see citing works
Self-citationDopamine D1 receptors facilitate transmitter release
Cameron, D. L., & Williams, J. T. (1993) · Nature · doi:10.1038/366344a0 · Cited by 263 · see citing works
Self-citation5-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
Opioid inhibition of GABA release from presynaptic terminals of rat hippocampal interneurons.
Cohen, G. A., Doze, V., & Madison, D. (1992) · Neuron · doi:10.1016/0896-6273(92)90171-9 · Cited by 244 · see citing works
Nestler, E. J., & Tallman, J. F. (1988) · Molecular Pharmacology · doi:10.1016/s0026-895x(25)13123-4 · Cited by 235 · see citing works
Bonci, A., & Williams, J. T. (1996) · Neuron · doi:10.1016/s0896-6273(00)80082-3 · Cited by 228 · see citing works
Self-citationInvolvement of D2 dopamine receptors in the nucleus accumbens in the opiate withdrawal syndrome
Harris, G. C., & Aston‐Jones, G. (1994) · Nature · doi:10.1038/371155a0 · Cited by 214 · see citing works
Cocaine inhibits GABA release in the VTA through endogenous 5-HT
Cameron, D., & Williams, J. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-11-06763.1994 · Cited by 188 · see citing works
Self-citationJohnson, S. M., & Fleming, W. W. (1989) · Pharmacological Reviews · doi:10.1016/s0031-6997(25)00035-3 · Cited by 175 · see citing works
Mennerick, S. J., & Zorumski, C. F. (1995) · The Journal of Physiology · doi:10.1113/jphysiol.1995.sp020948 · Cited by 171 · see citing works
Profound decrease of mesolimbic dopaminergic neuronal activity in morphine withdrawn rats.
Diana, M., Pistis, M., Muntoni, A. L., & Gessa, G. L. (1995) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)24484-6 · Cited by 170 · see citing works
Wimpey, T. L., & Chavkin, C. (1991) · Neuron · doi:10.1016/0896-6273(91)90363-5 · Cited by 141 · see citing works
Morphine tolerance and dependence in the locus coeruleus: Single cell studies in brain slices
Andrade, R., VanderMaelen, C. P., & Aghajanian, G. K. (1983) · European Journal of Pharmacology · doi:10.1016/0014-2999(83)90461-2 · Cited by 139 · see citing works
Kogan, J. H., Nestler, E. J., & Aghajanian, G. K. (1992) · European Journal of Pharmacology · doi:10.1016/0014-2999(92)90261-2 · Cited by 128 · see citing works
Opioid receptor reserve in normal and morphine-tolerant guinea pig ileum myenteric plexus
Chavkin, C., & Goldstein, A. (1984) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.81.22.7253 · Cited by 128 · see citing works
Law, P., Hom, D. S., & Loh, H. H. (1982) · Molecular Pharmacology · doi:10.1016/s0026-895x(25)14943-2 · Cited by 126 · see citing works
Chieng, B. C. H., & Christie, M. J. (1994) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.1994.tb16183.x · Cited by 125 · see citing works
Puttfarcken, P. S., Werling, L. L., & Cox, B. M. (1988) · Molecular Pharmacology · doi:10.1016/s0026-895x(25)13363-4 · Cited by 118 · see citing works
Regulation of Cyclic AMP by the μ‐Opioid Receptor in Human Neuroblastoma SH‐SY5Y Cells
Yu, V. C. K., Eiger, S. M., Duan, D. S., Lameh, J., & Sadée, W. (1990) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1990.tb03151.x · Cited by 101 · see citing works
Local Opioid Withdrawal in Rat Single Periaqueductal Gray NeuronsIn Vitro
Chieng, B. C. H., & Christie, M. J. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-22-07128.1996 · Cited by 75 · see citing works
Maren, T. H. (1982) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pa.22.040182.000245 · Cited by 52 · see citing works
Wu, Y., Mercuri, N. B., & Johnson, S. W. (1995) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)09507-2 · Cited by 47 · see citing works
Fry, J. P., Herz, A., & Zieglgänsberger, W. (1980) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.1980.tb14574.x · Cited by 46 · see citing works
Wimpey, T. L., Opheim, K. E., & Chavkin, C. (1989) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)20822-9 · Cited by 42 · see citing works
Kennedy, C., & Henderson, G. (1991) · PubMed · Cited by 38 · see citing works
TUNG, C. ‐., Grenhoff, J., & Svensson, T. H. (1990) · Acta Physiologica Scandinavica · doi:10.1111/j.1748-1716.1990.tb08888.x · Cited by 36 · see citing works
Kennedy, C., & Henderson, G. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90369-d · Cited by 25 · see citing works
Johnson, S. M., & Duggan, A. W. (1981) · Neuropharmacology · doi:10.1016/0028-3908(81)90093-9 · Cited by 25 · see citing works
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Molecular basis of long-term plasticity underlying addiction
Nestler, E. J. (2001) · Nature reviews. Neuroscience · doi:10.1038/35053570 · Cited by 1,857 · see citing works
Is there a common molecular pathway for addiction?
Nestler, E. J. (2005) · Nature Neuroscience · doi:10.1038/nn1578 · Cited by 1,388 · 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
Self-citationWaldhoer, M., Bartlett, S. E., & Whistler, J. L. (2004) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.73.011303.073940 · Cited by 740 · see citing works
Activation of VTA GABA Neurons Disrupts Reward Consumption
van Zessen, R., Phillips, J. L., Budygin, E. A., & Stuber, G. D. (2012) · Neuron · doi:10.1016/j.neuron.2012.02.016 · Cited by 609 · see citing works
Scofield, M. D., Heinsbroek, J. A., Gipson, C. D., Kupchik, Y. M., Spencer, S., Smith, A. C. W., Roberts-Wolfe, D., & Kalivas, P. W. (2016) · Pharmacological Reviews · doi:10.1124/pr.116.012484 · Cited by 598 · 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
Guidelines for the psychosocially assisted pharmacological treatment of opioid dependence
Uchtenhagen, A. (2009) · Zurich Open Repository and Archive (University of Zurich) · doi:10.5167/uzh-17408 · Cited by 487 · 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
Melis, M., Pistis, M., Perra, S., Muntoni, A. L., Pillolla, G., & Gessa, G. L. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.4503-03.2004 · Cited by 478 · see citing works
Neurobiology of opioid addiction: Opponent process, hyperkatifeia, and negative reinforcement
Koob, G. F. (2020) · Biological Psychiatry · doi:10.1016/j.biopsych.2019.05.023 · Cited by 477 · see citing works
Opioid dependence and addiction during opioid treatment of chronic pain
Ballantyne, J. C., & LaForge, S. K. (2007) · Pain · doi:10.1016/j.pain.2007.03.028 · Cited by 445 · see citing works
Historical review: molecular and cellular mechanisms of opiate and cocaine addiction
Nestler, E. J. (2004) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2004.02.005 · Cited by 425 · see citing works
Molecular Neurobiology of Addiction
Nestler, E. J. (2001) · American Journal on Addictions · doi:10.1080/105504901750532094 · Cited by 412 · see citing works
Regulation of Opioid Receptor Trafficking and Morphine Tolerance by Receptor Oligomerization
He, L., Fong, J. C., von Zastrow, M., & Whistler, J. L. (2002) · Cell · doi:10.1016/s0092-8674(02)00613-x · Cited by 340 · see citing works
Properties and opioid inhibition of mesolimbic dopamine neurons vary according to target location
Ford, C. P., Mark, G. P., & Williams, J. T. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.4331-05.2006 · Cited by 339 · see citing works
Self-citationDrug Addiction: Hyperkatifeia/Negative Reinforcement as a Framework for Medications Development
Koob, G. F. (2021) · Pharmacological Reviews · doi:10.1124/pharmrev.120.000083 · Cited by 337 · see citing works
Roberto, M., Schweitzer, P., Madamba, S. G., Stouffer, D. G., Parsons, L. H., & Siggins, G. R. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.5077-03.2004 · Cited by 312 · see citing works
Increased GABA Release in the Central Amygdala of Ethanol-Dependent Rats
Roberto, M., Madamba, S. G., Stouffer, D. G., Parsons, L. H., & Siggins, G. R. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.3004-04.2004 · Cited by 299 · see citing works
Endocytosis of the Mu Opioid Receptor Reduces Tolerance and a Cellular Hallmark of Opiate Withdrawal
Finn, A. K., & Whistler, J. L. (2001) · Neuron · doi:10.1016/s0896-6273(01)00517-7 · Cited by 285 · see citing works
Chen, K., Baram, T., & Soltesz, I. (1999) · Nature Medicine · doi:10.1038/11330 · Cited by 337 · see citing works
The Dopamine Hypothesis of Drug Addiction: Hypodopaminergic State
Melis, M., Spiga, S., & Diana, M. (2005) · International review of neurobiology · doi:10.1016/s0074-7742(05)63005-x · Cited by 271 · see citing works
Pain and Poppies: The Good, the Bad, and the Ugly of Opioid Analgesics
Trang, T., Al‐Hasani, R., Salvemini, D., Salter, M. W., Gutstein, H. B., & Cahill, C. M. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.2711-15.2015 · Cited by 277 · see citing works
Pu, L., Bao, G., Xu, N., Ma, L., & Pei, G. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-05-01914.2002 · Cited by 242 · see citing works
The endogenous opioid system: A common substrate in drug addiction
Trigo, J. M., Martín‐García, E., Berrendero, F., Robledo, P., & Maldonado, R. J. (2009) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2009.10.011 · Cited by 240 · 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
Self-citationAnhedonia and Substance Dependence: Clinical Correlates and Treatment Options
Hatzigiakoumis, D. S., Martinotti, G., Giannantonio, M. D., & Janiri, L. (2011) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2011.00010 · Cited by 238 · see citing works
The role of mu opioid receptor desensitization and endocytosis in morphine tolerance and dependence
Martini, L., & Whistler, J. L. (2007) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2007.10.004 · Cited by 234 · see citing works
Nucleus Accumbens Medium Spiny Neurons Target Non-Dopaminergic Neurons in the Ventral Tegmental Area
Xia, Y., Driscoll, J. R., Wilbrecht, L., Margolis, E. B., Fields, H. L., & Hjelmstad, G. O. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.1504-11.2011 · Cited by 218 · see citing works
Role of NMDA Receptors in Dopamine Neurons for Plasticity and Addictive Behaviors
Zweifel, L. S., Argilli, E., Bonci, A., & Palmiter, R. D. (2008) · Neuron · doi:10.1016/j.neuron.2008.05.028 · Cited by 210 · see citing works
Self-citationProtein kinases modulate the cellular adaptations associated with opioid tolerance and dependence
Liu, J. (2001) · Brain Research Reviews · doi:10.1016/s0165-0173(01)00057-1 · Cited by 209 · see citing works
Shaw-Lutchman, T. Z., Barrot, M., Wallace, T. L., Gilden, L., Zachariou, V., Impey, S., Duman, R. S., Storm, D. R., & Nestler, E. J. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-09-03663.2002 · Cited by 205 · see citing works
Laviolette, S. R., Gallegos, R. A., Henriksen, S. J., & van der Kooy, D. (2004) · Nature Neuroscience · doi:10.1038/nn1182 · Cited by 203 · 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
Melis, M., Camarini, R., Ungless, M. A., & Bonci, A. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-06-02074.2002 · Cited by 196 · see citing works
Self-citationMatsui, A., & Williams, J. T. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.4570-11.2011 · Cited by 191 · see citing works
Self-citationLecca, S., Melis, M., Luchicchi, A., Muntoni, A. L., & Pistis, M. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.302 · Cited by 185 · see citing works
Frenois, F., Cador, M., Caillé, S., Stinus, L., & Moine, C. L. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.02187.x · Cited by 179 · see citing works
Khirug, S., Huttu, K., Ludwig, A., Smirnov, S., Voipio, J., Rivera, C., Kaila, K., & Khiroug, L. S. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.03886.x · Cited by 168 · see citing works
McClung, C. A., Nestler, E. J., & Zachariou, V. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0062-05.2005 · Cited by 163 · see citing works
Martinez, D., Saccone, P., Liu, F., Slifstein, M., Orlowska, D., Grassetti, A., Cook, S., Broft, A., Heertum, R. V. V., & Comer, S. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.08.024 · Cited by 153 · see citing works
Enhanced Opioid Efficacy in Opioid Dependence Is Caused by an Altered Signal Transduction Pathway
Ingram, S., Vaughan, C. W., Bagley, E. E., Connor, M. A., & Christie, M. J. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-24-10269.1998 · Cited by 161 · see citing works
The tipsy terminal: presynaptic effects of ethanol.
Siggins, G., Roberto, M., & Nie, Z. (2005) · Pharmacology and Therapeutics · doi:10.1016/j.pharmthera.2005.01.006 · Cited by 167 · see citing works
Presynaptic Regulation of Glutamate Release in the Ventral Tegmental Area During Morphine Withdrawal
Manzoni, O. J., & Williams, J. T. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-15-06629.1999 · Cited by 156 · see citing works
Self-citationMolecular mechanisms of opiate and cocaine addiction
Nestler, E. J. (1997) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(97)80094-3 · Cited by 149 · see citing works
Mechanisms of Action and Persistent Neuroplasticity by Drugs of Abuse
Korpi, E. R., den Hollander, B., Farooq, U., Vashchinkina, E., Rajkumar, R., Nutt, D. J., Hyytiä, P., & Dawe, G. S. (2015) · Pharmacological Reviews · doi:10.1124/pr.115.010967 · Cited by 148 · see citing works
Ozaki, S., Narita, M., Narita, M., Iino, M., Sugita, J., Matsumura, Y., & Suzuki, T. (2002) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2002.01071.x · Cited by 142 · see citing works
Dumont, É. C., & Williams, J. T. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.0425-04.2004 · Cited by 137 · see citing works
Self-citationYe, J. H., Zhang, J., Xiao, C., & Kong, J. (2006) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2006.06.006 · Cited by 136 · see citing works
Loss of Plasticity in the D2-Accumbens Pallidal Pathway Promotes Cocaine Seeking
Heinsbroek, J. A., Neuhofer, D., Griffin, W. C., Siegel, G. S., Bobadilla, A., Kupchik, Y. M., & Kalivas, P. W. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.2659-16.2016 · Cited by 129 · see citing works
Lasting reduction in mesolimbic dopamine neuronal activity after morphine withdrawal
Diana, M., Muntoni, A. L., Pistis, M., Melis, M., & Gessa, G. L. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00488.x · Cited by 132 · see citing works
Chartoff, E. H., & Connery, H. S. (2014) · Frontiers in Pharmacology · doi:10.3389/fphar.2014.00116 · Cited by 128 · see citing works
Narita, M., Kishimoto, Y., Ise, Y., Yajima, Y., Misawa, K., & Suzuki, T. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300527 · Cited by 128 · 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
Ethanol Facilitates Glutamatergic Transmission to Dopamine Neurons in the Ventral Tegmental Area
Xiao, C., Shao, X. M., Olive, M. F., Griffin, W. C., Li, K.-Y., Krnjević, K., Zhou, C., & Ye, J. H. (2008) · Neuropsychopharmacology · doi:10.1038/npp.2008.99 · Cited by 129 · see citing works
Biased signaling by endogenous opioid peptides
Gomes, I., Sierra, S., Lueptow, L. M., Gupta, A., Gouty, S., Margolis, E. B., Cox, B. M., & Devi, L. A. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2000712117 · Cited by 127 · 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
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
Acute Opioid Receptor Desensitization And Tolerance: Is There A Link?
Borgland, S. L. (2001) · Clinical and Experimental Pharmacology and Physiology · doi:10.1046/j.1440-1681.2001.03418.x · Cited by 115 · see citing works
Increased Opioid Inhibition of GABA Release in Nucleus Accumbens during Morphine Withdrawal
Chieng, B. C. H., & Williams, J. T. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-17-07033.1998 · Cited by 112 · see citing works
Self-citationNuman, S., Lane-Ladd, S. B., Zhang, L., Lundgren, K. H., Russell, D., Seroogy, K. B., & Nestler, E. J. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-24-10700.1998 · Cited by 111 · see citing works
Jolas, T., Nestler, E. J., & Aghajanian, G. K. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00436-4 · Cited by 110 · see citing works
Nagai, T., Yamada, K., Yoshimura, M., Ishikawa, K., Miyamoto, Y., Hashimoto, K., Noda, Y., Nitta, A., & Nabeshima, T. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0306587101 · Cited by 110 · see citing works
Taylor, A. M. W., Castonguay, A., Ghogha, A., Vayssiere, P., Pradhan, A. A. A., Xue, L., Mehrabani, S., Wu, J., Levitt, P., Olmstead, M. C., et al. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2015.221 · Cited by 109 · see citing works
Koga, E., & Momiyama, T. (2000) · The Journal of Physiology · doi:10.1111/j.1469-7793.2000.t01-2-00163.x · Cited by 107 · 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
The Role of Opioid Receptor Internalization and ??-Arrestins in the Development of Opioid Tolerance
Zuo, Z. (2005) · Anesthesia & Analgesia · doi:10.1213/01.ane.0000160588.32007.ad · Cited by 103 · see citing works
Cannabinoids inhibit GABAergic synaptic transmission in mice nucleus accumbens
Manzoni, O. J., & Bockaert, J. (2001) · European Journal of Pharmacology · doi:10.1016/s0014-2999(01)00723-3 · Cited by 103 · see citing works
Ye, J.-H., Wang, F., Krnjević, K., Wang, W., Xiong, Z., & Zhang, J. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.2016-04.2004 · Cited by 100 · 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
cAMP-Mediated Mechanisms for Pain Sensitization during Opioid Withdrawal
Bie, B., Peng, Y., Zhang, Y., & Pan, Z. Z. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.5010-04.2005 · Cited by 92 · see citing works
Morphine-Induced Receptor Endocytosis in a Novel Knockin Mouse Reduces Tolerance and Dependence
Kim, J. A., Bartlett, S. E., Li, H., Nielsen, C. K., Chang, A. M., Kharazia, V., Waldhoer, M., Ou, C. J., Taylor, S., Ferwerda, M., et al. (2008) · Current Biology · doi:10.1016/j.cub.2007.12.057 · Cited by 92 · see citing works
Luca, M. A. D., Bimpisidis, Z., Melis, M., Marti, M., Caboni, P., Valentini, V., Margiani, G., Pintori, N., Polis, I. Y., Marsicano, G., et al. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2015.08.041 · Cited by 88 · see citing works
Drug Dependence as a Disorder of Neural Plasticity: Focus on Dopamine and Glutamate
Pulvirenti, L., & Diana, M. (2001) · Reviews in the Neurosciences · doi:10.1515/revneuro.2001.12.2.141 · Cited by 87 · see citing works
Morphine withdrawal‐induced morphological changes in the nucleus accumbens
Spiga, S., Puddu, M. C., Pisano, M., & Diana, M. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04416.x · Cited by 86 · see citing works
Modulation of GABA release during morphine withdrawal in midbrain neurons in vitro
Hack, S. P., Vaughan, C. W., & Christie, M. J. (2003) · Neuropharmacology · doi:10.1016/s0028-3908(03)00205-3 · Cited by 85 · see citing works
Bonci, A., Grillner, P., Mercuri, N. B., & Bernardi, G. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-17-06693.1998 · Cited by 85 · see citing works
Self-citationWetherington, J. P., & Lambert, N. A. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-04-01248.2002 · Cited by 85 · see citing works
Roberto, M., Cruz, M. T., Bajo, M., Siggins, G. R., Parsons, L. H., & Schweitzer, P. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.70 · Cited by 84 · see citing works
An Opiate Cocktail that Reduces Morphine Tolerance and Dependence
Li, H., & Whistler, J. L. (2005) · Current Biology · doi:10.1016/j.cub.2005.04.052 · Cited by 84 · see citing works
Histamine regulates activities of neurons in the ventrolateral preoptic nucleus
Liu, Y.-W., Li, J., & Ye, J.-H. (2010) · The Journal of Physiology · doi:10.1113/jphysiol.2010.193904 · Cited by 81 · see citing works
A Possible Mechanism Underlying the Effectiveness of Acupuncture in the Treatment of Drug Addiction
Yang, C. H., Lee, B. H., & Sohn, S. H. (2007) · Evidence-based Complementary and Alternative Medicine · doi:10.1093/ecam/nem081 · Cited by 81 · see citing works
Ballantyne, J. C., & Sullivan, M. D. (2017) · Pain · doi:10.1097/j.pain.0000000000001043 · Cited by 79 · see citing works
Regulation of Lateral Hypothalamic Orexin Activity by Local GABAergic Neurons
Ferrari, L. L., Park, D., Zhu, L., Palmer, M. R., Broadhurst, R. Y., & Arrigoni, E. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.1925-17.2017 · Cited by 79 · see citing works
Local Opiate Withdrawal in Locus Coeruleus Neurons In Vitro
Ivanov, A., & Aston‐Jones, G. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.85.6.2388 · Cited by 74 · see citing works
Harris, G. C. M. (2001) · Neuropsychopharmacology · doi:10.1016/s0893-133x(00)00184-6 · Cited by 75 · see citing works
Fuentealba, J. A., Forray, M. I., & Gysling, K. (2000) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2000.0750741.x · Cited by 74 · see citing works
Dacher, M., & Nugent, F. S. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.01.028 · Cited by 71 · see citing works
PKG and PKA Signaling in LTP at GABAergic Synapses
Nugent, F. S., Niehaus, J. L., & Kauer, J. A. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2009.5 · Cited by 73 · see citing works
Cruz, M. T., Herman, M. A., Kallupi, M., & Roberto, M. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.10.032 · Cited by 72 · see citing works
Giorgetti, M., Hotsenpiller, G., Froestl, W., & Wolf, M. E. (2002) · Neuroscience · doi:10.1016/s0306-4522(01)00510-3 · Cited by 72 · see citing works
Zachariou, V., Liu, R., LaPlant, Q., Xiao, G., Renthal, W., Chan, G. C., Storm, D. R., Aghajanian, G., & Nestler, E. J. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.11.021 · Cited by 70 · see citing works
Steffensen, S. C., Taylor, S. R., Horton, M. L., Barber, E. N., Lyle, L. T., Stobbs, S. H., & Allison, D. W. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06479.x · Cited by 70 · see citing works
Tao, R., Ma, Z., & Auerbach, S. B. (1998) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)37608-6 · Cited by 70 · see citing works
Madhavan, A., Bonci, A., & Whistler, J. L. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.3366-10.2010 · Cited by 69 · see citing works
Self-citationMorphine withdrawal‐induced abnormalities in the VTA: confocal laser scanning microscopy
Spiga, S., Serra, G. P., Puddu, M. C., Foddai, M., & Diana, M. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02435.x · Cited by 69 · see citing works
Ozaki, S., Narita, M., Narita, M., Ozaki, M., Khotib, J., & Suzuki, T. (2004) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2003.02272.x · Cited by 66 · see citing works
Collo, G., Cavalleri, L., & Spano, P. (2014) · Frontiers in Pharmacology · doi:10.3389/fphar.2014.00259 · Cited by 66 · see citing works
Cruz, M. T., Herman, M. A., Cote, D. M., Ryabinin, A. E., & Roberto, M. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2012.190 · Cited by 66 · see citing works
How to design an opioid drug that causes reduced tolerance and dependence
Berger, A. C., & Whistler, J. L. (2010) · Annals of Neurology · doi:10.1002/ana.22002 · Cited by 65 · see citing works
- Authors
- Bonci, A., & Williams, J. T.
- Affiliations
- Oregon Health & Science University (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 1997-01-15
- Volume
- 17
- Issue
- 2
- Pages
- 796-803
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6573250
- OpenAlex
- W2169322025
- Cited by
- 286
- References
- 45
- Citations by year
- 2026: 4 · 2025: 8 · 2024: 3 · 2023: 12 · 2022: 7 · 2021: 11 · 2020: 6 · 2019: 10 · 2018: 10 · 2017: 9 · 2016: 10 · 2015: 8 · 2014: 15 · 2013: 5 · 2012: 12
- FWCI
- 2.36
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute on Drug Abuse (R01DA008163, DA-08163)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Keywords
- morphine withdrawal, GABA release, ventral tegmental area, dopaminergic neurons, miniature IPSCs, opioid receptors, cAMP signaling, adenylate cyclase, protein kinase A, chronic morphine administration, synaptic plasticity, drug addiction
- MeSH terms
- Adenylyl Cyclase Inhibitors, Action Potentials, Cyclic AMP, Adenylyl Cyclases, Animals, Dopamine, Enzyme Activation, Enzyme Inhibitors, Colforsin, gamma-Aminobutyric Acid, Guinea Pigs, Interneurons, Morphine, Nerve Tissue Proteins, Organophosphorus Compounds, Picrotoxin, Receptors, GABA-A, Salicylamides, Serotonin, Strychnine, Substance Withdrawal Syndrome, Tegmentum Mesencephali, Thionucleotides, Phorbol 12,13-Dibutyrate, Signal Transduction, 2-Amino-5-phosphonovalerate, Cyclic AMP-Dependent Protein Kinases, Patch-Clamp Techniques, Dopamine Antagonists, Excitatory Amino Acid Antagonists, 6-Cyano-7-nitroquinoxaline-2,3-dione, GABA Antagonists, Staurosporine
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