Opioid and nondopamine reward circuitry and state-dependent mechanisms.
dopamine
nondopamine
opioid
reward
Journal
Annals of the New York Academy of Sciences
ISSN: 1749-6632
Titre abrégé: Ann N Y Acad Sci
Pays: United States
ID NLM: 7506858
Informations de publication
Date de publication:
09 2019
09 2019
Historique:
received:
13
10
2017
revised:
20
12
2017
accepted:
22
12
2017
pubmed:
8
3
2018
medline:
9
4
2020
entrez:
8
3
2018
Statut:
ppublish
Résumé
A common notion is that essentially all addictive drugs, including opioids, activate dopaminergic pathways in the brain reward system, and the inappropriate use of such drugs induces drug dependence. However, an opioid reward response is reportedly still observed in several models of dopamine depletion, including in animals that are treated with dopamine blockers, animals that are subjected to dopaminergic neuron lesions, and dopamine-deficient mice. The intracranial self-stimulation response is enhanced by stimulants but reduced by morphine. These findings suggest that dopaminergic neurotransmission may not always be required for opioid reward responses. Previous findings also indicate the possibility that dopamine-independent opioid reward may be observed in opioid-naive states but not in opioid-dependent states. Therefore, a history of opioid use should be considered when evaluating the dopamine dependency of opioid reward.
Substances chimiques
Analgesics, Opioid
0
Dopamine
VTD58H1Z2X
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
29-41Subventions
Organisme : Ministry of Education, Culture, Sports, Science and Technology
ID : 25116532
Pays : International
Organisme : Japan Society for the Promotion of Science
ID : 24659549
Pays : International
Organisme : Japan Society for the Promotion of Science
ID : 24659490
Pays : International
Organisme : Japan Society for the Promotion of Science
ID : 24650205
Pays : International
Organisme : Japan Society for the Promotion of Science
ID : 25116532
Pays : International
Organisme : Japan Society for the Promotion of Science
ID : 15H01303
Pays : International
Organisme : Japan Agency for Medical Research and Development
ID : 17dk030707
Pays : International
Organisme : Ministry of Health, Labour and Welfare of Japan
ID : H22-Iyaku-015
Pays : International
Organisme : Ministry of Health, Labour and Welfare of Japan
ID : H25-Iyaku-020
Pays : International
Organisme : Ministry of Health, Labour and Welfare of Japan
ID : 17mk010107 6h000
Pays : International
Organisme : Smoking Research Foundation
Pays : International
Organisme : Naito Foundation
Pays : International
Organisme : Astellas Foundation for Research on Metabolic Disorders
Pays : International
Informations de copyright
© 2018 New York Academy of Sciences.
Références
Daws, L.C., M.J. Avison, S.D. Robertson, et al. 2011. Insulin signaling and addiction. Neuropharmacology 61: 1123-1128.
Olsen, C.M. 2011. Natural rewards, neuroplasticity, and non-drug addictions. Neuropharmacology 61: 1109-1122.
Paredes, R.G. 2014. Opioids and sexual reward. Pharmacol. Biochem. Behav. 121: 124-131.
Vlachou, S. & G. Panagis. 2014. Regulation of brain reward by the endocannabinoid system: a critical review of behavioral studies in animals. Curr. Pharm. Des. 20: 2072-2088.
Mura, E., F. Pistoia, M. Sara, et al. 2014. Pharmacological modulation of the state of awareness in patients with disorders of consciousness: an overview. Curr. Pharm. Des. 20: 4121-4139.
Testa, A., R. Giannuzzi, F. Sollazzo, et al. 2013. Psychiatric emergencies (part II): psychiatric disorders coexisting with organic diseases. Eur. Rev. Med. Pharmacol. Sci. 17(Suppl. 1): 65-85.
Schmidt, K.T. & D. Weinshenker. 2014. Adrenaline rush: the role of adrenergic receptors in stimulant-induced behaviors. Mol. Pharmacol. 85: 640-650.
Fields, H. 2004. State-dependent opioid control of pain. Nat. Rev. Neurosci. 5: 565-575.
Navratilova, E., C.W. Atcherley & F. Porreca. 2015. Brain circuits encoding reward from pain relief. Trends Neurosci. 38: 741-750.
Di Chiara, G. & A. Imperato. 1988. Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc. Natl. Acad. Sci. USA 85: 5274-5278.
Wise, R.A. & P.P. Rompre. 1989. Brain dopamine and reward. Annu. Rev. Psychol. 40: 191-225.
Wise, R.A. 2008. Dopamine and reward: the anhedonia hypothesis 30 years on. Neurotox. Res. 14: 169-183.
Nutt, D.J., A. Lingford-Hughes, D. Erritzoe, et al. 2015. The dopamine theory of addiction: 40 years of highs and lows. Nat. Rev. Neurosci. 16: 305-312.
Diana, M. 2011. The dopamine hypothesis of drug addiction and its potential therapeutic value. Front. Psychiatry 2: 64.
Haber, S.N. 2014. The place of dopamine in the cortico-basal ganglia circuit. Neuroscience 282: 248-257.
Salamone, J.D. & M. Correa. 2012. The mysterious motivational functions of mesolimbic dopamine. Neuron 76: 470-485.
Cacabelos, R. 2017. Parkinson's disease: from pathogenesis to pharmacogenomics. Int. J. Mol. Sci. 18: 551.
Brisch, R., A. Saniotis, R. Wolf, et al. 2014. The role of dopamine in schizophrenia from a neurobiological and evolutionary perspective: old fashioned, but still in vogue. Front. Psychiatry 5: 47.
Brunelin, J., S. Fecteau & M.F. Suaud-Chagny. 2013. Abnormal striatal dopamine transmission in schizophrenia. Curr. Med. Chem. 20: 397-404.
Wise, R.A. 2009. Roles for nigrostriatal-not just mesocorticolimbic-dopamine in reward and addiction. Trends Neurosci. 32: 517-524.
Alonso-Alonso, M., S.C. Woods, M. Pelchat, et al. 2015. Food reward system: current perspectives and future research needs. Nutr. Rev. 73: 296-307.
Juarez, B. & M.H. Han. 2016. Diversity of dopaminergic neural circuits in response to drug exposure. Neuropsychopharmacology 41: 2424-2446.
Berridge, K.C. & M.L. Kringelbach. 2008. Affective neuroscience of pleasure: reward in humans and animals. Psychopharmacology 199: 457-480.
Berridge, K.C. & M.L. Kringelbach. 2015. Pleasure systems in the brain. Neuron 86: 646-664.
Keiflin, R. & P.H. Janak. 2015. Dopamine prediction errors in reward learning and addiction: from theory to neural circuitry. Neuron 88: 247-263.
Ledonne, A. & N.B. Mercuri. 2017. Current concepts on the physiopathological relevance of dopaminergic receptors. Front. Cell. Neurosci. 11: 27.
Hikida, T., M. Morita & T. Macpherson. 2016. Neural mechanisms of the nucleus accumbens circuit in reward and aversive learning. Neurosci. Res. 108: 1-5.
Morales, M. & E.B. Margolis. 2017. Ventral tegmental area: cellular heterogeneity, connectivity and behaviour. Nat. Rev. Neurosci. 18: 73-85.
Bergamini, G., H. Sigrist, B. Ferger, et al. 2016. Depletion of nucleus accumbens dopamine leads to impaired reward and aversion processing in mice: relevance to motivation pathologies. Neuropharmacology 109: 306-319.
Lammel, S., B.K. Lim & R.C. Malenka. 2014. Reward and aversion in a heterogeneous midbrain dopamine system. Neuropharmacology 76(Pt B): 351-359.
Trigo, J.M., E. Martin-Garcia, F. Berrendero, et al. 2010. The endogenous opioid system: a common substrate in drug addiction. Drug Alcohol Depend. 108: 183-194.
Kieffer, B.L. & C.J. Evans. 2009. Opioid receptors: from binding sites to visible molecules in vivo. Neuropharmacology 56(Suppl. 1): 205-212.
Zadina, J.E., L. Hackler, L.J. Ge, et al. 1997. A potent and selective endogenous agonist for the μ-opiate receptor. Nature 386: 499-502.
Chavkin, C., I.F. James & A. Goldstein. 1982. Dynorphin is a specific endogenous ligand of the κ opioid receptor. Science 215: 413-415.
Noble, F., M. Lenoir & N. Marie. 2015. The opioid receptors as targets for drug abuse medication. Br. J. Pharmacol. 172: 3964-3979.
Le Merrer, J., J.A. Becker, K. Befort, et al. 2009. Reward processing by the opioid system in the brain. Physiol. Rev. 89: 1379-1412.
Koob, G.F. & N.D. Volkow. 2010. Neurocircuitry of addiction. Neuropsychopharmacology 35: 217-238; erratum: 35: 1051.
Lutz, P.E. & B.L. Kieffer. 2013. Opioid receptors: distinct roles in mood disorders. Trends Neurosci. 36: 195-206.
McBride, W.J., J.M. Murphy & S. Ikemoto. 1999. Localization of brain reinforcement mechanisms: intracranial self-administration and intracranial place-conditioning studies. Behav. Brain Res. 101: 129-152.
Matthes, H.W., R. Maldonado, F. Simonin, et al. 1996. Loss of morphine-induced analgesia, reward effect and withdrawal symptoms in mice lacking the μ-opioid-receptor gene. Nature 383: 819-823.
Sora, I., N. Takahashi, M. Funada, et al. 1997. Opiate receptor knockout mice define μ receptor roles in endogenous nociceptive responses and morphine-induced analgesia. Proc. Natl. Acad. Sci. USA 94: 1544-1549.
Hall, F.S., X.F. Li, M. Goeb, et al. 2003. Congenic C57BL/6 μ opiate receptor (MOR) knockout mice: baseline and opiate effects. Genes Brain Behav. 2: 114-121.
Piepponen, T.P., T. Kivastik, J. Katajamaki, et al. 1997. Involvement of opioid μ1 receptors in morphine-induced conditioned place preference in rats. Pharmacol. Biochem. Behav. 58: 275-279.
Tang, X.C., K. McFarland, S. Cagle, et al. 2005. Cocaine-induced reinstatement requires endogenous stimulation of μ-opioid receptors in the ventral pallidum. J. Neurosci. 25: 4512-4520.
Norman, H. & M.S. D'Souza. 2017. Endogenous opioid system: a promising target for future smoking cessation medications. Psychopharmacology 234: 1371-1394.
Uhari-Vaananen, J., A. Raasmaja, P. Backstrom, et al. 2016. Accumbal μ-opioid receptors modulate ethanol intake in alcohol-preferring Alko Alcohol rats. Alcohol. Clin. Exp. Res. 40: 2114-2123.
Selleck, R.A. & B.A. Baldo. 2017. Feeding-modulatory effects of mu-opioids in the medial prefrontal cortex: a review of recent findings and comparison to opioid actions in the nucleus accumbens. Psychopharmacology 234: 1439-1449.
Tuulari, J.J., L. Tuominen, F. de Boer, et al. 2017. Feeding releases endogenous opioids in humans. J. Neurosci. 37: 8284-8291.
Pradhan, A.A., K. Befort, C. Nozaki, et al. 2011. The delta opioid receptor: an evolving target for the treatment of brain disorders. Trends Pharmacol. Sci. 32: 581-590.
Berrendero, F., A. Plaza-Zabala, L. Galeote, et al. 2012. Influence of δ-opioid receptors in the behavioral effects of nicotine. Neuropsychopharmacology 37: 2332-2344.
Chefer, V.I. & T.S. Shippenberg. 2009. Augmentation of morphine-induced sensitization but reduction in morphine tolerance and reward in delta-opioid receptor knockout mice. Neuropsychopharmacology 34: 887-898.
Le Merrer, J., A. Plaza-Zabala, C. Del Boca, et al. 2011. Deletion of the δ opioid receptor gene impairs place conditioning but preserves morphine reinforcement. Biol. Psychiatry 69: 700-703.
Lalanne, L., G. Ayranci, B.L. Kieffer, et al. 2014. The kappa opioid receptor: from addiction to depression, and back. Front. Psychiatry 5: 170.
Pfeiffer, A., V. Brantl, A. Herz, et al. 1986. Psychotomimesis mediated by κ opiate receptors. Science 233: 774-776.
Roth, B.L., K. Baner, R. Westkaemper, et al. 2002. Salvinorin A: a potent naturally occurring nonnitrogenous κ opioid selective agonist. Proc. Natl. Acad. Sci. USA 99: 11934-11939.
Mucha, R.F. & A. Herz. 1985. Motivational properties of kappa and mu opioid receptor agonists studied with place and taste preference conditioning. Psychopharmacology 86: 274-280.
Funada, M., T. Suzuki, M. Narita, et al. 1993. Blockade of morphine reward through the activation of κ-opioid receptors in mice. Neuropharmacology 32: 1315-1323.
Spanagel, R., A. Herz & T.S. Shippenberg. 1992. Opposing tonically active endogenous opioid systems modulate the mesolimbic dopaminergic pathway. Proc. Natl. Acad. Sci. USA 89: 2046-2050.
Margolis, E.B., G.O. Hjelmstad, A. Bonci, et al. 2003. Kappa-opioid agonists directly nhibit midbrain dopaminergic neurons. J. Neurosci. 23: 9981-9986.
Chefer, V.I., C.M. Backman, E.D. Gigante, et al. 2013. Kappa opioid receptors on dopaminergic neurons are necessary for kappa-mediated place aversion. Neuropsychopharmacology 38: 2623-2631.
He, S.Q., Z.N. Zhang, J.S. Guan, et al. 2011. Facilitation of μ-opioid receptor activity by preventing δ-opioid receptor-mediated codegradation. Neuron 69: 120-131.
Stockton, S.D., Jr. & L.A. Devi. 2012. Functional relevance of μ-δ opioid receptor heteromerization: a role in novel signaling and implications for the treatment of addiction disorders: from a symposium on new concepts in mu-opioid pharmacology. Drug Alcohol Depend. 121: 167-172.
Chakrabarti, S., N.J. Liu & A.R. Gintzler. 2010. Formation of μ-/κ-opioid receptor heterodimer is sex-dependent and mediates female-specific opioid analgesia. Proc. Natl. Acad. Sci. USA 107: 20115-20119.
Liu, N.J., S. Chakrabarti, S. Schnell, et al. 2011. Spinal synthesis of estrogen and concomitant signaling by membrane estrogen receptors regulate spinal κ- and μ-opioid receptor heterodimerization and female-specific spinal morphine antinociception. J. Neurosci. 31: 11836-11845.
Yoo, J.H., A. Bailey, A. Borsodi, et al. 2014. Knockout subtraction autoradiography: a novel ex vivo method to detect heteromers finds sparse KOP receptor/DOP receptor heterodimerization in the brain. Eur. J. Pharmacol. 731: 1-7.
Strayer, R.J., S.M. Motov & L.S. Nelson. 2017. Something for pain: responsible opioid use in emergency medicine. Am. J. Emerg. Med. 35: 337-341.
Volkow, N.D. & F.S. Collins. 2017. The role of science in addressing the opioid crisis. N. Engl. J. Med. 377: 391-394.
Zahari, Z., C.S. Lee, M.A. Ibrahim, et al. 2016. Comparison of pain tolerance between opioid dependent patients on methadone maintenance therapy (MMT) and opioid naive individuals. J. Pharm. Pharm. Sci. 19: 127-136.
Tu, H.J., K.H. Kang, S.Y. Ho, et al. 2016. Leukemia inhibitory factor (LIF) potentiates antinociception activity and inhibits tolerance induction of opioids. J. Pharm. Pharm. Sci. 117: 512-520.
Lin, C.P., K.H. Kang, H.J. Tu, et al. 2017. CXCL12/CXCR4 signaling contributes to the pathogenesis of opioid tolerance: a translational study. Anesth. Analg. 124: 972-979.
Suzuki, T., Y. Kishimoto & M. Misawa. 1996. Formalin- and carrageenan-induced inflammation attenuates place preferences produced by morphine, methamphetamine and cocaine. Life Sci. 59: 1667-1674.
Ozaki, S., M. Narita, M. Narita, et al. 2003. Suppression of the morphine-induced rewarding effect and G-protein activation in the lower midbrain following nerve injury in the mouse: involvement of G-protein-coupled receptor kinase 2. Neuroscience 116: 89-97.
Ozaki, S., M. Narita, M. Narita, et al. 2002. Suppression of the morphine-induced rewarding effect in the rat with neuropathic pain: implication of the reduction in μ-opioid receptor functions in the ventral tegmental area. J. Neurochem. 82: 1192-1198.
Wade, C.L., P. Krumenacher, K.F. Kitto, et al. 2013. Effect of chronic pain on fentanyl self-administration in mice. PLoS One 8: e79239.
Narita, M., Y. Kishimoto, Y. Ise, et al. 2005. Direct evidence for the involvement of the mesolimbic κ-opioid system in the morphine-induced rewarding effect under an inflammatory pain-like state. Neuropsychopharmacology 30: 111-118.
Massaly, N., J.A. Moron & R. Al-Hasani. 2016. A trigger for opioid misuse: chronic pain and stress dysregulate the mesolimbic pathway and kappa opioid system. Front. Neurosci. 10: 480.
Ting, A.K.R. & D. van der Kooy. 2012. The neurobiology of opiate motivation. Cold Spring Harb. Perspect. Med. 2: a012096.
Fields, H.L. & E.B. Margolis. 2015. Understanding opioid reward. Trends Neurosci. 38: 217-225.
Barrot, M., S.R. Sesack, F. Georges, et al. 2012. Braking dopamine systems: a new GABA master structure for mesolimbic and nigrostriatal functions. J. Neurosci. 32: 14094-14101.
Margolis, E.B., G.O. Hjelmstad, W. Fujita, et al. 2014. Direct bidirectional μ-opioid control of midbrain dopamine neurons. J. Neurosci. 34: 14707-14716.
Ide, S., T. Takahashi, Y. Takamatsu, et al. 2017. Distinct roles of opioid and dopamine systems in lateral hypothalamic intracranial self-stimulation. Int. J. Neuropsychopharmacol. 20: 403-409.
Miller, L.L., A.A. Altarifi & S.S. Negus. 2015. Effects of repeated morphine on intracranial self-stimulation in male rats in the absence or presence of a noxious pain stimulus. Exp. Clin. Psychopharmacol. 23: 405-414.
Negus, S.S. & L.L. Miller. 2014. Intracranial self-stimulation to evaluate abuse potential of drugs. Pharmacol. Rev. 66: 869-917.
Altarifi, A.A. & S.S. Negus. 2011. Some determinants of morphine effects on intracranial self-stimulation in rats: dose, pretreatment time, repeated treatment, and rate dependence. Behav. Pharmacol. 22: 663-673.
Ettenberg, A., H.O. Pettit, F.E. Bloom, et al. 1982. Heroin and cocaine intravenous self-administration in rats: mediation by separate neural systems. Psychopharmacology 78: 204-209.
Pettit, H.O., A. Ettenberg, F.E. Bloom, et al. 1984. Destruction of dopamine in the nucleus accumbens selectively attenuates cocaine but not heroin self-administration in rats. Psychopharmacology 84: 167-173.
Vaccarino, F.J., M. Amalric, N.R. Swerdlow, et al. 1986. Blockade of amphetamine but not opiate-induced locomotion following antagonism of dopamine function in the rat. Pharmacol. Biochem. Behav. 24: 61-65.
Kalivas, P.W., E. Widerlov, D. Stanley, et al. 1983. Enkephalin action on the mesolimbic system: a dopamine-dependent and a dopamine-independent increase in locomotor activity. J. Pharmacol. Exp. Ther. 227: 229-237.
Zhou, Q.Y. & R.D. Palmiter. 1995. Dopamine-deficient mice are severely hypoactive, adipsic, and aphagic. Cell 83: 1197-1209.
Nishii, K., N. Matsushita, H. Sawada, et al. 1998. Motor and learning dysfunction during postnatal development in mice defective in dopamine neuronal transmission. J. Neurosci. Res. 54: 450-464.
Szczypka, M.S., M.A. Rainey, D.S. Kim, et al. 1999. Feeding behavior in dopamine-deficient mice. Proc. Natl. Acad. Sci. USA 96: 12138-12143.
Hnasko, T.S., B.N. Sotak & R.D. Palmiter. 2005. Morphine reward in dopamine-deficient mice. Nature 438: 854-857.
Cannon, C.M. & R.D. Palmiter. 2003. Reward without dopamine. J. Neurosci. 23: 10827-10831.
Robinson, S., S.M. Sandstrom, V.H. Denenberg, et al. 2005. Distinguishing whether dopamine regulates liking, wanting, and/or learning about rewards. Behav. Neurosci. 119: 5-15.
Bechara, A. & D. van der Kooy. 1989. The tegmental pedunculopontine nucleus: a brain-stem output of the limbic system critical for the conditioned place preferences produced by morphine and amphetamine. J. Neurosci. 9: 3400-3409.
Bechara, A. & D. van der Kooy. 1992. A single brain stem substrate mediates the motivational effects of both opiates and food in nondeprived rats but not in deprived rats. Behav. Neurosci. 106: 351-363.
Nader, K. & D. van der Kooy. 1997. Deprivation state switches the neurobiological substrates mediating opiate reward in the ventral tegmental area. J. Neurosci. 17: 383-390.
Laviolette, S.R. & D. van der Kooy. 2001. GABAA receptors in the ventral tegmental area control bidirectional reward signalling between dopaminergic and non-dopaminergic neural motivational systems. Eur. J. Neurosci. 13: 1009-1015.
Churchill, L., R.P. Dilts & P.W. Kalivas. 1992. Autoradiographic localization of γ-aminobutyric acidA receptors within the ventral tegmental area. Neurochem. Res. 17: 101-106.
Steininger, T.L., D.B. Rye & B.H. Wainer. 1992. Afferent projections to the cholinergic pedunculopontine tegmental nucleus and adjacent midbrain extrapyramidal area in the albino rat: I. Retrograde tracing studies. J. Comp. Neurol. 321: 515-543.
Semba, K. & H.C. Fibiger. 1992. Afferent connections of the laterodorsal and the pedunculopontine tegmental nuclei in the rat: a retro- and antero-grade transport and immunohistochemical study. J. Comp. Neurol. 323: 387-410.
Xiao, C., J.R. Cho, C. Zhou, et al. 2016. Cholinergic mesopontine signals govern locomotion and reward through dissociable midbrain pathways. Neuron 90: 333-347.
Yoo, J.H., V. Zell, J. Wu, et al. 2017. Activation of pedunculopontine glutamate neurons is reinforcing. J. Neurosci. 37: 38-46.
Mena-Segovia, J. & J.P. Bolam. 2017. Rethinking the pedunculopontine nucleus: from cellular organization to function. Neuron 94: 7-18.
Wasserman, D.I., J.M. Tan, J.C. Kim, et al. 2016. Muscarinic control of rostromedial tegmental nucleus GABA neurons and morphine-induced locomotion. Eur. J. Neurosci. 44: 1761-1770.
Ikemoto, S. & A. Bonci. 2014. Neurocircuitry of drug reward. Neuropharmacology 76(Pt B): 329-341.
Laviolette, S.R., R.A. Gallegos, S.J. Henriksen, et al. 2004. Opiate state controls bi-directional reward signaling via GABAA receptors in the ventral tegmental area. Nat. Neurosci. 7: 160-169.
Obata, K., M. Oide & H. Tanaka. 1978. Excitatory and inhibitory actions of GABA and glycine on embryonic chick spinal neurons in culture. Brain Res. 144: 179-184.
Yamada, J., A. Okabe, H. Toyoda, et al. 2004. Cl- uptake promoting depolarizing GABA actions in immature rat neocortical neurones is mediated by NKCC1. J. Physiol. 557: 829-841.
Ben-Ari, Y., I. Khalilov, K.T. Kahle, et al. 2012. The GABA excitatory/inhibitory shift in brain maturation and neurological disorders. Neuroscientist 18: 467-486.
Gagnon, M., M.J. Bergeron, G. Lavertu, et al. 2013. Chloride extrusion enhancers as novel therapeutics for neurological diseases. Nat. Med. 19: 1524-1528.
Moore, Y.E., M.R. Kelley, N.J. Brandon, et al. 2017. Seizing control of KCC2: a new therapeutic target for epilepsy. Trends Neurosci. 40: 555-571.
Merner, N.D., M.R. Chandler, C. Bourassa, et al. 2015. Regulatory domain or CpG site variation in SLC12A5, encoding the chloride transporter KCC2, in human autism and schizophrenia. Front. Cell. Neurosci. 9: 386.
Tao, R., C. Li, E.N. Newburn, et al. 2012. Transcript-specific associations of SLC12A5 (KCC2) in human prefrontal cortex with development, schizophrenia, and affective disorders. J. Neurosci. 32: 5216-5222.
Taylor, A.M., A. Castonguay, A. Ghogha, et al. 2016. Neuroimmune regulation of GABAergic neurons within the ventral tegmental area during withdrawal from chronic morphine. Neuropsychopharmacology 41: 949-959.
Fiumelli, H., L. Cancedda & M.M. Poo. 2005. Modulation of GABAergic transmission by activity via postsynaptic Ca2+-dependent regulation of KCC2 function. Neuron 48: 773-786.
Ferrini, F., T. Trang, T.A. Mattioli, et al. 2013. Morphine hyperalgesia gated through microglia-mediated disruption of neuronal Cl- homeostasis. Nat. Neurosci. 16: 183-192.
Ferrini, F., L.E. Lorenzo, A.G. Godin, et al. 2017. Enhancing KCC2 function counteracts morphine-induced hyperalgesia. Sci. Rep. 7: 3870.
Ostroumov, A., A.M. Thomas, B.A. Kimmey, et al. 2016. Stress increases ethanol self-administration via a shift toward excitatory GABA signaling in the ventral tegmental area. Neuron 92: 493-504.
Golden, J.P., J.A. Demaro 3rd, A. Knoten, et al. 2013. Dopamine-dependent compensation maintains motor behavior in mice with developmental ablation of dopaminergic neurons. J. Neurosci. 33: 17095-17107.
Willard, A.M., R.S. Bouchard & A.H. Gittis. 2015. Differential degradation of motor deficits during gradual dopamine depletion with 6-hydroxydopamine in mice. Neuroscience 301: 254-267.
Bello, E.P., R. Casas-Cordero, G.L. Galinanes, et al. 2017. Inducible ablation of dopamine D2 receptors in adult mice impairs locomotion, motor skill learning and leads to severe parkinsonism. Mol. Psychiatry 22: 595-604.
Hagino, Y., S. Kasai, M. Fujita, et al. 2015. Involvement of cholinergic system in hyperactivity in dopamine-deficient mice. Neuropsychopharmacology 40: 1141-1150.
Edwards, N.J., H.A. Tejeda, M. Pignatelli, et al. 2017. Circuit specificity in the inhibitory architecture of the VTA regulates cocaine-induced behavior. Nat. Neurosci. 20: 438-448.
Tao, Y.M., C. Yu, W.S. Wang, et al. 2017. Heteromers of μ opioid and dopamine D1 receptors modulate opioid-induced locomotor sensitization in a dopamine-independent manner. Br. J. Pharmacol. 174: 2842-2861.