{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,17]],"date-time":"2026-07-17T03:21:59Z","timestamp":1784258519018,"version":"3.55.0"},"reference-count":70,"publisher":"Springer Science and Business Media LLC","issue":"4","license":[{"start":{"date-parts":[[2013,2,8]],"date-time":"2013-02-08T00:00:00Z","timestamp":1360281600000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/www.springer.com\/tdm"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Psychopharmacology"],"published-print":{"date-parts":[[2013,6]]},"DOI":"10.1007\/s00213-013-3002-3","type":"journal-article","created":{"date-parts":[[2013,2,7]],"date-time":"2013-02-07T12:01:11Z","timestamp":1360238471000},"page":"697-709","source":"Crossref","is-referenced-by-count":26,"title":["Ventral tegmental area GABA neurons and opiate motivation"],"prefix":"10.1007","volume":"227","author":[{"given":"Ryan","family":"Ting-A-Kee","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hector","family":"Vargas-Perez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jennifer K.","family":"Mabey","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Samuel I.","family":"Shin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Scott C.","family":"Steffensen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Derek","family":"van der Kooy","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2013,2,8]]},"reference":[{"key":"3002_CR1","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1002\/syn.20272","volume":"60","author":"DW Allison","year":"2006","unstructured":"Allison DW, Ohran AJ, Stobbs SH, Mameli M, Valenzuela CF, Sudweeks SN, Ray AP, Henriksen SJ, Steffensen SC (2006) Connexin-36 gap junctions mediate electrical coupling between ventral tegmental area GABA neurons. Synapse 60:20\u201331","journal-title":"Synapse"},{"key":"3002_CR2","doi-asserted-by":"crossref","first-page":"804","DOI":"10.1002\/syn.20907","volume":"65","author":"DW Allison","year":"2011","unstructured":"Allison DW, Wilcox RS, Ellefsen KL, Askew CE, Hansen DM, Wilcox JD, Sandoval SS, Eggett DL, Yanagawa Y, Steffensen SC (2011) Mefloquine effects on ventral tegmental area dopamine and GABA neuron inhibition: a physiologic role for connexin-36 GAP junctions. Synapse 65:804\u2013813","journal-title":"Synapse"},{"key":"3002_CR3","doi-asserted-by":"crossref","first-page":"8059","DOI":"10.1073\/pnas.131016298","volume":"98","author":"AP Auger","year":"2001","unstructured":"Auger AP, Perrot-Sinal TS, McCarthy MM (2001) Excitatory versus inhibitory GABA as a divergence point in steroid-mediated sexual differentiation of the brain. Proc Natl Acad Sci U S A 98:8059\u20138064","journal-title":"Proc Natl Acad Sci U S A"},{"key":"3002_CR4","doi-asserted-by":"crossref","first-page":"1143","DOI":"10.1002\/cne.22561","volume":"519","author":"JJ Balcita-Pedicino","year":"2011","unstructured":"Balcita-Pedicino JJ, Omelchenko N, Bell R, Sesack SR (2011) The inhibitory influence of the lateral habenula on midbrain dopamine cells: ultrastructural evidence for indirect mediation via the rostromedial mesopontine tegmental nucleus. J Comp Neurol 519:1143\u20131164","journal-title":"J Comp Neurol"},{"key":"3002_CR5","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1037\/0735-7044.106.2.351","volume":"106","author":"A Bechara","year":"1992","unstructured":"Bechara A, van der Kooy D (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\u2013363","journal-title":"Behav Neurosci"},{"key":"3002_CR6","doi-asserted-by":"crossref","first-page":"728","DOI":"10.1038\/nrn920","volume":"3","author":"Y Ben-Ari","year":"2002","unstructured":"Ben-Ari Y (2002) Excitatory actions of GABA during development: the nature of the nurture. Nat Rev Neurosci 3:728\u2013739","journal-title":"Nat Rev Neurosci"},{"key":"3002_CR7","doi-asserted-by":"crossref","first-page":"864","DOI":"10.1126\/science.1120972","volume":"311","author":"O Berton","year":"2006","unstructured":"Berton O, McClung CA, DiLeone RJ, Krishnan V, Renthal W, Russo SJ, Graham D, Tsankova NM, Bolanos CA, Rios M, Monteggia LM, Self DW, Nestler EJ (2006) Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 311:864\u2013868","journal-title":"Science"},{"key":"3002_CR8","doi-asserted-by":"crossref","first-page":"796","DOI":"10.1523\/JNEUROSCI.17-02-00796.1997","volume":"17","author":"A Bonci","year":"1997","unstructured":"Bonci A, Williams JT (1997) Increased probability of GABA release during withdrawal from morphine. J Neurosci 17:796\u2013803","journal-title":"J Neurosci"},{"key":"3002_CR9","doi-asserted-by":"crossref","first-page":"515","DOI":"10.1016\/0166-2236(91)90003-D","volume":"14","author":"E Cherubini","year":"1991","unstructured":"Cherubini E, Gaiarsa JL, Ben-Ari Y (1991) GABA: an excitatory transmitter in early postnatal life. Trends Neurosci 14:515\u2013519","journal-title":"Trends Neurosci"},{"key":"3002_CR10","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1007\/BF00966870","volume":"17","author":"L Churchill","year":"1992","unstructured":"Churchill L, Dilts R, Kalivas P (1992) Autoradiographic localization of gamma-aminobutyric acid-A receptors within the ventral tegmental area. Neurochem Res 17:101\u2013106","journal-title":"Neurochem Res"},{"key":"3002_CR11","doi-asserted-by":"crossref","first-page":"938","DOI":"10.1038\/nature01868","volume":"424","author":"JAM Coull","year":"2003","unstructured":"Coull JAM, Boudreau D, Bachand K, Prescott SA, Nault F, Sik A, De Koninck P, De Koninck Y (2003) Trans-synaptic shift in anion gradient in spinal lamina I neurons as a mechanism of neuropathic pain. Nature 424:938\u2013942","journal-title":"Nature"},{"key":"3002_CR12","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0166-4328(05)80282-7","volume":"50","author":"CL Cunningham","year":"1992","unstructured":"Cunningham CL, Malott DH, Dickinson SD, Risinger FO (1992) Haloperidol does not alter expression of ethanol-induced conditioned place preference. Behav Brain Res 50:1\u20135","journal-title":"Behav Brain Res"},{"key":"3002_CR13","doi-asserted-by":"crossref","first-page":"218","DOI":"10.1523\/JNEUROSCI.3884-09.2010","volume":"30","author":"A Dobi","year":"2010","unstructured":"Dobi A, Margolis EB, Wang HL, Harvey BK, Morales M (2010) Glutamatergic and nonglutamatergic neurons of the ventral tegmental area establish local synaptic contacts with dopaminergic and nondopaminergic neurons. J Neurosci 30:218\u2013229","journal-title":"J Neurosci"},{"key":"3002_CR14","doi-asserted-by":"crossref","first-page":"5302","DOI":"10.1523\/JNEUROSCI.14-09-05302.1994","volume":"14","author":"J-M Fritschy","year":"1994","unstructured":"Fritschy J-M, Paysan J, Enna A, Mohler H (1994) Switch in the expression of rat GABA-A-receptor subtypes during postnatal development: an immunohistochemical study. J Neurosci 14:5302\u20135324","journal-title":"J Neurosci"},{"key":"3002_CR15","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1002\/syn.1088","volume":"41","author":"M Garzon","year":"2001","unstructured":"Garzon M, Pickel VM (2001) Plasmalemmal mu-opioid receptor distribution mainly in nondopaminergic neurons in the rat ventral tegmental area. Synapse 41:311\u2013328","journal-title":"Synapse"},{"key":"3002_CR16","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1016\/0091-3057(84)90284-3","volume":"20","author":"NE Goeders","year":"1984","unstructured":"Goeders NE, Lane JD, Smith JE (1984) Self-administration of methionine enkephalin into the nucleus accumbens. Pharmacol Biochem Behav 20:451\u2013455","journal-title":"Pharmacol Biochem Behav"},{"key":"3002_CR17","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1037\/a0014015","volume":"123","author":"A Heinmiller","year":"2009","unstructured":"Heinmiller A, Ting-A-Kee R, Vargas-Perez H, Yeh A, van der Kooy D (2009) Tegmental pedunculopontine glutamate and GABA-B synapses mediate morphine reward. Behav Neurosci 123:145\u2013155","journal-title":"Behav Neurosci"},{"key":"3002_CR18","doi-asserted-by":"crossref","first-page":"854","DOI":"10.1038\/nature04172","volume":"438","author":"TS Hnasko","year":"2005","unstructured":"Hnasko TS, Sotak BN, Palmiter RD (2005) Morphine reward in dopamine-deficient mice. Nature 438:854\u2013857","journal-title":"Nature"},{"key":"3002_CR19","doi-asserted-by":"crossref","first-page":"515","DOI":"10.1016\/S0896-6273(01)00297-5","volume":"30","author":"CA Hubner","year":"2001","unstructured":"Hubner CA, Stein V, Hermans-Borgmeyer I, Meyer T, Ballanyi K, Jentsch TJ (2001) Disruption of KCC2 reveals an essential role of K-Cl cotransport already in early synaptic inhibition. Neuron 30:515\u2013524","journal-title":"Neuron"},{"key":"3002_CR20","doi-asserted-by":"crossref","first-page":"16446","DOI":"10.1073\/pnas.1105418108","volume":"108","author":"M Jalabert","year":"2011","unstructured":"Jalabert M, Bourdy R, Courtin J, Veinante P, Manzoni OJ, Barrot M, Georges F (2011) Neuronal circuits underlying acute morphine action on dopamine neurons. Proc Natl Acad Sci U S A 108:16446\u201316450","journal-title":"Proc Natl Acad Sci U S A"},{"key":"3002_CR21","doi-asserted-by":"crossref","first-page":"786","DOI":"10.1016\/j.neuron.2009.02.001","volume":"61","author":"TC Jhou","year":"2009","unstructured":"Jhou TC, Fields HL, Baxter MG, Saper CB, Holland PC (2009) The rostromedial tegmental nucleus (RMTg), a GABAergic afferent to midbrain dopamine neurons, encodes aversive stimuli and inhibits motor responses. Neuron 61:786\u2013800","journal-title":"Neuron"},{"key":"3002_CR22","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1523\/JNEUROSCI.12-02-00483.1992","volume":"12","author":"SW Johnson","year":"1992","unstructured":"Johnson SW, North RA (1992a) Opioids excite dopamine neurons by hyperpolarization of local interneurons. J Neurosci 12:483\u2013488","journal-title":"J Neurosci"},{"key":"3002_CR23","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1113\/jphysiol.1992.sp019136","volume":"450","author":"SW Johnson","year":"1992","unstructured":"Johnson SW, North RA (1992b) Two types of neurone in the rat ventral tegmental area and their synaptic inputs. J Physiol 450:455\u2013468","journal-title":"J Physiol"},{"key":"3002_CR24","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1016\/0301-0082(94)90049-3","volume":"42","author":"K Kaila","year":"1994","unstructured":"Kaila K (1994) Ionic basis of GABA-A receptor channel function in the nervous system. Prog Neurobiol 42:489\u2013537","journal-title":"Prog Neurobiol"},{"key":"3002_CR25","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1113\/jphysiol.1993.sp019634","volume":"464","author":"K Kaila","year":"1993","unstructured":"Kaila K, Voipio J, Paalasmaa P, Pasternack M, Deisz RA (1993) The role of bicarbonate in GABA-A receptor-mediated IPSPs of rat neocortical neurones. J Physiol 464:273\u2013289","journal-title":"J Physiol"},{"key":"3002_CR26","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1016\/0165-0173(93)90008-N","volume":"18","author":"PW Kalivas","year":"1993","unstructured":"Kalivas PW (1993) Neurotransmitter regulation of dopamine neurons in the ventral tegmental area. Brain Res Rev 18:75\u2013113","journal-title":"Brain Res Rev"},{"key":"3002_CR27","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1038\/nrn2515","volume":"10","author":"PW Kalivas","year":"2009","unstructured":"Kalivas PW (2009) The glutamate homeostasis hypothesis of addiction. Nat Rev Neurosci 10:561\u2013572","journal-title":"Nat Rev Neurosci"},{"key":"3002_CR28","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1038\/sj.mp.4001197","volume":"8","author":"SR Laviolette","year":"2003","unstructured":"Laviolette SR, van der Kooy D (2003) Blockade of mesolimbic dopamine transmission dramatically increases sensitivity to the rewarding effects of nicotine in the ventral tegmental area. Mol Psychiatry 8:50\u201359","journal-title":"Mol Psychiatry"},{"key":"3002_CR29","doi-asserted-by":"crossref","first-page":"2179","DOI":"10.1111\/j.1460-9568.2004.03665.x","volume":"20","author":"SR Laviolette","year":"2004","unstructured":"Laviolette SR, van der Kooy D (2004) GABAA receptors signal bidirectional reward transmission from the ventral tegmental area to the tegmental pedunculopontine nucleus as a function of opiate state. Eur J Neurosci 20:2179\u20132187","journal-title":"Eur J Neurosci"},{"key":"3002_CR30","doi-asserted-by":"crossref","first-page":"160","DOI":"10.1038\/nn1182","volume":"7","author":"SR Laviolette","year":"2004","unstructured":"Laviolette SR, Gallegos RA, Henriksen SJ, van der Kooy D (2004) Opiate state controls bi-directional reward signaling via GABA-A receptors in the ventral tegmental area. Nat Neurosci 7:160\u2013169","journal-title":"Nat Neurosci"},{"key":"3002_CR31","doi-asserted-by":"crossref","first-page":"589","DOI":"10.1038\/npp.2010.190","volume":"36","author":"S Lecca","year":"2011","unstructured":"Lecca S, Melis M, Luchicchi A, Ennas MG, Castelli MP, Muntoni AL, Pistis M (2011) Effects of drugs of abuse on putative rostromedial tegmental neurons, inhibitory afferents to midbrain dopamine cells. Neuropsychopharmacology 36:589\u2013602","journal-title":"Neuropsychopharmacology"},{"key":"3002_CR32","doi-asserted-by":"crossref","first-page":"736","DOI":"10.1038\/nn.2806","volume":"14","author":"HH Lee","year":"2011","unstructured":"Lee HH, Deeb TZ, Walker JA, Davies PA, Moss SJ (2011) NMDA receptor activity downregulates KCC2 resulting in depolarizing GABA(A) receptor-mediated currents. Nat Neurosci 14:736\u2013743","journal-title":"Nat Neurosci"},{"key":"3002_CR33","doi-asserted-by":"crossref","first-page":"907","DOI":"10.1113\/jphysiol.2006.117069","volume":"577","author":"EB Margolis","year":"2006","unstructured":"Margolis EB, Lock H, Hjelmstad GO, Fields HL (2006) The ventral tegmental area revisited: is there an electrophysiological marker for dopaminergic neurons? J Physiol 577:907\u2013924","journal-title":"J Physiol"},{"key":"3002_CR34","doi-asserted-by":"crossref","first-page":"2887","DOI":"10.1152\/jn.2001.86.6.2887","volume":"86","author":"M Martina","year":"2001","unstructured":"Martina M, Royer S, Pare D (2001) Cell-type-specific GABA responses and chloride homeostasis in the cortex and amygdala. J Neurophysiol 86:2887\u20132895","journal-title":"J Neurophysiol"},{"key":"3002_CR35","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1016\/0006-8993(82)91123-4","volume":"243","author":"RF Mucha","year":"1982","unstructured":"Mucha RF, van der Kooy D, O'Shaughnessy M, Bucenieks P (1982) Drug reinforcement studied by the use of place conditioning in rat. Brain Res 243:91\u2013105","journal-title":"Brain Res"},{"key":"3002_CR36","doi-asserted-by":"crossref","first-page":"68","DOI":"10.3758\/BF03327082","volume":"22","author":"K Nader","year":"1994","unstructured":"Nader K, van der Kooy D (1994) The motivation produced by morphine and food is isomorphic: approaches to specific motivational stimuli are learned. Psychobiology 22:68\u201376","journal-title":"Psychobiology"},{"key":"3002_CR37","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1111\/j.1460-9568.2010.07256.x","volume":"32","author":"JL Niehaus","year":"2010","unstructured":"Niehaus JL, Murali M, Kauer JA (2010) Drugs of abuse and stress impair LTP at inhibitory synapses in the ventral tegmental area. Eur J Neurosci 32:108\u2013117","journal-title":"Eur J Neurosci"},{"key":"3002_CR38","doi-asserted-by":"crossref","unstructured":"Okada H, Matsushita N, Kobayashi K (2004) Identification of GABAA receptor subunit variants in midbrain dopaminergic neurons. J Neurochem 89:7\u201314","DOI":"10.1111\/j.1471-4159.2004.02271.x"},{"key":"3002_CR39","doi-asserted-by":"crossref","first-page":"429","DOI":"10.1016\/0006-8993(82)90454-1","volume":"237","author":"ME Olds","year":"1982","unstructured":"Olds ME (1982) Reinforcing effects of morphine in the nucleus accumbens. Brain Res 237:429\u2013440","journal-title":"Brain Res"},{"key":"3002_CR40","doi-asserted-by":"crossref","first-page":"411","DOI":"10.1016\/0306-4522(93)90072-N","volume":"57","author":"MC Olmstead","year":"1993","unstructured":"Olmstead MC, Franklin KB (1993) Effects of pedunculopontine tegmental nucleus lesions on morphine-induced conditioned place preference and analgesia in the formalin test. Neuroscience 57:411\u2013418","journal-title":"Neuroscience"},{"key":"3002_CR41","doi-asserted-by":"crossref","first-page":"5035","DOI":"10.1523\/JNEUROSCI.18-13-05035.1998","volume":"18","author":"MC Olmstead","year":"1998","unstructured":"Olmstead MC, Munn EM, Franklin KB, Wise RA (1998) Effects of pedunculopontine tegmental nucleus lesions on responding for intravenous heroin under different schedules of reinforcement. J Neurosci 18:5035\u20135044","journal-title":"J Neurosci"},{"key":"3002_CR42","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1002\/cne.20417","volume":"483","author":"N Omelchenko","year":"2005","unstructured":"Omelchenko N, Sesack SR (2005) Laterodorsal tegmental projections to identified cell populations in the rat ventral tegmental area. J Comp Neurol 483:217\u2013235","journal-title":"J Comp Neurol"},{"key":"3002_CR43","doi-asserted-by":"crossref","first-page":"895","DOI":"10.1002\/syn.20668","volume":"63","author":"N Omelchenko","year":"2009","unstructured":"Omelchenko N, Sesack SR (2009) Ultrastructural analysis of local collaterals of rat ventral tegmental area neurons: GABA phenotype and synapses onto dopamine and GABA cells. Synapse 63:895\u2013906","journal-title":"Synapse"},{"key":"3002_CR44","volume-title":"The rat brain in stereotaxic coordinates","author":"G Paxinos","year":"1986","unstructured":"Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates, 2nd edn. Academic, Toronto","edition":"2"},{"key":"3002_CR45","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1007\/BF00427441","volume":"84","author":"HO Pettit","year":"1984","unstructured":"Pettit HO, Ettenberg A, Bloom FE, Koob GF (1984) Destruction of dopamine in the nucleus accumbens selectively attenuates cocaine but not heroin self-administration in rats. Psychopharmacology (Berlin) 84:167\u2013173","journal-title":"Psychopharmacology (Berlin)"},{"key":"3002_CR46","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1038\/16697","volume":"397","author":"C Rivera","year":"1999","unstructured":"Rivera C, Voipio J, Payne JA, Ruusuvuori E, Lahtinen H, Lamsa K, Pirvola U, Saarma M, Kaila K (1999) The K+\/Cl- co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397:251\u2013255","journal-title":"Nature"},{"key":"3002_CR47","doi-asserted-by":"crossref","first-page":"747","DOI":"10.1083\/jcb.200209011","volume":"159","author":"C Rivera","year":"2002","unstructured":"Rivera C, Li H, Thomas-Crusells J, Lahtinen H, Viitanen T, Nanobashvili A, Kokaia Z, Airaksinen MS, Voipio J, Kaila K, Saarma M (2002) BDNF-induced TrkB activation down-regulates the K+\u2013Cl\u2212 cotransporter KCC2 and impairs neuronal Cl\u2212 extrusion. J Cell Biol 159:747\u2013752","journal-title":"J Cell Biol"},{"key":"3002_CR48","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1016\/0165-0173(93)90013-P","volume":"18","author":"TE Robinson","year":"1993","unstructured":"Robinson TE, Berridge KC (1993) The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res Rev 18:247\u2013291","journal-title":"Brain Res Rev"},{"key":"3002_CR49","doi-asserted-by":"crossref","first-page":"18198","DOI":"10.1523\/JNEUROSCI.2560-11.2011","volume":"31","author":"J Sarkar","year":"2011","unstructured":"Sarkar J, Wakefield S, MacKenzie G, Moss SJ, Maguire J (2011) Neurosteroidogenesis is required for the physiological response to stress: role of neurosteroid-sensitive GABAA receptors. J Neurosci 31:18198\u201318210","journal-title":"J Neurosci"},{"key":"3002_CR50","doi-asserted-by":"crossref","first-page":"526","DOI":"10.1002\/cne.1158","volume":"433","author":"C Schwarzer","year":"2001","unstructured":"Schwarzer C, Berresheim U, Pirker S, Wieselthaler A, Fuchs K, Sieghart W, Sperk G (2001) Distribution of the major gamma-aminobutyric acid(A) receptor subunits in the basal ganglia and associated limbic brain areas of the adult rat. J Comp Neurol 433:526\u2013549","journal-title":"J Comp Neurol"},{"key":"3002_CR51","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1002\/cne.903200202","volume":"320","author":"SR Sesack","year":"1992","unstructured":"Sesack SR, Pickel VM (1992) Synapse on unlabeled neuronal targets of catecholamine terminals in the nucleus accumbens septi and on dopamine neurons in the ventral tegmental area. J Comp Neurol 320:145\u2013160","journal-title":"J Comp Neurol"},{"issue":"5226","key":"3002_CR52","doi-asserted-by":"crossref","first-page":"977","DOI":"10.1126\/science.7638623","volume":"269","author":"KJ Staley","year":"1995","unstructured":"Staley KJ, Soldo BL, Proctor WR (1995) Ionic mechanisms of neuronal excitation by inhibitory GABA-A receptors. Science 269(5226):977\u2013981","journal-title":"Science"},{"key":"3002_CR53","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1016\/j.expneurol.2006.05.023","volume":"202","author":"SC Steffensen","year":"2006","unstructured":"Steffensen SC, Stobbs SH, Colago EE, Lee RS, Koob GF, Gallegos RA, Henriksen SJ (2006) Contingent and non-contingent effects of heroin on mu-opioid receptor-containing ventral tegmental area GABA neurons. Exp Neurol 202:139\u2013151","journal-title":"Exp Neurol"},{"key":"3002_CR54","doi-asserted-by":"crossref","first-page":"695","DOI":"10.1002\/syn.20885","volume":"65","author":"SC Steffensen","year":"2011","unstructured":"Steffensen SC, Bradley KD, Hansen DM, Wilcox JD, Wilcox RS, Allison DW, Merrill CB, Edwards JG (2011) The role of connexin-36 gap junctions in alcohol intoxication and consumption. Synapse 65:695\u2013707","journal-title":"Synapse"},{"key":"3002_CR55","first-page":"961","volume":"297","author":"M-K Sun","year":"2001","unstructured":"Sun M-K, Alkon DL (2001) Pharmacological enhancement of synaptic efficacy, spatial learning, and memory through carbonic anhydrase activation in rats. J Pharmacol Exp Ther 297:961\u2013967","journal-title":"J Pharmacol Exp Ther"},{"key":"3002_CR56","doi-asserted-by":"crossref","first-page":"661","DOI":"10.1111\/j.1460-9568.2012.08007.x","volume":"35","author":"L Sun","year":"2012","unstructured":"Sun L, Yu Z, Wang W, Liu X (2012) Both NKCC1 and anion exchangers contribute to Cl(\u2212) accumulation in postnatal forebrain neuronal progenitors. Eur J Neurosci 35:661\u2013672","journal-title":"Eur J Neurosci"},{"key":"3002_CR57","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1002\/syn.1079","volume":"41","author":"AL Svingos","year":"2001","unstructured":"Svingos AL, Garzon M, Colago EEO, Pickel VM (2001) mu-opioid receptors in the ventral tegmental area are targeted to presynaptically and directly modulate mesocortical projection neurons. Synapse 41:221\u2013229","journal-title":"Synapse"},{"key":"3002_CR58","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1016\/0361-9230(82)90145-9","volume":"9","author":"LW Swanson","year":"1982","unstructured":"Swanson LW (1982) The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study. Brain Res Bull 9:321\u2013353","journal-title":"Brain Res Bull"},{"key":"3002_CR59","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1002\/cne.10905","volume":"467","author":"N Tamamaki","year":"2003","unstructured":"Tamamaki N, Yanagawa Y, Tomioka R, Miyazaki J, Obata K, Kaneko T (2003) Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol 467:60\u201379","journal-title":"J Comp Neurol"},{"key":"3002_CR60","doi-asserted-by":"crossref","first-page":"769","DOI":"10.1038\/nature08758","volume":"463","author":"KR Tan","year":"2010","unstructured":"Tan KR, Brown M, Labouebe G, Yvon C, Creton C, Fritschy JM, Rudolph U, Luscher C (2010) Neural bases for addictive properties of benzodiazepines. Nature 463:769\u2013774","journal-title":"Nature"},{"key":"3002_CR61","doi-asserted-by":"crossref","first-page":"210","DOI":"10.1016\/0006-8993(80)90788-X","volume":"201","author":"AM Thierry","year":"1980","unstructured":"Thierry AM, Deniau JM, Herve D, Chevalier G (1980) Electrophysiological evidence for non-dopaminergic mesocortical and mesolimbic neurons in the rat. Brain Res 201:210\u2013214","journal-title":"Brain Res"},{"key":"3002_CR62","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1016\/0304-3940(88)90479-X","volume":"89","author":"SM Thompson","year":"1988","unstructured":"Thompson SM, Deisz RA, Prince DA (1988) Outward chloride\/cation co-transport in mammalian cortical neurons. Neurosci Lett 89:49\u201354","journal-title":"Neurosci Lett"},{"key":"3002_CR63","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1016\/0006-8993(95)00334-M","volume":"682","author":"EJ Bockstaele Van","year":"1995","unstructured":"Van Bockstaele EJ, Pickel VM (1995) GABA-containing neurons in the ventral tegmental area project to the nucleus accumbens in rat brain. Brain Res 682:215\u2013221","journal-title":"Brain Res"},{"key":"3002_CR64","doi-asserted-by":"crossref","first-page":"1732","DOI":"10.1126\/science.1168501","volume":"324","author":"H Vargas-Perez","year":"2009","unstructured":"Vargas-Perez H, Ting-A-Kee R, Walton CH, Hansen DM, Razavi R, Clarke L, Bufalino MR, Allison DW, Steffensen SC, van der Kooy D (2009) Ventral tegmental area BDNF induces an opiate-dependent-like reward state in naive rats. Science 324:1732\u20131734","journal-title":"Science"},{"key":"3002_CR65","doi-asserted-by":"crossref","first-page":"1527","DOI":"10.1113\/jphysiol.2009.181826","volume":"588","author":"T Viitanen","year":"2010","unstructured":"Viitanen T, Ruusuvuori E, Kaila K, Voipio J (2010) The K+\u2013Cl\u2212 cotransporter KCC2 promotes GABAergic excitation in the mature rat hippocampus. J Physiol 588:1527\u20131540","journal-title":"J Physiol"},{"key":"3002_CR66","doi-asserted-by":"crossref","first-page":"598","DOI":"10.1038\/42468","volume":"387","author":"S Wagner","year":"1997","unstructured":"Wagner S, Castel M, Gainer H, Yarom Y (1997) GABA in the mammalian suprachiasmatic nucleus and its role in diurnal rhythmicity. Nature 387:598\u2013603","journal-title":"Nature"},{"key":"3002_CR67","doi-asserted-by":"crossref","first-page":"1642","DOI":"10.1523\/JNEUROSCI.3104-06.2007","volume":"27","author":"H Wake","year":"2007","unstructured":"Wake H, Watanabe M, Moorhouse AJ, Kanematsu T, Horibe S, Matsukawa N, Asai K, Ojika K, Hirata M, Nabekura J (2007) Early changes in KCC2 phosphorylation in response to neuronal stress result in functional downregulation. J Neurosci 27:1642\u20131650","journal-title":"J Neurosci"},{"key":"3002_CR68","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1017\/S0140525X00010372","volume":"5","author":"RA Wise","year":"1982","unstructured":"Wise RA (1982) Neuroleptics and operant behavior: the anhedonia hypothesis. Behav Brain Sci 5:39\u201387","journal-title":"Behav Brain Sci"},{"key":"3002_CR69","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1016\/S0149-7634(89)80021-1","volume":"13","author":"RA Wise","year":"1989","unstructured":"Wise RA (1989) Opiate reward: sites and substrates. Neurosci Biobehav Rev 13:129\u2013133","journal-title":"Neurosci Biobehav Rev"},{"key":"3002_CR70","doi-asserted-by":"crossref","first-page":"7811","DOI":"10.1523\/JNEUROSCI.1504-11.2011","volume":"31","author":"Y Xia","year":"2011","unstructured":"Xia Y, Driscoll JR, Wilbrecht L, Margolis EB, Fields HL, Hjelmstad GO (2011) Nucleus accumbens medium spiny neurons target non-dopaminergic neurons in the ventral tegmental area. J Neurosci 31:7811\u20137816","journal-title":"J Neurosci"}],"container-title":["Psychopharmacology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s00213-013-3002-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/article\/10.1007\/s00213-013-3002-3\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s00213-013-3002-3","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,2,8]],"date-time":"2022-02-08T00:43:33Z","timestamp":1644281013000},"score":1,"resource":{"primary":{"URL":"http:\/\/link.springer.com\/10.1007\/s00213-013-3002-3"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2013,2,8]]},"references-count":70,"journal-issue":{"issue":"4","published-print":{"date-parts":[[2013,6]]}},"alternative-id":["3002"],"URL":"https:\/\/doi.org\/10.1007\/s00213-013-3002-3","relation":{},"ISSN":["0033-3158","1432-2072"],"issn-type":[{"value":"0033-3158","type":"print"},{"value":"1432-2072","type":"electronic"}],"subject":[],"published":{"date-parts":[[2013,2,8]]}}}