{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,9]],"date-time":"2026-10-09T03:19:30Z","timestamp":1791515970581,"version":"4.3.4"},"reference-count":53,"publisher":"Elsevier BV","content-domain":{"domain":["elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Pharmacology Biochemistry and Behavior"],"published-print":{"date-parts":[[2013,8]]},"DOI":"10.1016\/j.pbb.2013.04.015","type":"journal-article","created":{"date-parts":[[2013,5,4]],"date-time":"2013-05-04T17:32:08Z","timestamp":1367688728000},"page":"77-83","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":47,"special_numbering":"C","title":["Morphine dependence and withdrawal induced changes in cholinergic signaling"],"prefix":"10.1016","volume":"109","author":[{"given":"Nichole M.","family":"Neugebauer","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Emily B.","family":"Einstein","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maria B.","family":"Lopez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tristan D.","family":"McClure-Begley","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yann S.","family":"Mineur","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marina R.","family":"Picciotto","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.pbb.2013.04.015_bb0005","first-page":"187","article-title":"Selective changes in sensitivity to cholinergic agonists and receptor changes elicited by continuous physostigmine infusion","volume":"255","author":"Bhat","year":"1990","journal-title":"J Pharmacol Exp Ther"},{"key":"10.1016\/j.pbb.2013.04.015_bb0010","doi-asserted-by":"crossref","first-page":"44033","DOI":"10.1074\/jbc.M211719200","article-title":"The effects of beta3 subunit incorporation on the pharmacology and single channel properties of oocyte-expressed human alpha3beta4 neuronal nicotinic receptors","volume":"278","author":"Boorman","year":"2003","journal-title":"J Biol Chem"},{"key":"10.1016\/j.pbb.2013.04.015_bb0015","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/0014-2999(74)90066-1","article-title":"Cholinergic modification of naloxone-induced jumping in morphine dependent mice","volume":"26","author":"Brase","year":"1974","journal-title":"Eur J Pharmacol"},{"key":"10.1016\/j.pbb.2013.04.015_bb0020","doi-asserted-by":"crossref","first-page":"76","DOI":"10.1016\/S0006-8993(99)02197-6","article-title":"Prevention of precipitated withdrawal symptoms by activating central cholinergic systems during a dependence-producing schedule of morphine in rats","volume":"852","author":"Buccafusco","year":"2000","journal-title":"Brain Res"},{"key":"10.1016\/j.pbb.2013.04.015_bb0025","doi-asserted-by":"crossref","first-page":"695","DOI":"10.1111\/j.1476-5381.1994.tb14793.x","article-title":"Blockade of nicotinic responses by physostigmine, tacrine and other cholinesterase inhibitors in rat striatum","volume":"111","author":"Clarke","year":"1994","journal-title":"Br J Pharmacol"},{"key":"10.1016\/j.pbb.2013.04.015_bb0030","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1007\/BF00963983","article-title":"Brain acetylcholine during morphine withdrawal","volume":"9","author":"Crossland","year":"1984","journal-title":"Neurochem Res"},{"key":"10.1016\/j.pbb.2013.04.015_bb0035","doi-asserted-by":"crossref","first-page":"3321","DOI":"10.1523\/JNEUROSCI.22-09-03321.2002","article-title":"Neural systems underlying opiate addiction","volume":"22","author":"De Vries","year":"2002","journal-title":"J Neurosci"},{"key":"10.1016\/j.pbb.2013.04.015_bb0040","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1016\/S0006-2952(01)00899-1","article-title":"A novel mechanism of action and potential use for lobeline as a treatment for psychostimulant abuse","volume":"63","author":"Dwoskin","year":"2002","journal-title":"Biochem Pharmacol"},{"key":"10.1016\/j.pbb.2013.04.015_bb0045","doi-asserted-by":"crossref","first-page":"522","DOI":"10.1016\/j.neuron.2011.04.013","article-title":"Aversion to nicotine is regulated by the balanced activity of beta4 and alpha5 nicotinic receptor subunits in the medial habenula","volume":"70","author":"Frahm","year":"2011","journal-title":"Neuron"},{"key":"10.1016\/j.pbb.2013.04.015_bb0050","doi-asserted-by":"crossref","first-page":"1377","DOI":"10.1046\/j.1460-9568.2002.02187.x","article-title":"Neural correlates of the motivational and somatic components of naloxone-precipitated morphine withdrawal","volume":"16","author":"Frenois","year":"2002","journal-title":"Eur J Neurosci"},{"key":"10.1016\/j.pbb.2013.04.015_bb0055","doi-asserted-by":"crossref","first-page":"5720","DOI":"10.1523\/JNEUROSCI.5032-05.2006","article-title":"No effect of morphine on ventral tegmental dopamine neurons during withdrawal","volume":"26","author":"Georges","year":"2006","journal-title":"J Neurosci"},{"key":"10.1016\/j.pbb.2013.04.015_bb0060","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1016\/j.ejphar.2006.03.045","article-title":"18-Methoxycoronaridine acts in the medial habenula and\/or interpeduncular nucleus to decrease morphine self-administration in rats","volume":"537","author":"Glick","year":"2006","journal-title":"Eur J Pharmacol"},{"key":"10.1016\/j.pbb.2013.04.015_bb0070","doi-asserted-by":"crossref","first-page":"2007","DOI":"10.1124\/mol.105.011940","article-title":"Expression of nigrostriatal alpha 6-containing nicotinic acetylcholine receptors is selectively reduced, but not eliminated, by beta 3 subunit gene deletion","volume":"67","author":"Gotti","year":"2005","journal-title":"Mol Pharmacol"},{"key":"10.1016\/j.pbb.2013.04.015_bb0075","doi-asserted-by":"crossref","first-page":"1162","DOI":"10.1124\/mol.105.015925","volume":"68","author":"Gotti","year":"2005","journal-title":"Mol Pharmacol"},{"key":"10.1016\/j.pbb.2013.04.015_bb0065","doi-asserted-by":"crossref","first-page":"2272","DOI":"10.1523\/JNEUROSCI.5121-08.2009","article-title":"Rodent habenulo-interpeduncular pathway expresses a large variety of uncommon nAChR subtypes, but only the alpha3beta4* and alpha3beta3beta4* subtypes mediate acetylcholine release","volume":"29","author":"Grady","year":"2009","journal-title":"J Neurosci"},{"key":"10.1016\/j.pbb.2013.04.015_bb0080","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1016\/j.pbb.2007.09.010","article-title":"Repeated administration of nicotine attenuates the development of morphine tolerance and dependence in mice","volume":"88","author":"Haghparast","year":"2008","journal-title":"Pharmacol Biochem Behav"},{"key":"10.1016\/j.pbb.2013.04.015_bb0085","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1038\/newbio245219a0","article-title":"Modification of precipitated morphine and methadone abstinence in mice by acetylcholine antagonists","volume":"245","author":"Jhamandas","year":"1973","journal-title":"Nat New Biol"},{"key":"10.1016\/j.pbb.2013.04.015_bb0090","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1016\/S0009-2797(99)00046-0","article-title":"Anticholinesterases induce multigenic transcriptional feedback response suppressing cholinergic neurotransmission","volume":"119\u2013120","author":"Kaufer","year":"1999","journal-title":"Chem Biol Interact"},{"key":"10.1016\/j.pbb.2013.04.015_bb0095","doi-asserted-by":"crossref","first-page":"186","DOI":"10.1016\/0166-2236(92)90171-4","article-title":"Neural substrates of opiate withdrawal","volume":"15","author":"Koob","year":"1992","journal-title":"Trends Neurosci"},{"key":"10.1016\/j.pbb.2013.04.015_bb0100","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1016\/S0021-9258(18)71242-8","article-title":"The quantitative histochemistry of brain. II. Enzyme measurements","volume":"207","author":"Lowry","year":"1954","journal-title":"J Biol Chem"},{"key":"10.1016\/j.pbb.2013.04.015_bb0105","doi-asserted-by":"crossref","first-page":"905","DOI":"10.1016\/S0896-6273(02)00625-6","article-title":"Synaptic mechanisms underlie nicotine-induced excitability of brain reward areas","volume":"33","author":"Mansvelder","year":"2002","journal-title":"Neuron"},{"key":"10.1016\/j.pbb.2013.04.015_bb0110","first-page":"817","article-title":"Effects of chronic nicotine infusion on tolerance development and nicotinic receptors","volume":"226","author":"Marks","year":"1983","journal-title":"J Pharmacol Exp Ther"},{"key":"10.1016\/j.pbb.2013.04.015_bb9000","doi-asserted-by":"crossref","first-page":"947","DOI":"10.1124\/mol.106.025338","article-title":"Deletion of the alpha7, beta2, or beta4 nicotinic receptor subunit genes identifies highly expressed subtypes with relatively low affinity for [3H]epibatidine","volume":"70","author":"Marks","year":"2006","journal-title":"Mol Pharmacol"},{"key":"10.1016\/j.pbb.2013.04.015_bb0115","first-page":"728983","article-title":"New acetylcholinesterase inhibitors for Alzheimer's disease","volume":"2012","author":"Mehta","year":"2012","journal-title":"Int J Alzheimers Dis"},{"key":"10.1016\/j.pbb.2013.04.015_bb0120","doi-asserted-by":"crossref","first-page":"2654","DOI":"10.1016\/S0028-3908(00)00140-4","article-title":"Lobeline inhibits nicotine-evoked [(3)H]dopamine overflow from rat striatal slices and nicotine-evoked (86)Rb(+) efflux from thalamic synaptosomes","volume":"39","author":"Miller","year":"2000","journal-title":"Neuropharmacology"},{"key":"10.1016\/j.pbb.2013.04.015_bb0125","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1016\/S0091-3057(02)00996-6","article-title":"Lobeline attenuates locomotor stimulation induced by repeated nicotine administration in rats","volume":"74","author":"Miller","year":"2003","journal-title":"Pharmacol Biochem Behav"},{"key":"10.1016\/j.pbb.2013.04.015_bb0130","doi-asserted-by":"crossref","first-page":"282","DOI":"10.1016\/j.drugalcdep.2007.02.003","article-title":"Lobeline, a potential pharmacotherapy for drug addiction, binds to mu opioid receptors and diminishes the effects of opioid receptor agonists","volume":"89","author":"Miller","year":"2007","journal-title":"Drug Alcohol Depend"},{"key":"10.1016\/j.pbb.2013.04.015_bb0135","doi-asserted-by":"crossref","first-page":"1330","DOI":"10.1126\/science.1201889","article-title":"Nicotine decreases food intake through activation of POMC neurons","volume":"332","author":"Mineur","year":"2011","journal-title":"Science"},{"key":"10.1016\/j.pbb.2013.04.015_bb0140","doi-asserted-by":"crossref","first-page":"589","DOI":"10.1016\/0361-9230(83)90026-6","article-title":"Acetylcholinesterase changes in the central nervous system of mice during the development of morphine tolerance addiction and withdrawal","volume":"10","author":"Mohanakumar","year":"1983","journal-title":"Brain Res Bull"},{"key":"10.1016\/j.pbb.2013.04.015_bb0145","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1016\/0304-3940(88)90276-5","article-title":"Mecamylamine is a selective non-competitive antagonist of N-methyl-D-aspartate- and aspartate-induced currents in horizontal cells dissociated from the catfish retina","volume":"94","author":"O'Dell","year":"1988","journal-title":"Neurosci Lett"},{"key":"10.1016\/j.pbb.2013.04.015_bb0150","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1016\/j.ejphar.2005.09.060","article-title":"Attenuation of morphine withdrawal signs by intracerebral administration of 18-methoxycoronaridine","volume":"525","author":"Panchal","year":"2005","journal-title":"Eur J Pharmacol"},{"key":"10.1016\/j.pbb.2013.04.015_bb0155","doi-asserted-by":"crossref","first-page":"1132","DOI":"10.1124\/mol.54.6.1132","article-title":"Neuronal nicotinic receptor 2 and 4 subunits confer large differences in agonist binding affinity","volume":"54","author":"Parker","year":"1998","journal-title":"Mol Pharm"},{"key":"10.1016\/j.pbb.2013.04.015_bb0160","series-title":"The rat brain stereotaxic coordinates","author":"Paxinos","year":"2005"},{"key":"10.1016\/j.pbb.2013.04.015_bb0165","doi-asserted-by":"crossref","first-page":"116","DOI":"10.1016\/j.neuron.2012.08.036","article-title":"Acetylcholine as a neuromodulator: cholinergic signaling shapes nervous system function and behavior","volume":"76","author":"Picciotto","year":"2012","journal-title":"Neuron"},{"key":"10.1016\/j.pbb.2013.04.015_bb0170","doi-asserted-by":"crossref","first-page":"401","DOI":"10.1038\/37120","article-title":"Nicotine activates and desensitizes midbrain dopamine neurons","volume":"390","author":"Pidoplichko","year":"1997","journal-title":"Nature"},{"key":"10.1016\/j.pbb.2013.04.015_bb0175","doi-asserted-by":"crossref","first-page":"354","DOI":"10.1016\/0006-8993(91)91616-9","article-title":"Microdialysis evidence that acetylcholine in the nucleus accumbens is involved in morphine withdrawal and its treatment with clonidine","volume":"561","author":"Rada","year":"1991","journal-title":"Brain Res"},{"key":"10.1016\/j.pbb.2013.04.015_bb0180","doi-asserted-by":"crossref","first-page":"1437","DOI":"10.1007\/s00702-008-0107-7","article-title":"Effects of cholinesterase inhibitors on rat nicotinic receptor levels in vivo and in vitro","volume":"115","author":"Reid","year":"2008","journal-title":"J Neural Transm"},{"key":"10.1016\/j.pbb.2013.04.015_bb0185","doi-asserted-by":"crossref","first-page":"3014","DOI":"10.1523\/JNEUROSCI.4934-08.2009","article-title":"Nicotinic receptors in the habenulo-interpeduncular system are necessary for nicotine withdrawal in mice","volume":"29","author":"Salas","year":"2009","journal-title":"J Neurosci"},{"key":"10.1016\/j.pbb.2013.04.015_bb0190","doi-asserted-by":"crossref","first-page":"427","DOI":"10.1111\/j.1471-4159.1985.tb04005.x","article-title":"In vivo regulation of [3H]acetylcholine recognition sites in brain by nicotinic cholinergic drugs","volume":"45","author":"Schwartz","year":"1985","journal-title":"J Neurochem"},{"key":"10.1016\/j.pbb.2013.04.015_bb0195","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1016\/j.brainres.2009.08.028","article-title":"Role of orexin\/hypocretin in dependence and addiction","volume":"1314","author":"Sharf","year":"2010","journal-title":"Brain Res"},{"key":"10.1016\/j.pbb.2013.04.015_bb0200","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1016\/j.ejphar.2004.12.037","article-title":"Cholinergic drugs potentiate human nicotinic alpha4beta2 acetylcholine receptors by a competitive mechanism","volume":"509","author":"Smulders","year":"2005","journal-title":"Eur J Pharmacol"},{"key":"10.1016\/j.pbb.2013.04.015_bb0205","first-page":"475","article-title":"Acetylcholinesterase fluctuations in the brain of mice during morphine dependence development, withdrawal and naloxone induced withdrawal","volume":"31","author":"Sood","year":"1985","journal-title":"Cell Mol Biol"},{"key":"10.1016\/j.pbb.2013.04.015_bb0210","doi-asserted-by":"crossref","first-page":"294","DOI":"10.1038\/35067589","article-title":"Acetylcholinesterase \u2014 new roles for an old actor","volume":"2","author":"Soreq","year":"2001","journal-title":"Nat Rev Neurosci"},{"key":"10.1016\/j.pbb.2013.04.015_bb0215","doi-asserted-by":"crossref","first-page":"318","DOI":"10.1248\/bpb.32.318","article-title":"Roles of nicotinic receptors in acetylcholinesterase inhibitor-induced neuroprotection and nicotinic receptor up-regulation","volume":"32","author":"Takada-Takatori","year":"2009","journal-title":"Biol Pharm Bull"},{"key":"10.1016\/j.pbb.2013.04.015_bb0220","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1016\/j.ejphar.2013.01.005","article-title":"Nicotine\u2013morphine interactions at alpha4beta2, alpha7 and alpha3() nicotinic acetylcholine receptors","volume":"701","author":"Talka","year":"2013","journal-title":"Eur J Pharmacol"},{"key":"10.1016\/j.pbb.2013.04.015_bb0225","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1016\/j.neuropharm.2007.04.010","article-title":"Morphine-induced changes in acetylcholine release in the interpeduncular nucleus and relationship to changes in motor behavior in rats","volume":"53","author":"Taraschenko","year":"2007","journal-title":"Neuropharmacology"},{"key":"10.1016\/j.pbb.2013.04.015_bb0230","first-page":"1432","article-title":"Lobeline and nicotine evoke [3H]overflow from rat striatal slices preloaded with [3H]dopamine: differential inhibition of synaptosomal and vesicular [3H]dopamine uptake","volume":"280","author":"Teng","year":"1997","journal-title":"J Pharmacol Exp Ther"},{"key":"10.1016\/j.pbb.2013.04.015_bb0235","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1093\/ntr\/ntq206","article-title":"Parallel anxiolytic-like effects and upregulation of neuronal nicotinic acetylcholine receptors following chronic nicotine and varenicline","volume":"13","author":"Turner","year":"2011","journal-title":"Nicotine Tob Res"},{"key":"10.1016\/j.pbb.2013.04.015_bb0240","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1016\/j.physbeh.2011.04.045","article-title":"Neurobiology of aversive states","volume":"104","author":"Umberg","year":"2011","journal-title":"Physiol Behav"},{"key":"10.1016\/j.pbb.2013.04.015_bb0245","first-page":"1","article-title":"Simultaneous quantitative assessment of morphine tolerance and physical dependence","volume":"167","author":"Way","year":"1969","journal-title":"J Pharmacol Exp Ther"},{"key":"10.1016\/j.pbb.2013.04.015_bb0250","doi-asserted-by":"crossref","first-page":"3360","DOI":"10.1073\/pnas.79.10.3360","article-title":"Regional cerebral glucose utilization during morphine withdrawal in the rat","volume":"79","author":"Wooten","year":"1982","journal-title":"Proc Natl Acad Sci U S A"},{"key":"10.1016\/j.pbb.2013.04.015_bb0255","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1113\/jphysiol.2006.114645","article-title":"Roles of nicotinic acetylcholine receptor beta subunits in function of human alpha4-containing nicotinic receptors","volume":"576","author":"Wu","year":"2006","journal-title":"J Physiol"},{"key":"10.1016\/j.pbb.2013.04.015_bb0260","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/0014-2999(95)00761-X","article-title":"Nicotine attenuates naloxone-induced jumping behaviour in morphine-dependent mice","volume":"298","author":"Zarrindast","year":"1996","journal-title":"Eur J Pharmacol"}],"container-title":["Pharmacology Biochemistry and Behavior"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0091305713001160?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0091305713001160?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2022,2,16]],"date-time":"2022-02-16T02:36:39Z","timestamp":1644978999000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0091305713001160"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2013,8]]},"references-count":53,"alternative-id":["S0091305713001160"],"URL":"https:\/\/doi.org\/10.1016\/j.pbb.2013.04.015","relation":{},"ISSN":["0091-3057"],"issn-type":[{"value":"0091-3057","type":"print"}],"subject":[],"published":{"date-parts":[[2013,8]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Morphine dependence and withdrawal induced changes in cholinergic signaling","name":"articletitle","label":"Article Title"},{"value":"Pharmacology Biochemistry and Behavior","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.pbb.2013.04.015","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"Copyright \u00a9 2013 Elsevier Inc. All rights reserved.","name":"copyright","label":"Copyright"}]}}