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08-06-2024 | Original Article

Modulation of Nicotine-Associated Behaviour in Rats By μ-Opioid Signals from the Medial Prefrontal Cortex to the Nucleus Accumbens Shell

Authors: Feng Zhu, Hirosato Kanda, Hiroyuki Neyama, Yuping Wu, Shigeki Kato, Di Hu, Shaoqi Duan, Koichi Noguchi, Yasuyoshi Watanabe, Kazuto Kobayashi, Yi Dai, Yilong Cui

Published in: Neuroscience Bulletin | Issue 12/2024

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Abstract

Nicotine addiction is a concern worldwide. Most mechanistic investigations are on nicotine substance dependence properties based on its pharmacological effects. However, no effective therapeutic treatment has been established. Nicotine addiction is reinforced by environments or habits. We demonstrate the neurobiological basis of the behavioural aspect of nicotine addiction. We utilized the conditioned place preference to establish nicotine-associated behavioural preferences (NABP) in rats. Brain-wide neuroimaging analysis revealed that the medial prefrontal cortex (mPFC) was activated and contributed to NABP. Chemogenetic manipulation of µ-opioid receptor positive (MOR+) neurons in the mPFC or the excitatory outflow to the nucleus accumbens shell (NAcShell) modulated the NABP. Electrophysiological recording confirmed that the MOR+ neurons directly regulate the mPFC-NAcShell circuit via GABAA receptors. Thus, the MOR+ neurons in the mPFC modulate the formation of behavioural aspects of nicotine addiction via direct excitatory innervation to the NAcShell, which may provide new insight for the development of effective therapeutic strategies.
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Literature
1.
2.
go back to reference Le Foll B, Piper ME, Fowler CD, Tonstad S, Bierut L, Lu L. Tobacco and nicotine use. Nat Rev Dis Primers 2022, 8: 19.PubMedCrossRef Le Foll B, Piper ME, Fowler CD, Tonstad S, Bierut L, Lu L. Tobacco and nicotine use. Nat Rev Dis Primers 2022, 8: 19.PubMedCrossRef
4.
go back to reference Tamburin S, Dal Lago D, Armani F, Turatti M, Saccà R, Campagnari S, et al. Smoking-related cue reactivity in a virtual reality setting: Association between craving and EEG measures. Psychopharmacology 2021, 238: 1363–1371.PubMedCrossRef Tamburin S, Dal Lago D, Armani F, Turatti M, Saccà R, Campagnari S, et al. Smoking-related cue reactivity in a virtual reality setting: Association between craving and EEG measures. Psychopharmacology 2021, 238: 1363–1371.PubMedCrossRef
5.
go back to reference Shiffman S, Dunbar M, Kirchner T, Li X, Tindle H, Anderson S, et al. Smoker reactivity to cues: Effects on craving and on smoking behavior. J Abnorm Psychol 2013, 122: 264–280.PubMedCrossRef Shiffman S, Dunbar M, Kirchner T, Li X, Tindle H, Anderson S, et al. Smoker reactivity to cues: Effects on craving and on smoking behavior. J Abnorm Psychol 2013, 122: 264–280.PubMedCrossRef
6.
go back to reference Conklin CA, Coffman BA, McClernon FJ, Joyce C. Smokers’ self-report and behavioral reactivity to combined personal smoking cues (proximal + environment + people): A pilot study. Brain Sci 2022, 12: 1547.PubMedPubMedCentralCrossRef Conklin CA, Coffman BA, McClernon FJ, Joyce C. Smokers’ self-report and behavioral reactivity to combined personal smoking cues (proximal + environment + people): A pilot study. Brain Sci 2022, 12: 1547.PubMedPubMedCentralCrossRef
7.
go back to reference Spagnolo PA, Gómez Pérez LJ, Terraneo A, Gallimberti L, Bonci A. Neural correlates of cue- and stress-induced craving in gambling disorders: Implications for transcranial magnetic stimulation interventions. Eur J Neurosci 2019, 50: 2370–2383.PubMedCrossRef Spagnolo PA, Gómez Pérez LJ, Terraneo A, Gallimberti L, Bonci A. Neural correlates of cue- and stress-induced craving in gambling disorders: Implications for transcranial magnetic stimulation interventions. Eur J Neurosci 2019, 50: 2370–2383.PubMedCrossRef
8.
go back to reference Limbrick-Oldfield EH, Mick I, Cocks RE, McGonigle J, Sharman SP, Goldstone AP, et al. Neural substrates of cue reactivity and craving in gambling disorder. Transl Psychiatry 2017, 7: e992.PubMedPubMedCentralCrossRef Limbrick-Oldfield EH, Mick I, Cocks RE, McGonigle J, Sharman SP, Goldstone AP, et al. Neural substrates of cue reactivity and craving in gambling disorder. Transl Psychiatry 2017, 7: e992.PubMedPubMedCentralCrossRef
9.
go back to reference Arend AK, Schnepper R, Lutz APC, Eichin KN, Blechert J. Prone to food in bad mood-Emotion-potentiated food-cue reactivity in patients with binge-eating disorder. Int J Eat Disord 2022, 55: 564–569.PubMedPubMedCentralCrossRef Arend AK, Schnepper R, Lutz APC, Eichin KN, Blechert J. Prone to food in bad mood-Emotion-potentiated food-cue reactivity in patients with binge-eating disorder. Int J Eat Disord 2022, 55: 564–569.PubMedPubMedCentralCrossRef
10.
go back to reference Janes AC, Farmer S, Frederick BD, Nickerson LD, Lukas SE. An increase in tobacco craving is associated with enhanced medial prefrontal cortex network coupling. PLoS One 2014, 9: e88228.PubMedPubMedCentralCrossRef Janes AC, Farmer S, Frederick BD, Nickerson LD, Lukas SE. An increase in tobacco craving is associated with enhanced medial prefrontal cortex network coupling. PLoS One 2014, 9: e88228.PubMedPubMedCentralCrossRef
11.
go back to reference Hayashi T, Ko JH, Strafella AP, Dagher A. Dorsolateral prefrontal and orbitofrontal cortex interactions during self-control of cigarette craving. Proc Natl Acad Sci U S A 2013, 110: 4422–4427.PubMedPubMedCentralCrossRef Hayashi T, Ko JH, Strafella AP, Dagher A. Dorsolateral prefrontal and orbitofrontal cortex interactions during self-control of cigarette craving. Proc Natl Acad Sci U S A 2013, 110: 4422–4427.PubMedPubMedCentralCrossRef
12.
go back to reference Kober H, Mende-Siedlecki P, Kross EF, Weber J, Mischel W, Hart CL, et al. Prefrontal-striatal pathway underlies cognitive regulation of craving. Proc Natl Acad Sci U S A 2010, 107: 14811–14816.PubMedPubMedCentralCrossRef Kober H, Mende-Siedlecki P, Kross EF, Weber J, Mischel W, Hart CL, et al. Prefrontal-striatal pathway underlies cognitive regulation of craving. Proc Natl Acad Sci U S A 2010, 107: 14811–14816.PubMedPubMedCentralCrossRef
13.
go back to reference Sun N, Laviolette SR, Addiction Research Group. Dopamine receptor blockade modulates the rewarding and aversive properties of nicotine via dissociable neuronal activity patterns in the nucleus accumbens. Neuropsychopharmacology 2014, 39: 2799–2815.PubMedPubMedCentralCrossRef Sun N, Laviolette SR, Addiction Research Group. Dopamine receptor blockade modulates the rewarding and aversive properties of nicotine via dissociable neuronal activity patterns in the nucleus accumbens. Neuropsychopharmacology 2014, 39: 2799–2815.PubMedPubMedCentralCrossRef
14.
go back to reference Xia L, Nygard SK, Sobczak GG, Hourguettes NJ, Bruchas MR. Dorsal-CA1 hippocampal neuronal ensembles encode nicotine-reward contextual associations. Cell Rep 2017, 19: 2143–2156.PubMedPubMedCentralCrossRef Xia L, Nygard SK, Sobczak GG, Hourguettes NJ, Bruchas MR. Dorsal-CA1 hippocampal neuronal ensembles encode nicotine-reward contextual associations. Cell Rep 2017, 19: 2143–2156.PubMedPubMedCentralCrossRef
15.
go back to reference Nygard SK, Hourguettes NJ, Sobczak GG, Carlezon WA, Bruchas MR. Stress-induced reinstatement of nicotine preference requires dynorphin/kappa opioid activity in the basolateral amygdala. J Neurosci 2016, 36: 9937–9948.PubMedPubMedCentralCrossRef Nygard SK, Hourguettes NJ, Sobczak GG, Carlezon WA, Bruchas MR. Stress-induced reinstatement of nicotine preference requires dynorphin/kappa opioid activity in the basolateral amygdala. J Neurosci 2016, 36: 9937–9948.PubMedPubMedCentralCrossRef
16.
go back to reference Xue YX, Chen YY, Zhang LB, Zhang LQ, Huang GD, Sun SC, et al. Selective inhibition of amygdala neuronal ensembles encoding nicotine-associated memories inhibits nicotine preference and relapse. Biol Psychiatry 2017, 82: 781–793.PubMedPubMedCentralCrossRef Xue YX, Chen YY, Zhang LB, Zhang LQ, Huang GD, Sun SC, et al. Selective inhibition of amygdala neuronal ensembles encoding nicotine-associated memories inhibits nicotine preference and relapse. Biol Psychiatry 2017, 82: 781–793.PubMedPubMedCentralCrossRef
17.
go back to reference Hillhouse TM, Olson KM, Hallahan JE, Rysztak LG, Sears BF, Meurice C, et al. The buprenorphine analogue BU10119 attenuates drug-primed and stress-induced cocaine reinstatement in mice. J Pharmacol Exp Ther 2021, 378: 287–299.PubMedPubMedCentralCrossRef Hillhouse TM, Olson KM, Hallahan JE, Rysztak LG, Sears BF, Meurice C, et al. The buprenorphine analogue BU10119 attenuates drug-primed and stress-induced cocaine reinstatement in mice. J Pharmacol Exp Ther 2021, 378: 287–299.PubMedPubMedCentralCrossRef
18.
go back to reference De Sa Nogueira D, Bourdy R, Filliol D, Romieu P, Befort K. Hippocampal mu opioid receptors are modulated following cocaine self-administration in rat. Eur J Neurosci 2021, 53: 3341–3349.CrossRef De Sa Nogueira D, Bourdy R, Filliol D, Romieu P, Befort K. Hippocampal mu opioid receptors are modulated following cocaine self-administration in rat. Eur J Neurosci 2021, 53: 3341–3349.CrossRef
19.
go back to reference Brown TG, Xu J, Hurd YL, Pan YX. Dysregulated expression of the alternatively spliced variant mRNAs of the mu opioid receptor gene, OPRM1, in the medial prefrontal cortex of male human heroin abusers and heroin self-administering male rats. J Neurosci Res 2022, 100: 35–47.PubMedCrossRef Brown TG, Xu J, Hurd YL, Pan YX. Dysregulated expression of the alternatively spliced variant mRNAs of the mu opioid receptor gene, OPRM1, in the medial prefrontal cortex of male human heroin abusers and heroin self-administering male rats. J Neurosci Res 2022, 100: 35–47.PubMedCrossRef
20.
go back to reference Tanda G, Di Chiara G. A dopamine-mu1 opioid link in the rat ventral tegmentum shared by palatable food (Fonzies) and non-psychostimulant drugs of abuse. Eur J Neurosci 1998, 10: 1179–1187.PubMedCrossRef Tanda G, Di Chiara G. A dopamine-mu1 opioid link in the rat ventral tegmentum shared by palatable food (Fonzies) and non-psychostimulant drugs of abuse. Eur J Neurosci 1998, 10: 1179–1187.PubMedCrossRef
21.
go back to reference Krause D, Warnecke M, Schuetz CG, Soyka M, Manz KM, Proebstl L, et al. The impact of the opioid antagonist naloxone on experimentally induced craving in nicotine-dependent individuals. Eur Addict Res 2018, 24: 255–265.PubMedCrossRef Krause D, Warnecke M, Schuetz CG, Soyka M, Manz KM, Proebstl L, et al. The impact of the opioid antagonist naloxone on experimentally induced craving in nicotine-dependent individuals. Eur Addict Res 2018, 24: 255–265.PubMedCrossRef
22.
go back to reference King AC, Meyer PJ. Naltrexone alteration of acute smoking response in nicotine-dependent subjects. Pharmacol Biochem Behav 2000, 66: 563–572.PubMedCrossRef King AC, Meyer PJ. Naltrexone alteration of acute smoking response in nicotine-dependent subjects. Pharmacol Biochem Behav 2000, 66: 563–572.PubMedCrossRef
23.
go back to reference Hutchison KE, Monti PM, Rohsenow DJ, Swift RM, Colby SM, Gnys M, et al. Effects of naltrexone with nicotine replacement on smoking cue reactivity: Preliminary results. Psychopharmacology 1999, 142: 139–143.PubMedCrossRef Hutchison KE, Monti PM, Rohsenow DJ, Swift RM, Colby SM, Gnys M, et al. Effects of naltrexone with nicotine replacement on smoking cue reactivity: Preliminary results. Psychopharmacology 1999, 142: 139–143.PubMedCrossRef
24.
go back to reference Cui Y, Toyoda H, Sako T, Onoe K, Hayashinaka E, Wada Y, et al. A voxel-based analysis of brain activity in high-order trigeminal pathway in the rat induced by cortical spreading depression. Neuroimage 2015, 108: 17–22.PubMedCrossRef Cui Y, Toyoda H, Sako T, Onoe K, Hayashinaka E, Wada Y, et al. A voxel-based analysis of brain activity in high-order trigeminal pathway in the rat induced by cortical spreading depression. Neuroimage 2015, 108: 17–22.PubMedCrossRef
25.
go back to reference Zeng Y, Hu D, Yang W, Hayashinaka E, Wada Y, Watanabe Y, et al. A voxel-based analysis of neurobiological mechanisms in placebo analgesia in rats. Neuroimage 2018, 178: 602–612.PubMedCrossRef Zeng Y, Hu D, Yang W, Hayashinaka E, Wada Y, Watanabe Y, et al. A voxel-based analysis of neurobiological mechanisms in placebo analgesia in rats. Neuroimage 2018, 178: 602–612.PubMedCrossRef
26.
go back to reference Cui Y, Neyama H, Hu D, Huang T, Hayashinaka E, Wada Y, et al. FDG PET imaging of the pain matrix in neuropathic pain model rats. Biomedicines 2022, 11: 63.PubMedPubMedCentralCrossRef Cui Y, Neyama H, Hu D, Huang T, Hayashinaka E, Wada Y, et al. FDG PET imaging of the pain matrix in neuropathic pain model rats. Biomedicines 2022, 11: 63.PubMedPubMedCentralCrossRef
27.
go back to reference Schweinhardt P, Fransson P, Olson L, Spenger C, Andersson JLR. A template for spatial normalisation of MR images of the rat brain. J Neurosci Methods 2003, 129: 105–113.PubMedCrossRef Schweinhardt P, Fransson P, Olson L, Spenger C, Andersson JLR. A template for spatial normalisation of MR images of the rat brain. J Neurosci Methods 2003, 129: 105–113.PubMedCrossRef
29.
go back to reference Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG. Improving bioscience research reporting: The ARRIVE guidelines for reporting animal research. PLoS Biol 2010, 8: e1000412.PubMedPubMedCentralCrossRef Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG. Improving bioscience research reporting: The ARRIVE guidelines for reporting animal research. PLoS Biol 2010, 8: e1000412.PubMedPubMedCentralCrossRef
30.
go back to reference Natarajan R, Wright JW, Harding JW. Nicotine-induced conditioned place preference in adolescent rats. Pharmacol Biochem Behav 2011, 99: 519–523.PubMedCrossRef Natarajan R, Wright JW, Harding JW. Nicotine-induced conditioned place preference in adolescent rats. Pharmacol Biochem Behav 2011, 99: 519–523.PubMedCrossRef
31.
go back to reference Xu W, He Y, Zhang J, Li H, Wan X, Li M, et al. Simvastatin blocks reinstatement of cocaine-induced conditioned place preference in male mice with brain lipidome remodeling. Neurosci Bull 2021, 37: 1683–1702.PubMedPubMedCentralCrossRef Xu W, He Y, Zhang J, Li H, Wan X, Li M, et al. Simvastatin blocks reinstatement of cocaine-induced conditioned place preference in male mice with brain lipidome remodeling. Neurosci Bull 2021, 37: 1683–1702.PubMedPubMedCentralCrossRef
32.
go back to reference Schmill MP, Cadney MD, Thompson Z, Hiramatsu L, Albuquerque RL, McNamara MP, et al. Conditioned place preference for cocaine and methylphenidate in female mice from lines selectively bred for high voluntary wheel-running behavior. Genes Brain Behav 2021, 20: e12700.PubMedCrossRef Schmill MP, Cadney MD, Thompson Z, Hiramatsu L, Albuquerque RL, McNamara MP, et al. Conditioned place preference for cocaine and methylphenidate in female mice from lines selectively bred for high voluntary wheel-running behavior. Genes Brain Behav 2021, 20: e12700.PubMedCrossRef
33.
go back to reference McKendrick G, Graziane NM. Drug-induced conditioned place preference and its practical use in substance use disorder research. Front Behav Neurosci 2020, 14: 582147.PubMedPubMedCentralCrossRef McKendrick G, Graziane NM. Drug-induced conditioned place preference and its practical use in substance use disorder research. Front Behav Neurosci 2020, 14: 582147.PubMedPubMedCentralCrossRef
34.
go back to reference Huang T, Okauchi T, Hu D, Shigeta M, Wu Y, Wada Y, et al. Pain matrix shift in the rat brain following persistent colonic inflammation revealed by voxel-based statistical analysis. Mol Pain 2019, 15: 1744806919891327.PubMedPubMedCentralCrossRef Huang T, Okauchi T, Hu D, Shigeta M, Wu Y, Wada Y, et al. Pain matrix shift in the rat brain following persistent colonic inflammation revealed by voxel-based statistical analysis. Mol Pain 2019, 15: 1744806919891327.PubMedPubMedCentralCrossRef
35.
go back to reference Marks MJ, Burch JB, Collins AC. Genetics of nicotine response in four inbred strains of mice. J Pharmacol Exp Ther 1983, 226: 291–302.PubMed Marks MJ, Burch JB, Collins AC. Genetics of nicotine response in four inbred strains of mice. J Pharmacol Exp Ther 1983, 226: 291–302.PubMed
36.
go back to reference Ksir C, Hakan RL, Kellar KJ. Chronic nicotine and locomotor activity: Influences of exposure dose and test dose. Psychopharmacology 1987, 92: 25–29.PubMedCrossRef Ksir C, Hakan RL, Kellar KJ. Chronic nicotine and locomotor activity: Influences of exposure dose and test dose. Psychopharmacology 1987, 92: 25–29.PubMedCrossRef
37.
go back to reference Kiianmaa K, Tuomainen P, Makova N, Seppä T, Mikkola JA, Petteri Piepponen T, et al. The effects of nicotine on locomotor activity and dopamine overflow in the alcohol-preferring AA and alcohol-avoiding ANA rats. Eur J Pharmacol 2000, 407: 293–302.PubMedCrossRef Kiianmaa K, Tuomainen P, Makova N, Seppä T, Mikkola JA, Petteri Piepponen T, et al. The effects of nicotine on locomotor activity and dopamine overflow in the alcohol-preferring AA and alcohol-avoiding ANA rats. Eur J Pharmacol 2000, 407: 293–302.PubMedCrossRef
38.
go back to reference Kuwabara H, Heishman SJ, Brasic JR, Contoreggi C, Cascella N, Mackowick KM, et al. Mu opioid receptor binding correlates with nicotine dependence and reward in smokers. PLoS One 2014, 9: e113694.PubMedPubMedCentralCrossRef Kuwabara H, Heishman SJ, Brasic JR, Contoreggi C, Cascella N, Mackowick KM, et al. Mu opioid receptor binding correlates with nicotine dependence and reward in smokers. PLoS One 2014, 9: e113694.PubMedPubMedCentralCrossRef
39.
go back to reference Hurley SW, Carelli RM. Activation of infralimbic to nucleus accumbens shell pathway suppresses conditioned aversion in male but not female rats. J Neurosci 2020, 40: 6888–6895.PubMedPubMedCentralCrossRef Hurley SW, Carelli RM. Activation of infralimbic to nucleus accumbens shell pathway suppresses conditioned aversion in male but not female rats. J Neurosci 2020, 40: 6888–6895.PubMedPubMedCentralCrossRef
40.
go back to reference Ikemoto S, Qin M, Liu ZH. Primary reinforcing effects of nicotine are triggered from multiple regions both inside and outside the ventral tegmental area. J Neurosci 2006, 26: 723–730.PubMedPubMedCentralCrossRef Ikemoto S, Qin M, Liu ZH. Primary reinforcing effects of nicotine are triggered from multiple regions both inside and outside the ventral tegmental area. J Neurosci 2006, 26: 723–730.PubMedPubMedCentralCrossRef
41.
go back to reference Witkowski G, Szulczyk P. Opioid mu receptor activation inhibits sodium currents in prefrontal cortical neurons via a protein kinase A- and C-dependent mechanism. Brain Res 2006, 1094: 92–106.PubMedCrossRef Witkowski G, Szulczyk P. Opioid mu receptor activation inhibits sodium currents in prefrontal cortical neurons via a protein kinase A- and C-dependent mechanism. Brain Res 2006, 1094: 92–106.PubMedCrossRef
42.
go back to reference Férézou I, Hill EL, Cauli B, Gibelin N, Kaneko T, Rossier J, et al. Extensive overlap of mu-opioid and nicotinic sensitivity in cortical interneurons. Cereb Cortex 2007, 17: 1948–1957.PubMedCrossRef Férézou I, Hill EL, Cauli B, Gibelin N, Kaneko T, Rossier J, et al. Extensive overlap of mu-opioid and nicotinic sensitivity in cortical interneurons. Cereb Cortex 2007, 17: 1948–1957.PubMedCrossRef
43.
go back to reference Wills L, Ables JL, Braunscheidel KM, Caligiuri SPB, Elayouby KS, Fillinger C, et al. Neurobiological mechanisms of nicotine reward and aversion. Pharmacol Rev 2022, 74: 271–310.PubMedPubMedCentralCrossRef Wills L, Ables JL, Braunscheidel KM, Caligiuri SPB, Elayouby KS, Fillinger C, et al. Neurobiological mechanisms of nicotine reward and aversion. Pharmacol Rev 2022, 74: 271–310.PubMedPubMedCentralCrossRef
44.
go back to reference Janes AC, Pizzagalli DA, Richardt S, de Frederick B, Chuzi S, Pachas G, et al. Brain reactivity to smoking cues prior to smoking cessation predicts ability to maintain tobacco abstinence. Biol Psychiatry 2010, 67: 722–729.PubMedPubMedCentralCrossRef Janes AC, Pizzagalli DA, Richardt S, de Frederick B, Chuzi S, Pachas G, et al. Brain reactivity to smoking cues prior to smoking cessation predicts ability to maintain tobacco abstinence. Biol Psychiatry 2010, 67: 722–729.PubMedPubMedCentralCrossRef
45.
go back to reference Field M, Marhe R, Franken IHA. The clinical relevance of attentional bias in substance use disorders. CNS Spectr 2014, 19: 225–230.PubMedCrossRef Field M, Marhe R, Franken IHA. The clinical relevance of attentional bias in substance use disorders. CNS Spectr 2014, 19: 225–230.PubMedCrossRef
46.
go back to reference Zheng J, Liu N, Xu H. Pathway matters: Prefrontal control of negative emotions via distinct downstream regions. Neurosci Bull 2022, 38: 226–228.PubMedCrossRef Zheng J, Liu N, Xu H. Pathway matters: Prefrontal control of negative emotions via distinct downstream regions. Neurosci Bull 2022, 38: 226–228.PubMedCrossRef
47.
go back to reference Tanabe J, Thompson L, Claus E, Dalwani M, Hutchison K, Banich MT. Prefrontal cortex activity is reduced in gambling and nongambling substance users during decision-making. Hum Brain Mapp 2007, 28: 1276–1286.PubMedPubMedCentralCrossRef Tanabe J, Thompson L, Claus E, Dalwani M, Hutchison K, Banich MT. Prefrontal cortex activity is reduced in gambling and nongambling substance users during decision-making. Hum Brain Mapp 2007, 28: 1276–1286.PubMedPubMedCentralCrossRef
48.
go back to reference Veit R, Schag K, Schopf E, Borutta M, Kreutzer J, Ehlis AC, et al. Diminished prefrontal cortex activation in patients with binge eating disorder associates with trait impulsivity and improves after impulsivity-focused treatment based on a randomized controlled IMPULS trial. Neuroimage Clin 2021, 30: 102679.PubMedPubMedCentralCrossRef Veit R, Schag K, Schopf E, Borutta M, Kreutzer J, Ehlis AC, et al. Diminished prefrontal cortex activation in patients with binge eating disorder associates with trait impulsivity and improves after impulsivity-focused treatment based on a randomized controlled IMPULS trial. Neuroimage Clin 2021, 30: 102679.PubMedPubMedCentralCrossRef
49.
go back to reference Melugin PR, Nolan SO, Siciliano CA. Bidirectional causality between addiction and cognitive deficits. Int Rev Neurobiol 2021, 157: 371–407.PubMedCrossRef Melugin PR, Nolan SO, Siciliano CA. Bidirectional causality between addiction and cognitive deficits. Int Rev Neurobiol 2021, 157: 371–407.PubMedCrossRef
51.
go back to reference Yoo JH, Kitchen I, Bailey A. The endogenous opioid system in cocaine addiction: What lessons have opioid peptide and receptor knockout mice taught us? Br J Pharmacol 2012, 166: 1993–2014.PubMedPubMedCentralCrossRef Yoo JH, Kitchen I, Bailey A. The endogenous opioid system in cocaine addiction: What lessons have opioid peptide and receptor knockout mice taught us? Br J Pharmacol 2012, 166: 1993–2014.PubMedPubMedCentralCrossRef
52.
go back to reference Gorelick DA, Kim YK, Bencherif B, Boyd SJ, Nelson R, Copersino M, et al. Imaging brain mu-opioid receptors in abstinent cocaine users: Time course and relation to cocaine craving. Biol Psychiatry 2005, 57: 1573–1582.PubMedCrossRef Gorelick DA, Kim YK, Bencherif B, Boyd SJ, Nelson R, Copersino M, et al. Imaging brain mu-opioid receptors in abstinent cocaine users: Time course and relation to cocaine craving. Biol Psychiatry 2005, 57: 1573–1582.PubMedCrossRef
53.
go back to reference Hikida T, Morita M, MacPherson T. Neural mechanisms of the nucleus accumbens circuit in reward and aversive learning. Neurosci Res 2016, 108: 1–5.PubMedCrossRef Hikida T, Morita M, MacPherson T. Neural mechanisms of the nucleus accumbens circuit in reward and aversive learning. Neurosci Res 2016, 108: 1–5.PubMedCrossRef
54.
go back to reference Floresco SB. The nucleus accumbens: An interface between cognition, emotion, and action. Annu Rev Psychol 2015, 66: 25–52.PubMedCrossRef Floresco SB. The nucleus accumbens: An interface between cognition, emotion, and action. Annu Rev Psychol 2015, 66: 25–52.PubMedCrossRef
55.
go back to reference Corre J, van Zessen R, Loureiro M, Patriarchi T, Tian L, Pascoli V, et al. Dopamine neurons projecting to medial shell of the nucleus accumbens drive heroin reinforcement. Elife 2018, 7: e39945.PubMedPubMedCentralCrossRef Corre J, van Zessen R, Loureiro M, Patriarchi T, Tian L, Pascoli V, et al. Dopamine neurons projecting to medial shell of the nucleus accumbens drive heroin reinforcement. Elife 2018, 7: e39945.PubMedPubMedCentralCrossRef
56.
go back to reference Kiyatkin EA, Stein EA. Fluctuations in nucleus accumbens dopamine during cocaine self-administration behavior: An in vivo electrochemical study. Neuroscience 1995, 64: 599–617.PubMedCrossRef Kiyatkin EA, Stein EA. Fluctuations in nucleus accumbens dopamine during cocaine self-administration behavior: An in vivo electrochemical study. Neuroscience 1995, 64: 599–617.PubMedCrossRef
57.
go back to reference Linnet J, Mouridsen K, Peterson E, Møller A, Doudet DJ, Gjedde A. Striatal dopamine release codes uncertainty in pathological gambling. Psychiatry Res 2012, 204: 55–60.PubMedCrossRef Linnet J, Mouridsen K, Peterson E, Møller A, Doudet DJ, Gjedde A. Striatal dopamine release codes uncertainty in pathological gambling. Psychiatry Res 2012, 204: 55–60.PubMedCrossRef
58.
go back to reference Hildebrandt BA, Sinclair EB, Sisk CL, Klump KL. Exploring reward system responsivity in the nucleus accumbens across chronicity of binge eating in female rats. Int J Eat Disord 2018, 51: 989–993.PubMedPubMedCentralCrossRef Hildebrandt BA, Sinclair EB, Sisk CL, Klump KL. Exploring reward system responsivity in the nucleus accumbens across chronicity of binge eating in female rats. Int J Eat Disord 2018, 51: 989–993.PubMedPubMedCentralCrossRef
59.
go back to reference Tzschentke TM, Schmidt WJ. Functional relationship among medial prefrontal cortex, nucleus accumbens, and ventral tegmental area in locomotion and reward. Crit Rev Neurobiol 2000, 14: 131–142.PubMedCrossRef Tzschentke TM, Schmidt WJ. Functional relationship among medial prefrontal cortex, nucleus accumbens, and ventral tegmental area in locomotion and reward. Crit Rev Neurobiol 2000, 14: 131–142.PubMedCrossRef
60.
go back to reference Hill DF, Parent KL, Atcherley CW, Cowen SL, Heien ML. Differential release of dopamine in the nucleus accumbens evoked by low-versus high-frequency medial prefrontal cortex stimulation. Brain Stimul 2018, 11: 426–434.PubMedCrossRef Hill DF, Parent KL, Atcherley CW, Cowen SL, Heien ML. Differential release of dopamine in the nucleus accumbens evoked by low-versus high-frequency medial prefrontal cortex stimulation. Brain Stimul 2018, 11: 426–434.PubMedCrossRef
61.
go back to reference Quansah Amissah R, Basha D, Bukhtiyarova O, Timofeeva E, Timofeev I. Neuronal activities during palatable food consumption in the reward system of binge-like eating female rats. Physiol Behav 2021, 242: 113604.PubMedCrossRef Quansah Amissah R, Basha D, Bukhtiyarova O, Timofeeva E, Timofeev I. Neuronal activities during palatable food consumption in the reward system of binge-like eating female rats. Physiol Behav 2021, 242: 113604.PubMedCrossRef
62.
go back to reference Koehler S, Ovadia-Caro S, van der Meer E, Villringer A, Heinz A, Romanczuk-Seiferth N, et al. Increased functional connectivity between prefrontal cortex and reward system in pathological gambling. PLoS One 2013, 8: e84565.PubMedPubMedCentralCrossRef Koehler S, Ovadia-Caro S, van der Meer E, Villringer A, Heinz A, Romanczuk-Seiferth N, et al. Increased functional connectivity between prefrontal cortex and reward system in pathological gambling. PLoS One 2013, 8: e84565.PubMedPubMedCentralCrossRef
63.
go back to reference Koehl M, Bjijou Y, Le Moal M, Cador M. Nicotine-induced locomotor activity is increased by preexposure of rats to prenatal stress. Brain Res 2000, 882: 196–200.PubMedCrossRef Koehl M, Bjijou Y, Le Moal M, Cador M. Nicotine-induced locomotor activity is increased by preexposure of rats to prenatal stress. Brain Res 2000, 882: 196–200.PubMedCrossRef
64.
65.
go back to reference Bagdas D, Diester, Riley J, Carper M, Alkhlaif Y, AlOmari D, et al. Assessing nicotine dependence using an oral nicotine free-choice paradigm in mice. Neuropharmacology 2019, 157: 107669.PubMedPubMedCentralCrossRef Bagdas D, Diester, Riley J, Carper M, Alkhlaif Y, AlOmari D, et al. Assessing nicotine dependence using an oral nicotine free-choice paradigm in mice. Neuropharmacology 2019, 157: 107669.PubMedPubMedCentralCrossRef
Metadata
Title
Modulation of Nicotine-Associated Behaviour in Rats By μ-Opioid Signals from the Medial Prefrontal Cortex to the Nucleus Accumbens Shell
Authors
Feng Zhu
Hirosato Kanda
Hiroyuki Neyama
Yuping Wu
Shigeki Kato
Di Hu
Shaoqi Duan
Koichi Noguchi
Yasuyoshi Watanabe
Kazuto Kobayashi
Yi Dai
Yilong Cui
Publication date
08-06-2024
Publisher
Springer Nature Singapore
Published in
Neuroscience Bulletin / Issue 12/2024
Print ISSN: 1673-7067
Electronic ISSN: 1995-8218
DOI
https://doi.org/10.1007/s12264-024-01230-1

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