Impact of the gut microbiome on nicotine’s motivational effects and glial cells in the ventral tegmental area in male mice
Open accessAbstract
A link between gut dysbiosis and the pathogenesis of brain disorders has been identified. A role for gut bacteria in drug reward and addiction has been suggested but very few studies have investigated their impact on brain and behavioral responses to addictive drugs so far. In particular, their influence on nicotine's addiction-like processes remains unknown. In addition, evidence shows that glial cells shape the neuronal activity of the mesolimbic system but their regulation, within this system, by the gut microbiome is not established. We demonstrate that a lack of gut microbiota in male mice potentiates the nicotine-induced activation of sub-regions of the mesolimbic system. We further show that gut microbiota depletion enhances the response to nicotine of dopaminergic neurons of the posterior ventral tegmental area (pVTA), and alters nicotine's rewarding and aversive effects in an intra-VTA self-administration procedure. These effects were not associated with gross behavioral alterations and the nicotine withdrawal syndrome was not impacted. We further show that depletion of the gut microbiome modulates the glial cells of the mesolimbic system. Notably, it increases the number of astrocytes selectively in the pVTA, and the expression of postsynaptic density protein 95 in both VTA sub-regions, without altering the density of the astrocytic glutamatergic transporter GLT1. Finally, we identify several sub-populations of microglia in the VTA that differ between its anterior and posterior sub-parts, and show that they are re-organized in conditions of gut microbiota depletion. The present study paves the way for refining our understanding of the pathophysiology of nicotine addiction.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Gut microbiota manipulation is linked to alterations in astrocytic proliferation and functions.
“Gut microbiota manipulation has also been linked to alterations in astrocytic proliferation and functions.253–256”
From Microbiota–gut–brain axis and its therapeutic applications in neurodegenerative diseases (2024) · cites this paper as [254]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Host microbiota constantly control maturation and function of microglia in the CNS
Erny, D., Hrabě de Angelis, A. L., Jaitin, D., Wieghofer, P., Staszewski, O., David, E., Keren-Shaul, H., Mahlakoiv, T., Jakobshagen, K., Buch, T., et al. (2015) · Nature Neuroscience · doi:10.1038/nn.4030 · Cited by 3,569 · see citing works
Gut microbiota, metabolites and host immunity
Rooks, M. G., & Garrett, W. S. (2016) · Nature reviews. Immunology · doi:10.1038/nri.2016.42 · Cited by 3,409 · see citing works
Interactions between the microbiota, immune and nervous systems in health and disease
Fung, T. C., Olson, C. A., & Hsiao, E. Y. (2017) · Nature Neuroscience · doi:10.1038/nn.4476 · Cited by 1,900 · see citing works
Bercik, P., Denou, E., Collins, J., Jackson, W., Lu, J., Jury, J., Deng, Y., Blennerhassett, P., Macri, J., McCoy, K. D., et al. (2011) · Gastroenterology · doi:10.1053/j.gastro.2011.04.052 · Cited by 1,748 · see citing works
Rothhammer, V., Mascanfroni, I. D., Bunse, L., Takenaka, M. C., Kenison, J. E., Mayo, L., Chao, C.-C., Patel, B., Yan, R., Blain, M., et al. (2016) · Nature Medicine · doi:10.1038/nm.4106 · Cited by 1,559 · see citing works
Ikemoto, S. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.05.004 · Cited by 1,477 · see citing works
Suez, J., Zmora, N., Zilberman-Schapira, G., Mor, U., Dori-Bachash, M., Bashiardes, S., Zur, M., Regev-Lehavi, D., Ben-Zeev Brik, R., Federici, S., et al. (2018) · Cell · doi:10.1016/j.cell.2018.08.047 · Cited by 1,184 · see citing works
Microbial reconstitution reverses maternal diet-induced social and synaptic deficits in offspring
Buffington, S. A., Di Prisco, G. V., Auchtung, T. A., Ajami, N. J., Petrosino, J. F., & Costa-Mattioli, M. (2016) · Cell · doi:10.1016/j.cell.2016.06.001 · Cited by 1,163 · see citing works
Stress & the gut-brain axis: Regulation by the microbiome
Foster, J. A., Rinaman, L., & Cryan, J. F. (2017) · Neurobiology of Stress · doi:10.1016/j.ynstr.2017.03.001 · Cited by 1,150 · see citing works
Kim, W., Mohney, R. P., Wilson, B. C., Jeohn, G., Liu, B., & Hong, J. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-16-06309.2000 · Cited by 881 · see citing works
Sgritta, M., Dooling, S. W., Buffington, S. A., Momin, E. N., Francis, M. B., Britton, R. A., & Costa-Mattioli, M. (2019) · Neuron · doi:10.1016/j.neuron.2018.11.018 · Cited by 865 · see citing works
Effects of abstinence from tobacco: Valid symptoms and time course
Hughes, J. (2007) · Nicotine & Tobacco Research · doi:10.1080/14622200701188919 · Cited by 793 · see citing works
Microbiome Influences Prenatal and Adult Microglia in a Sex-Specific Manner
Thion, M. S., Low, D., Silvin, A., Chen, J., Grisel, P., Schulte-Schrepping, J., Blecher, R., Ulas, T., Squarzoni, P., Hoeffel, G., et al. (2018) · Cell · doi:10.1016/j.cell.2017.11.042 · Cited by 779 · see citing works
Invited review c-Fos as a transcription factor: a stressful (re)view from a functional map
Kovács, K. J. (1998) · Neurochemistry International · doi:10.1016/s0197-0186(98)00023-0 · Cited by 740 · see citing works
A Neural Circuit for Gut-Induced Reward
Han, W., Téllez, L. A., Perkins, M. H., Pérez-Martínez, I. O., Qu, T., Ferreira, J. G. P., Ferreira, T. L., Quinn, D., Liu, Z.-W., Gao, X., et al. (2018) · Cell · doi:10.1016/j.cell.2018.08.049 · Cited by 739 · see citing works
Nicotine Activation of α4* Receptors: Sufficient for Reward, Tolerance, and Sensitization
Tapper, A. R., McKinney, S. L., Nashmi, R., Schwarz, J., Deshpande, P., Labarca, C., Whiteaker, P., Marks, M. J., Collins, A. C., & Lester, H. A. (2004) · Science · doi:10.1126/science.1099420 · Cited by 686 · see citing works
Kennedy, E. A., King, K. Y., & Baldridge, M. T. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.01534 · Cited by 602 · see citing works
Nicotine reinforcement and cognition restored by targeted expression of nicotinic receptors
Maskos, U., Molles, B. E., Pons, S., Besson, M., Guiard, B. P., Guilloux, J.-P., Evrard, A., Cazala, P., Cormier, A., Mameli-Engvall, M., et al. (2005) · Nature · doi:10.1038/nature03694 · Cited by 566 · see citing works
Self-citationReward system and addiction: what dopamine does and doesn’t do
DiChiara, G., & Bassareo, V. (2006) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2006.11.003 · Cited by 534 · see citing works
Local cues establish and maintain region-specific phenotypes of basal ganglia microglia
De Biase, L. M., Schuebel, K. E., Fusfeld, Z. H., Jair, K., Hawes, I. A., Cimbro, R., Zhang, H.-Y., Liu, Q.-R., Shen, H., Xi, Z.-X., et al. (2017) · Neuron · doi:10.1016/j.neuron.2017.06.020 · Cited by 432 · see citing works
The Multifaceted Profile of Activated Microglia
Lynch, M. A. (2009) · Molecular Neurobiology · doi:10.1007/s12035-009-8077-9 · Cited by 323 · see citing works
Le Foll, B., Piper, M. E., Fowler, C. D., Tonstad, S., Bierut, L., Lu, L., Jha, P., & Hall, W. D. (2022) · Nature Reviews Disease Primers · doi:10.1038/s41572-022-00346-w · Cited by 316 · see citing works
Morphometric characterization of microglial phenotypes in human cerebral cortex
Torres-Platas, S. G., Comeau, S., Rachalski, A., Bo, G. D., Cruceanu, C., Turecki, G., Giros, B., & Mechawar, N. (2014) · Journal of Neuroinflammation · doi:10.1186/1742-2094-11-12 · Cited by 313 · see citing works
Pons, S., Fattore, L., Cossu, G., Tolu, S., Porcu, E., McIntosh, J. M., Changeux, J. P., Maskos, U., & Fratta, W. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.3918-08.2008 · Cited by 312 · see citing works
Self-citationNankova, B. B., Agarwal, R., MacFabe, D. F., & La Gamma, E. F. (2014) · PLoS ONE · doi:10.1371/journal.pone.0103740 · Cited by 294 · see citing works
Ge, X., Ding, C., Zhao, W., Xu, L., Tian, H., Gong, J., Zhu, M., Li, J., & Li, N. (2017) · Journal of Translational Medicine · doi:10.1186/s12967-016-1105-4 · Cited by 274 · see citing works
Cross talk: the microbiota and neurodevelopmental disorders
Kelly, J. R., Minuto, C., Cryan, J. F., Clarke, G., & Dinan, T. G. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00490 · Cited by 271 · see citing works
Alterations of the Host Microbiome Affect Behavioral Responses to Cocaine
Kiraly, D. D., Walker, D. M., Calipari, E. S., Labonté, B., Issler, O., Peña, C. J., Ribeiro, E., Russo, S. J., & Nestler, E. J. (2016) · Scientific Reports · doi:10.1038/srep35455 · Cited by 264 · see citing works
Characterization of spontaneous and precipitated nicotine withdrawal in the mouse
Damaj, M. I., Kao, W., & Martin, B. R. (2003) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.103.054908 · Cited by 222 · see citing works
Current advances in research in treatment and recovery: Nicotine addiction
Prochaska, J. J., & Benowitz, N. L. (2019) · Science Advances · doi:10.1126/sciadv.aay9763 · Cited by 219 · see citing works
Glutamate neurons within the midbrain dopamine regions
Morales, M., & Root, D. H. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.05.032 · Cited by 218 · see citing works
Smoking, nicotine and neuropsychiatric disorders
Döme, P., Lazáry, J., Kalapos, M. P., & Rihmer, Z. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.07.013 · Cited by 215 · see citing works
Etiology of autistic features: the persisting neurotoxic effects of propionic acid
El-Ansary, A. K., Bacha, A. B., & Kotb, M. (2012) · Journal of Neuroinflammation · doi:10.1186/1742-2094-9-74 · Cited by 209 · see citing works
A neural circuit for gut-induced reward
Han, W., Tellez, L. A., Perkins, M. H., Perez, I. O., Qu, T., Ferreira, J., Ferreira, T. L., Quinn, D., Liu, Z.-W., Gao, X.-B., et al. (2018) · Cell · doi:10.1016/j.cell.2018.10.018 · Cited by 204 · cited 1× · see citing works
“Gut microbiota modulation of astrocytes within the pVTA Several mechanisms may connect the gut microbiota to VTA DA neurons including bacterial production of short chain fatty acids [70–72], gut peptides [15, 57] or the vagus nerve [12, 73].”
Toro-Barbosa, M. D., Hurtado‐Romero, A., García-Amezquita, L. E., & García‐Cayuela, T. (2020) · Nutrients · doi:10.3390/nu12123896 · Cited by 195 · see citing works
Perego, C., Vanoni, C., Bossi, M., Massari, S., Basudev, H., Longhi, R., & Pietrini, G. (2000) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2000.0751076.x · Cited by 193 · see citing works
Lee, K., Vuong, H. E., Nusbaum, D. J., Hsiao, E. Y., Evans, C. J., & Taylor, A. M. W. (2018) · Neuropsychopharmacology · doi:10.1038/s41386-018-0211-9 · Cited by 172 · see citing works
Oral administration of Proteus mirabilis damages dopaminergic neurons and motor functions in mice
Choi, J. G., Kim, N., Ju, I. G., Eo, H., Lim, S.-M., Jang, S.-E., Kim, D.-H., & Oh, M. S. (2018) · Scientific Reports · doi:10.1038/s41598-018-19646-x · Cited by 170 · see citing works
Synaptic Glutamate Spillover Due to Impaired Glutamate Uptake Mediates Heroin Relapse
Shen, H., Scofield, M. D., Boger, H. A., Hensley-Simon, M. E., & Kalivas, P. W. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.4564-13.2014 · Cited by 164 · see citing works
Co-activation of VTA DA and GABA neurons mediates nicotine reinforcement
Tolu, S., Eddine, R., Marti, F., David, V, Graupner, M., Pons, S., Baudonnat, M., Husson, M., Besson, M., Reperant, C., et al. (2013) · Molecular Psychiatry · doi:10.1038/mp.2012.83 · Cited by 151 · see citing works
Self-citationMicrobiota‐gut‐brain axis as a regulator of reward processes
García‐Cabrerizo, R., Carbia, C., O’Riordan, K. J., Schellekens, H., & Cryan, J. F. (2020) · Journal of Neurochemistry · doi:10.1111/jnc.15284 · Cited by 147 · see citing works
Glutamate Transporter GLT-1 as a Therapeutic Target for Substance Use Disorders
Roberts-Wolfe, D., & Kalivas, P. W. (2015) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/1871527314666150529144655 · Cited by 146 · see citing works
A potential role for the gut microbiome in substance use disorders
Meckel, K. R., & Kiraly, D. D. (2019) · Psychopharmacology · doi:10.1007/s00213-019-05232-0 · Cited by 141 · see citing works
Can’t or Won’t? Immunometabolic Constraints on Dopaminergic Drive
Treadway, M. T., Cooper, J. A., & Miller, A. H. (2019) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2019.03.003 · Cited by 134 · see citing works
Cell adhesion molecules at the synapse
Gerrow, K. (2006) · Frontiers in bioscience · doi:10.2741/1978 · Cited by 133 · see citing works
Engel, J. A., & Jerlhag, E. (2014) · CNS Drugs · doi:10.1007/s40263-014-0178-y · Cited by 132 · see citing works
Phenotypic clustering: a novel method for microglial morphology analysis
Verdonk, F., Roux, P., Flamant, P., Fiette, L., Bozza, F. A., Simard, S., Lemaire, M., Plaud, B., Shorte, S. L., Sharshar, T., et al. (2016) · Journal of Neuroinflammation · doi:10.1186/s12974-016-0614-7 · Cited by 132 · see citing works
Self-citationNeurobiological Mechanisms of Nicotine Reward and Aversion
Wills, L. P., Ables, J. L., Braunscheidel, K. M., Caligiuri, S. P. B., Elayouby, K. S., Fillinger, C., Ishikawa, M., Moen, J. K., & Kenny, P. J. (2022) · Pharmacological Reviews · doi:10.1124/pharmrev.121.000299 · Cited by 126 · see citing works
Ikemoto, S., & Bonci, A. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.04.031 · Cited by 122 · see citing works
Glial glutamate transporter expression patterns in brains from multiple mammalian species
Williams, S. M., Sullivan, R., Scott, H. L., Finkelstein, D. I., Colditz, P. B., Lingwood, B. E., Dodd, P. R., & Pow, D. V. (2004) · Glia · doi:10.1002/glia.20139 · Cited by 117 · see citing works
Zhao-Shea, R., Liu, L., Soll, L. G., Improgo, M. R., Meyers, E. E., McIntosh, J. M., Grady, S. R., Marks, M. J., Gardner, P. D., & Tapper, A. R. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.240 · Cited by 113 · see citing works
Tirelle, P., Breton, J., Riou, G., Déchelotte, P., Coëffier, M., & Ribet, D. (2020) · BMC Microbiology · doi:10.1186/s12866-020-02018-9 · Cited by 113 · see citing works
The antero-posterior heterogeneity of the ventral tegmental area
Sánchez-Catalán, M. J., Kaufling, J., Georges, F. E., Veinante, P., & Barrot, M. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.09.025 · Cited by 112 · see citing works
Long-term effects of chronic nicotine exposure on brain nicotinic receptors
Besson, M., Granon, S., Mameli-Engvall, M., Cloëz-Tayarani, I., Maubourguet, N., Cormier, A., Cazala, P., David, V., Changeux, J., & Fauré, P. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0702698104 · Cited by 109 · see citing works
Self-citationGlial and neuroinflammatory targets for treating substance use disorders
Bachtell, R. K., Jones, J. D., Heinzerling, K. G., Beardsley, P. M., & Comer, S. D. (2017) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2017.08.003 · Cited by 104 · see citing works
Dopaminergic and cholinergic learning mechanisms in nicotine addiction
Subramaniyan, M., & Dani, J. A. (2015) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12871 · Cited by 103 · see citing works
Koutzoumis, D. N., Vergara, M., Pino, J. A., Buddendorff, J., Khoshbouei, H., Mandel, R. J., & Torres, G. E. (2019) · Experimental Neurology · doi:10.1016/j.expneurol.2019.113159 · Cited by 103 · see citing works
The microbiota–microglia axis in central nervous system disorders
Mossad, O., & Erny, D. (2020) · Brain Pathology · doi:10.1111/bpa.12908 · Cited by 98 · see citing works
Sartor, C. E., Lessov-Schlaggar, C. N., Scherrer, J. F., Bucholz, K. K., Madden, P. A. F., Pergadia, M. L., Grant, J. D., Jacob, T., & Xian, H. (2010) · Addictive Behaviors · doi:10.1016/j.addbeh.2010.03.004 · Cited by 93 · see citing works
Chi, L., Mahbub, R., Gao, B., Bian, X., Tu, P., Ru, H., & Lü, K. (2017) · Chemical Research in Toxicology · doi:10.1021/acs.chemrestox.7b00162 · Cited by 90 · see citing works
David, V., Besson, M., Changeux, J.-P., Granon, S., & Cazala, P. (2006) · Neuropharmacology · doi:10.1016/j.neuropharm.2006.02.003 · Cited by 87 · see citing works
Self-citationStoker, A. K., Semenova, S., & Markou, A. (2008) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.03.013 · Cited by 85 · see citing works
Glial Modulators as Potential Treatments of Psychostimulant Abuse
Beardsley, P. M., & Hauser, K. F. (2014) · Advances in pharmacology · doi:10.1016/b978-0-12-420118-7.00001-9 · Cited by 82 · see citing works
Besson, M., David, V., Suarez, S., Cormier, A., Cazala, P., Changeux, J.-P., & Granon, S. (2006) · Psychopharmacology · doi:10.1007/s00213-006-0418-z · Cited by 73 · see citing works
Self-citationShort chain fatty acids induce TH gene expression via ERK-dependent phosphorylation of CREB protein
Shah, P. G., Nankova, B. B., Parab, S., & Gamma, E. F. L. (2006) · Brain Research · doi:10.1016/j.brainres.2006.05.097 · Cited by 70 · see citing works
Alajaji, M., Bowers, M. S., Knackstedt, L. A., & Damaj, M. I. (2013) · Psychopharmacology · doi:10.1007/s00213-013-3047-3 · Cited by 66 · see citing works
Glial mechanisms underlying substance use disorders
Linker, K. E., Cross, S. J., & Leslie, F. M. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14163 · Cited by 64 · see citing works
Ables, J. L., Görlich, A., Antolin‐Fontes, B., Wang, C., Lipford, S. M., Riad, M. H., Ren, J., Hu, F., Luo, M., Kenny, P. J., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1717506114 · Cited by 61 · see citing works
Reward system and addiction: what dopamine does and doesn’t do
Chiara, G. D., & Bassareo, V. (2007) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2007.02.001 · Cited by 59 · see citing works
Besson, M., David, V., Baudonnat, M., Cazala, P., Guilloux, J., Repérant, C., Cloëz-Tayarani, I., Changeux, J., Gardier, A. M., & Granon, S. (2011) · Psychopharmacology · doi:10.1007/s00213-011-2422-1 · Cited by 57 · see citing works
Self-citationElayouby, K. S., Ishikawa, M., Dukes, A. J., Smith, A. C. W., Lu, Q., Fowler, C. D., & Kenny, P. J. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.0127-19.2020 · Cited by 57 · see citing works
Clemens, K. J., Caillé, S., & Cador, M. (2010) · Psychopharmacology · doi:10.1007/s00213-010-1866-z · Cited by 56 · see citing works
An inhibitory brainstem input to dopamine neurons encodes nicotine aversion
Liu, C. J., Tose, A. J., Verharen, J. P. H., Zhu, Y., Tang, L. W., de Jong, J. W., Du, J. X., Beier, K. T., & Lammel, S. (2022) · Neuron · doi:10.1016/j.neuron.2022.07.003 · Cited by 55 · see citing works
Morton, G., Nasirova, N., Sparks, D. W., Brodsky, M., Sivakumaran, S., Lambe, E. K., & Turner, E. E. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.0023-18.2018 · Cited by 48 · see citing works
Hardaway, J. A., Sturgeon, S. M., Snarrenberg, C. L., Li, Z., Xu, X. Z. S., Bermingham, D. P., Odiase, P., Spencer, W. C., Miller, D. M., Carvelli, L., et al. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.0800-15.2015 · Cited by 44 · see citing works
Characterization of pharmacological and behavioral differences to nicotine in C57Bl/6 and DBA/2 mice
Jackson, K. J., Walters, C. L., Miles, M. F., Martin, B. R., & Damaj, M. I. (2009) · Neuropharmacology · doi:10.1016/j.neuropharm.2009.07.020 · Cited by 41 · see citing works
Verplaetse, T. L., Morris, E. D., McKee, S. A., & Cosgrove, K. (2018) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2018.04.004 · Cited by 41 · see citing works
A Human Polymorphism in CHRNA5 Is Linked to Relapse to Nicotine Seeking in Transgenic Rats
Forget, B., Scholze, P., Vives, F. L., Morel, C., Pons, S., Mondoloni, S., Besson, M., Cuttoli, R. D.-D., Hay, Y. A., Tricoire, L., et al. (2018) · Current Biology · doi:10.1016/j.cub.2018.08.044 · Cited by 41 · see citing works
Self-citationAssociation between the oral microbiome and brain resting state connectivity in smokers
Lin, D., Hutchison, K. E., Portillo, S., Vergara, V. M., Ellingson, J. M., Liu, J., Krauter, K. S., Carroll‐Portillo, A., & Calhoun, V. D. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.06.023 · Cited by 40 · see citing works
Harrington, L., Viñals, X., Herrera-Solís, A., Flores, Á., Morel, C., Tolu, S., Fauré, P., Maldonado, R. J., Maskos, U., & Robledo, P. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.346 · Cited by 36 · see citing works
Self-citationβ2* nAChRs on VTA dopamine and GABA neurons separately mediate nicotine aversion and reward
Grieder, T. E., Besson, M., Maal‐Bared, G., Pons, S., Maskos, U., & van der Kooy, D. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1908724116 · Cited by 36 · see citing works
Self-citationWild, A. R., Bollands, M., Morris, P. G., & Jones, S. (2015) · European Journal of Neuroscience · doi:10.1111/ejn.13075 · Cited by 34 · see citing works
Kongsui, R., Johnson, S. J., Graham, B. A., Nilsson, M., & Walker, F. R. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.09.061 · Cited by 31 · see citing works
Saravia, R., Flores, Á., Plaza‐Zabala, A., Busquets-García, A., Pastor, A., de la Torre, R., Marzo, V. D., Marsicano, G., Ozaita, A., Maldonado, R. J., et al. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.07.007 · Cited by 31 · see citing works
Fouyssac, M., & Belin, D. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14416 · Cited by 28 · see citing works
Ren, M., & Lotfipour, S. (2022) · Microorganisms · doi:10.3390/microorganisms10061127 · Cited by 27 · see citing works
Pizarro, N., Kossatz, E., González, P., Gamero, A., Veza-Estévez, E., Fernández, C., Gabaldón, T., de la Torre, R., & Robledo, P. (2021) · Frontiers in Nutrition · doi:10.3389/fnut.2021.750333 · Cited by 23 · see citing works
González‐González, I. M., García‐Tardón, N., Giménez, C., & Zafra, F. (2009) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2009.06125.x · Cited by 21 · see citing works
Husson, M., Harrington, L., Tochon, L., Cho, Y. H., Ibáñez-Tallon, I., Maskos, U., & David, V. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.0356-19.2020 · Cited by 21 · see citing works
Self-citationGlial regulation of synaptic function in models of addiction
Stellwagen, D., Kemp, G. M., Valade, S., & Chambon, J. (2019) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2019.02.010 · Cited by 20 · see citing works
VTA dopamine neuron plasticity – the unusual suspects
Xin, W., Edwards, N., & Bonci, A. (2016) · European Journal of Neuroscience · doi:10.1111/ejn.13425 · Cited by 17 · see citing works
Endocrine cross‐talk between the gut microbiome and glial cells in development and disease
Anbalagan, S. (2020) · Journal of Neuroendocrinology · doi:10.1111/jne.12924 · Cited by 9 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Microbiota–gut–brain axis and its therapeutic applications in neurodegenerative diseases
Loh, J. S., Mak, W. Q., Tan, L. K. S., Ng, C. X., Chan, H. H., Yeow, S. H., Foo, J. B., Ong, Y. S., How, C. W., & Khaw, K. Y. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-01743-1 · Cited by 1,193 · see citing works
Advancing lifelong precision medicine for cardiovascular diseases through gut microbiota modulation
Shi, B., Li, H., & He, X. (2024) · Gut Microbes · doi:10.1080/19490976.2024.2323237 · Cited by 42 · see citing works
Microbiota-Gut-Brain Axis in Psychiatry: Focus on Depressive Disorders
Wang, I.-C., Buffington, S. A., & Salas, R. (2024) · Current Epidemiology Reports · doi:10.1007/s40471-024-00349-z · Cited by 22 · see citing works
Neurobiological mechanisms of nicotine's effects on feeding and body weight
Li, Y., Mao, J., Chai, G., Zheng, R., Liu, X., & Xie, J. (2025) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2025.106021 · Cited by 11 · see citing works
Boiangiu, R. Ş., Brinza, I., Honceriu, I., Mihăşan, M., & Hriţcu, L. (2023) · Biomolecules · doi:10.3390/biom14010023 · Cited by 10 · see citing works
Radford‐Smith, D. E., Oke, K., Costa, C. F. F. A., & Anthony, D. C. (2025) · Brain Behavior & Immunity - Health · doi:10.1016/j.bbih.2025.101013 · Cited by 8 · see citing works
The Gut–Brain–Immune Axis in Glioma: Emerging Mechanisms and Therapeutic Opportunities
Feng, R., Yang, Z., Zhou, Y., & Zhao, H. (2026) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-026-01680-3 · Cited by 7 · see citing works
Neuroglia in substance use disorders
Castro, E. M., Lotfipour, S., & Leslie, F. M. (2025) · Handbook of clinical neurology · doi:10.1016/b978-0-443-19102-2.00014-4 · Cited by 1 · see citing works
de Chaumont, F., Icick, R., Gorwood, P. A. P. M., Granon, S., Forget, B., Bouarab, C., Mattioni, J., Bourgeron, T., Maskos, U., Ramoz, N., et al. (2025) · Translational Psychiatry · doi:10.1038/s41398-025-03725-5 · Cited by 1 · see citing works
Self-citationThe role of the gut microbiome in nicotine withdrawal and dependence
Köşeli, E., Tyc, K. M., Buzzi, B., Akbarali, H. I., & Damaj, M. I. (2026) · Nicotine & Tobacco Research · doi:10.1093/ntr/ntag057 · Cited by 1 · see citing works
- Authors
- Lakosa, A., Rahimian, A., Tomasi, F., Marti, F., Reynolds, L. M., Tochon, L., David, V., Danckaert, A., Canonne, C., Tahraoui, S., de Chaumont, F., Forget, B., Maskos, U., & Besson, M.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Institut Pasteur (FR)
- Corresponding author
- Besson, Morgane
- ORCID
- Venue
- Neuropsychopharmacology
- Published
- 2023-03-17
- Volume
- 48
- Issue
- 6
- Pages
- 963-974
- ISSN
- 0893-133X (ISSN-L)
- 1740-634X
- PMC
- PMC10156728
- OpenAlex
- W4327745362
- Cited by
- 10
- References
- 92
- Citations by year
- 2026: 2 · 2025: 4 · 2024: 3 · 2023: 1
- FWCI
- 1.21
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- Locations
- Neuropsychopharmacology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion, cc-by-nc)
- Funders
- Agence Nationale de la Recherche (ANR-10-INSB-04-01, “Investments for the future”)
- Institut Pasteur (GPF Microbes and Brain, project “µBIOTADDICT”)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Keywords
- gut microbiota, nicotine dependence, ventral tegmental area, mesolimbic system, glial cells, microglia, astrocytes, PSD-95, GLT-1, drug reward, nicotine self-administration, gut dysbiosis, nicotine withdrawal
- MeSH terms
- Gastrointestinal Microbiome, Animals, Dopamine, Male, Neuroglia, Nicotine, Reward, Substance Withdrawal Syndrome, Ventral Tegmental Area, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
