Cue reactivity; Dorsolateral prefrontal cortex; Reward availability; Ventral striatum; fMRI; rTMS; Humans; Prefrontal Cortex/physiology; Brain; Transcranial Magnetic Stimulation/methods; Reward; Dorsolateral Prefrontal Cortex; Cues; Prefrontal Cortex; Transcranial Magnetic Stimulation; Neuropsychology and Physiological Psychology; Experimental and Cognitive Psychology; Cognitive Neuroscience
Résumé :
[en] Brain imaging studies have shown that stimulation of the left dorsolateral prefrontal cortex (dlPFC), which plays a pivotal role in high-order cognitive control processes, modulates brain reactivity to reward-related cues. Nevertheless, the impact of contextual factors such as reward availability (the reward that is depicted in the cue exposure task) on such modulation effect remains unclear. Here we tested whether a single session of high-frequency repetitive transcranial magnetic stimulation (HF-rTMS) over the left dlPFC differently impacts brain reactivity to cues signalling either availability or unavailability of a sports betting opportunity. Employing a within-subject design (verum versus sham HF-rTMS) among thirty-two frequent sports bettors, we first observed that, as compared to the sham condition, verum HF-rTMS modulated brain reactivity to game cues prior to being made (un)available for betting, through simultaneous increases (posterior insula and caudate nucleus) and decreases (occipital pole) in brain activation. Second, verum HF-rTMS led to increased ventral striatal activity towards cues available for betting but did not modulate brain response to cues unavailable for betting. Taken together, these findings demonstrate that transient stimulation of the left dlPFC led to a general modulation in brain activity in responses to cues, and that this effect is only partly dependent on cues signalling for reward (un)availability.
Disciplines :
Neurosciences & comportement
Auteur, co-auteur :
BREVERS, Damien ✱; University of Luxembourg > Faculty of Humanities, Education and Social Sciences > Department of Behavioural and Cognitive Sciences > Team Claus VÖGELE
Baeken, Chris; Department of Psychiatry University Hospital (UZBrussel), Brussels, Belgium, Ghent Experimental Psychiatry (GHEP) Lab, Ghent, Belgium, Department of Head and Skin, Ghent University Hospital, Ghent University, Ghent, Belgium, Eindhoven University of Technology, Department of Electrical Engineering, Eindhoven, the Netherlands
De Smet, Stefanie; Ghent Experimental Psychiatry (GHEP) Lab, Ghent, Belgium
Catoira, Beatriz; Department of Psychiatry University Hospital (UZBrussel), Brussels, Belgium
De Witte, Sara; Ghent Experimental Psychiatry (GHEP) Lab, Ghent, Belgium
He, Qinghua; Faculty of Psychology, Southwest University, 2 Tiansheng Rd, Chongqing, China
Maurage, Pierre; Louvain for Experimental Psychopathology Research Group (LEP), Psychological Sciences Research Institute (IPSY), UCLouvain, Louvain-la-Neuve, Belgium
SCHULZE-STEINEN, Laimi Marja Elina ; University of Luxembourg > Faculty of Humanities, Education and Social Sciences > Department of Behavioural and Cognitive Sciences > Team Claus VÖGELE
Sescousse, Guillaume; Lyon Neuroscience Research Center - INSERM U1028 - CNRS UMR5292, PSYR2 Team, University of Lyon, Lyon, France
Verde, Claudia Vila; Institute for Health and Behaviour, Department of Behavioural and Cognitive Sciences, University of Luxembourg, Esch-sur-Alzette, Luxembourg
VÖGELE, Claus ; University of Luxembourg > Faculty of Humanities, Education and Social Sciences (FHSE) > Department of Behavioural and Cognitive Sciences (DBCS) > Health and Behaviour
Billieux, Joël ✱; Institute of Psychology, University of Lausanne, Lausanne, Switzerland, Centre for Excessive Gambling, Addiction Medicine, Lausanne University Hospitals (CHUV), Lausanne, Switzerland
✱ Ces auteurs ont contribué de façon équivalente à la publication.
Co-auteurs externes :
yes
Langue du document :
Anglais
Titre :
Stimulation of the dorsolateral prefrontal cortex modulates brain cue reactivity to reward (un)availability.
Date de publication/diffusion :
juillet 2023
Titre du périodique :
Cortex: A Journal Devoted to the Study of the Nervous System and Behavior
R-AGR-3548 - C18/BM/12552025 BETHAB - part UL - VÖGELE Claus
Organisme subsidiant :
FNR - Fonds National de la Recherche
Subventionnement (détails) :
The work of D.B. is supported by the Luxembourg National Research Fund (FNR) ; CORE – Junior Track [BETHAB; C18/BM/12552025 ]. P.M. (Senior Research Associate) is funded by the Belgian Fund for Scientific Research (F.R.S.-FNRS, Belgium). These funds did not exert any editorial direction or censorship on any part of this article. All authors declare no conflicts of interest relevant to this manuscript. The authors would like to thank Anita Cebolla and Mathieu Petieau for their help in running the brain stimulation sessions.
Barch, D.M., Sheline, Y.I., Csernansky, J.G., Snyder, A.Z., Working memory and prefrontal cortex dysfunction: Specificity to schizophrenia compared with major depression. Biological psychiatry 53:5 (2003), 376–384, 10.1016/s0006-3223(02)01674-8.
Blechert, J., Klackl, J., Miedl, S.F., Wilhelm, F.H., To eat or not to eat: Effects of food availability on reward system activity during food picture viewing. Appetite 99 (2016), 254–261, 10.1016/j.appet.2016.01.006.
Brevers, D., Baeken, C., Bechara, A., He, Q., Maurage, P., Petieau, M., Sescousse, G., Vögele, C., Billieux, J., Increased brain reactivity to gambling unavailability as a marker of problem gambling. Addiction Biology, 26(4), 2021, e12996, 10.1111/adb.12996.
Brevers, D., Bechara, A., Cleeremans, A., Noël, X., Iowa Gambling Task (IGT): Twenty years after - gambling disorder and IGT. Frontiers in Psychology, 4, 2013, 665, 10.3389/fpsyg.2013.00665.
Brevers, D., Herremans, S.C., He, Q., Vanderhasselt, M.-A., Petieau, M., Verdonck, D., Poppa, T., De Witte, S., Kornreich, C., Bechara, A., Baeken, C., Facing temptation: The neural correlates of gambling availability during sports picture exposure. Cognitive, Affective & Behavioral Neuroscience 18:4 (2018), 718–729, 10.3758/s13415-018-0599-z.
Brevers, D., Sescousse, G., Maurage, P., Billieux, J., Examining neural reactivity to gambling cues in the age of online betting. Current Behavioral Neuroscience Reports 6:3 (2019), 59–71, 10.1007/s40473-019-00177-2.
Brevers, D., Vögele, C., Billieux, J., The evolving landscape of sports betting: A risk for young people?. Heinen, A., (eds.) Well-being and health among young people, 2022, Springer International Publishing.
Brunoni, A.R., Vanderhasselt, M.-A., Working memory improvement with non-invasive brain stimulation of the dorsolateral prefrontal cortex: A systematic review and meta-analysis. Brain and Cognition 86 (2014), 1–9, 10.1016/j.bandc.2014.01.008.
Chiang, T.C., Lu, R.B., Hsieh, S., Chang, Y.H., Yang, Y.K., Stimulation in the dorsolateral prefrontal cortex changes subjective evaluation of percepts. Plos One, 9(9), 2014, e106943, 10.1371/journal.pone.0106943.
Claus, E.D., Ewing, S.W.F., Filbey, F.M., Sabbineni, A., Hutchison, K.E., Identifying neurobiological phenotypes associated with alcohol use disorder severity. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology 36:10 (2011), 2086–2096, 10.1038/npp.2011.99.
Cosme, D., Ludwig, R.M., Berkman, E.T., Comparing two neurocognitive models of self-control during dietary decisions. [Social Cognitive and Affective Neuroscience Electronic Resource] 14:9 (2019), 957–966, 10.1093/scan/nsz068.
Courtney, K.E., Schacht, J.P., Hutchison, K., Roche, D.J.O., Ray, L.A., Neural substrates of cue reactivity: Association with treatment outcomes and relapse. Addiction Biology 21:1 (2016), 3–22, 10.1111/adb.12314.
D'Esposito, M., Detre, J.A., Alsop, D.C., Shin, R.K., Atlas, S., Grossman, M., The neural basis of the central executive system of working memory. Nature 378:6554 (1995), 279–281, 10.1038/378279a0.
D'Esposito, M., Postle, B.R., Rypma, B., Prefrontal cortical contributions to working memory: Evidence from event-related fMRI studies. Experimental Brain Research 133:1 (2000), 3–11, 10.1007/s002210000395.
Devoto, F., Zapparoli, L., Spinelli, G., Scotti, G., Paulesu, E., How the harm of drugs and their availability affect brain reactions to drug cues: A meta-analysis of 64 neuroimaging activation studies. Translational Psychiatry, 10, 2020, 429, 10.1038/s41398-020-01115-7.
Ekhtiari, H., Zare-Bidoky, M., Sangchooli, A., Janes, A.C., Kaufman, M.J., Oliver, J.A., Prisciandaro, J.J., Wüstenberg, T., Anton, R.F., Bach, P., Baldacchino, A., Beck, A., Bjork, J.M., Brewer, J., Childress, A.R., Claus, E.D., Courtney, K.E., Ebrahimi, M., Filbey, F.M., Zilverstand, A., A methodological checklist for fMRI drug cue reactivity studies: Development and expert consensus. Nature Protocols 17:3 (2022), 567–595, 10.1038/s41596-021-00649-4.
Ferris, J., Wynne, H., The Canadian problem gambling Index: Final report., 2001, Canadian Centre on Substance Abuse, Ottawa, ON.
Filimon, F., Nelson, J.D., Sejnowski, T.J., Sereno, M.I., Cottrell, G.W., The ventral striatum dissociates information expectation, reward anticipation, and reward receipt. Proceedings of the National Academy of Sciences of the United States of America 117:26 (2020), 15200–15208, 10.1073/pnas.1911778117.
Flayelle, M., Brevers, D., King, D.L., Maurage, P., Perales, C.J., Billieux, J., A taxonomy of technology design features that promote potentially addictive online behaviours. Nature Psychology Reviews 2 (2023), 136–150, 10.1038/s44159-023-00153-4.
George, O., Koob, G.F., Individual differences in prefrontal cortex function and the transition from drug use to drug dependence. Neuroscience and Biobehavioral Reviews 35:2 (2010), 232–247, 10.1016/j.neubiorev.2010.05.002.
George, O., Koob, G.F., Control of craving by the prefrontal cortex. Proceedings of the National Academy of Sciences of the United States of America 110:11 (2013), 4165–4166, 10.1073/pnas.1301245110.
Hanlon, C.A., Dowdle, L.T., Naselaris, T., Canterberry, M., Cortese, B.M., Visual cortex activation to drug cues: A meta-analysis of functional neuroimaging papers in addiction and substance abuse literature. Drug and Alcohol Dependence 143 (2014), 206–212, 10.1016/j.drugalcdep.2014.07.028.
Hayashi, T., Ko, J.H., Strafella, A.P., Dagher, A., Dorsolateral prefrontal and orbitofrontal cortex interactions during self-control of cigarette craving. Proceedings of the National Academy of Sciences of the United States of America 110:11 (2013), 4422–4427, 10.1073/pnas.1212185110.
Herremans, S.C., Van Schuerbeek, P., De Raedt, R., Matthys, F., Buyl, R., De Mey, J., Baeken, C., The impact of accelerated right prefrontal high-frequency repetitive transcranial magnetic stimulation (rTMS) on cue-reactivity: An fMRI study on craving in recently detoxified alcohol-dependent patients. Plos One, 10(8), 2015, e0136182, 10.1371/journal.pone.0136182.
Hill-Bowen, L.D., Riedel, M.C., Poudel, R., Salo, T., Flannery, J.S., Camilleri, J.A., Eickhoff, S.B., Laird, A.R., Sutherland, M.T., The cue-reactivity paradigm: An ensemble of networks driving attention and cognition when viewing drug and natural reward-related stimuli. Neuroscience and Biobehavioral Reviews 130 (2021), 201–213, 10.1016/j.neubiorev.2021.08.010.
Howard, J.D., Kahnt, T., Identity-specific reward representations in orbitofrontal cortex are modulated by selective devaluation. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience 37:10 (2017), 2627–2638, 10.1523/JNEUROSCI.3473-16.2017.
Jasinska, A.J., Stein, E.A., Kaiser, J., Naumer, M.J., Yalachkov, Y., Factors modulating neural reactivity to drug cues in addiction: A survey of human neuroimaging studies. Neuroscience and Biobehavioral Reviews 38 (2014), 1–16, 10.1016/j.neubiorev.2013.10.013.
Jauhar, S., Fortea, L., Solanes, A., Albajes-Eizagirre, A., McKenna, P.J., Radua, J., Brain activations associated with anticipation and delivery of monetary reward: A systematic review and meta-analysis of fMRI studies. PloS one, 16(8), 2021, e0255292 https://doi.org/10.1371/journal.pone.0255292.
Knutson, B., Cooper, J.C., Functional magnetic resonance imaging of reward prediction. Current Opinion in Neurology 18:4 (2005), 411–417, 10.1097/01.wco.0000173463.24758.f6.
Lee, M.R., Caparelli, E.C., Leff, M., Steele, V.R., Maxwell, A.M., McCullough, K., Salmeron, B.J., Repetitive transcranial magnetic stimulation delivered with an H-coil to the right insula reduces functional connectivity between insula and medial prefrontal cortex. Neuromodulation: journal of the International Neuromodulation Society 23:3 (2020), 384–392, 10.1111/ner.13033.
Leotti, L.A., Delgado, M.R., The inherent reward of choice. Psychological Science 22:10 (2011), 1310–1318, 10.1177/0956797611417005.
Li, X., Sahlem, G.L., Badran, B.W., McTeague, L.M., Hanlon, C.A., Hartwell, K.J., Henderson, S., George, M.S., Transcranial magnetic stimulation of the dorsal lateral prefrontal cortex inhibits medial orbitofrontal activity in smokers. The American Journal on Addictions 26:8 (2017), 788–794, 10.1111/ajad.12621.
Lopatina, N., McDannald, M.A., Styer, C.V., Sadacca, B.F., Cheer, J.F., Schoenbaum, G., Lateral orbitofrontal neurons acquire responses to upshifted, downshifted, or blocked cues during unblocking. ELife, 4, 2015, e11299, 10.7554/eLife.11299.
Mansouri, F.A., Tanaka, K., Buckley, M.J., Conflict-induced behavioural adjustment: A clue to the executive functions of the prefrontal cortex. Nature reviews. Neuroscience 10:2 (2009), 141–152, 10.1038/nrn2538.
McBride, D., Barrett, S.P., Kelly, J.T., Aw, A., Dagher, A., Effects of expectancy and abstinence on the neural response to smoking cues in cigarette smokers: An fMRI study. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology 31:12 (2006), 2728–2738, 10.1038/sj.npp.1301075.
Monterosso, J., Luo, S., Willpower is not synonymous with "executive function. The Behavioral and Brain Sciences 36:6 (2013), 700–726, 10.1017/S0140525X1300112X.
Noël, X., Brevers, D., Bechara, A., A neurocognitive approach to understanding the neurobiology of addiction. Current Opinion in Neurobiology 23:4 (2013), 632–638, 10.1016/j.conb.2013.01.018.
O'Doherty, J., Critchley, H., Deichmann, R., Dolan, R.J., Dissociating valence of outcome from behavioral control in human orbital and ventral prefrontal cortices. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience 23:21 (2003), 7931–7939, 10.1523/JNEUROSCI.23-21-07931.2003.
Pulopulos, M.M., Allaert, J., Vanderhasselt, M.-A., Sanchez-Lopez, A., De Witte, S., Baeken, C., De Raedt, R., Effects of HF-rTMS over the left and right DLPFC on proactive and reactive cognitive control. [Social Cognitive and Affective Neuroscience Electronic Resource] 17:1 (2022), 109–119, 10.1093/scan/nsaa082.
Rossi, S., Antal, A., Bestmann, S., Bikson, M., Brewer, C., Brockmöller, J., Carpenter, L. L., Cincotta, M., Chen, R., Daskalakis, J. D., Di Lazzaro, V., Fox, M. D., George, M. S., Gilbert, D., Kimiskidis, V. K., Koch, G., Ilmoniemi, R. J., Lefaucheur, J. P., Leocani, L., Lisanby, S. H., … basis of this article began with a Consensus Statement from the IFCN Workshop on "Present, Future of TMS: Safety, Ethical Guidelines", Siena, October 17-20, 2018, updating through April 2020 (2021). Safety and recommendations for TMS use in healthy subjects and patient populations, with updates on training, ethical and regulatory issues: Expert Guidelines. Clinical neurophysiology: official journal of the International Federation of Clinical Neurophysiology, 132(1), 269–306. https://doi.org/10.1016/j.clinph.2020.10.003.
Rossi, S., Hallett, M., Rossini, P.M., Pascual-Leone, A., Safety of TMS Consensus Group. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clinical Neurophysiology: Official Journal of the International Federation of Clinical Neurophysiology 120:12 (2009), 2008–2039, 10.1016/j.clinph.2009.08.016.
Saunders, J.B., Aasland, O.G., Babor, T.F., de la Fuente, J.R., Grant, M., Development of the alcohol use Disorders identification test (AUDIT): WHO collaborative Project on early detection of persons with harmful alcohol consumption—II. Addiction 88 (1993), 791–804, 10.1111/j.1360-0443.1993.tb02093.x.
Shekhar, M., Rahnev, D., Distinguishing the roles of dorsolateral and anterior PFC in visual metacognition. The Journal of neuroscience: the official journal of the Society for Neuroscience 38:22 (2018), 5078–5087, 10.1523/JNEUROSCI.3484-17.2018.
Stalnaker, T.A., Cooch, N.K., Schoenbaum, G., What the orbitofrontal cortex does not do. Nature Neuroscience 18:5 (2015), 620–627, 10.1038/nn.3982.
Thut, G., Pascual-Leone, A., A review of combined TMS-EEG studies to characterize lasting effects of repetitive TMS and assess their usefulness in cognitive and clinical neuroscience. Brain topography 22:4 (2010), 219–232, 10.1007/s10548-009-0115-4.
Vanderhasselt, M.A., De Raedt, R., Baeken, C., Leyman, L., D'Haenen, H., A single session of rTMS over the left dorsolateral prefrontal cortex influences attentional control in depressed patients. The world journal of biological psychiatry: the official journal of the World Federation of Societies of Biological Psychiatry 10:1 (2009), 34–42, 10.1080/15622970701816514.
Wang, K.S., Yang, Y.-Y., Delgado, M.R., How perception of control shapes decision making. Current Opinion in Behavioral Sciences 41 (2021), 85–91, 10.1016/j.cobeha.2021.04.003.
Wilson, S.J., Creswell, K.G., Sayette, M.A., Fiez, J.A., Ambivalence about smoking and cue-elicited neural activity in quitting-motivated smokers faced with an opportunity to smoke. Addictive Behaviors 38:2 (2013), 1541–1549, 10.1016/j.addbeh.2012.03.020.
Wilson, S.J., Sayette, M.A., Delgado, M.R., Fiez, J.A., Instructed smoking expectancy modulates cue-elicited neural activity: A preliminary study. Nicotine & Tobacco Research: Official Journal of the Society for Research on Nicotine and Tobacco 7:4 (2005), 637–645, 10.1080/14622200500185520.
Wilson, S.J., Sayette, M.A., Fiez, J.A., Prefrontal responses to drug cues: A neurocognitive analysis. Nature Neuroscience 7:3 (2004), 211–214, 10.1038/nn1200.
Wilson, S.J., Sayette, M.A., Fiez, J.A., Quitting-unmotivated and quitting-motivated cigarette smokers exhibit different patterns of cue-elicited brain activation when anticipating an opportunity to smoke. Journal of Abnormal Psychology 121:1 (2012), 198–211, 10.1037/a0025112.
Yalachkov, Y., Kaiser, J., Naumer, M.J., Functional neuroimaging studies in addiction: Multisensory drug stimuli and neural cue reactivity. Neuroscience and Biobehavioral Reviews 36:2 (2012), 825–835, 10.1016/j.neubiorev.2011.12.004.
Yang, L.-Z., Shi, B., Li, H., Zhang, W., Liu, Y., Wang, H., Zhou, Y., Wang, Y., Lv, W., Ji, X., Hudak, J., Zhou, Y., Fallgatter, A.J., Zhang, X., Electrical stimulation reduces smokers' craving by modulating the coupling between dorsal lateral prefrontal cortex and parahippocampal gyrus. [Social Cognitive and Affective Neuroscience Electronic Resource] 12:8 (2017), 1296–1302, 10.1093/scan/nsx055.
