Higher-order comparative reward processing is affected by noninvasive stimulation of the ventromedial prefrontal cortex.

magnetoencephalography reward processing transcranial direct current stimulation ventromedial prefrontal cortex

Journal

Journal of neuroscience research
ISSN: 1097-4547
Titre abrégé: J Neurosci Res
Pays: United States
ID NLM: 7600111

Informations de publication

Date de publication:
Mar 2024
Historique:
revised: 17 08 2023
received: 31 05 2023
accepted: 10 09 2023
pubmed: 10 10 2023
medline: 10 10 2023
entrez: 10 10 2023
Statut: ppublish

Résumé

A crucial skill, especially in rapidly changing environments, is to be able to learn efficiently from prior rewards or losses and apply this acquired knowledge in upcoming situations. Often, we must weigh the risks of different options and decide whether an option is worth the risk or whether we should choose a safer option. The ventromedial prefrontal cortex (vmPFC) is suggested as a major hub for basic but also higher-order reward processing. Dysfunction in this region has been linked to cognitive risk factors for depression and behavioral addictions, including reduced optimism and feedback learning. Here, we test whether modulations of vmPFC excitability via noninvasive transcranial direct current stimulation (tDCS) can alter reward anticipation and reward processing. In a financial gambling task, participants chose between a higher and a lower monetary risk option and eventually received feedback whether they won or lost. Simultaneously feedback on the unchosen option was presented as well. Behavioral and magnetoencephalographic correlates of reward processing were evaluated in direct succession of either excitatory or inhibitory tDCS of the vmPFC. We were able to show modulated reward approach behavior (expectancy of greater reward magnitudes) as well as altered reevaluation of received feedback by vmPFC tDCS as indicated by modified choice behavior following the feedback. Thereby, tDCS not only influenced early, rather basic reward processing, but it also modulated higher-order comparative feedback evaluation of gains and losses relative to alternative outcomes. The neural results underline this idea, as stimulation-driven modulations of the basic reward-related effect occurred at rather early time intervals and were followed by stimulation effects related to comparative reward processing. Importantly, behavioral ratings were correlated with neural activity in left frontal areas. Our results imply a dual function of the vmPFC consisting of approaching reward (as indicated by more risky choices) and elaborately evaluating outcomes. In addition, our data suggest that vmPFC activity is associated with adaptive decision-making in the future via modulated behavioral adaptation or reinforcement learning.

Identifiants

pubmed: 37815024
doi: 10.1002/jnr.25248
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e25248

Subventions

Organisme : Deutsche Forschungsgemeinschaft
ID : JU 445/9-1
Organisme : Narodowe Centrum Nauki
ID : UMO-2018/31/G/HS6/02490
Organisme : Interdisciplinary Center for Clinical Research of the University of Muenster
ID : Ju2/024/15

Informations de copyright

© 2023 The Authors. Journal of Neuroscience Research published by Wiley Periodicals LLC.

Références

Adrián-Ventura, J., Costumero, V., Parcet, M. A., & Ávila, C. (2019). Reward network connectivity “at rest” is associated with reward sensitivity in healthy adults: A resting-state fMRI study. Cognitive, Affective, & Behavioral Neuroscience, 19(3), 726-736. https://doi.org/10.3758/s13415-019-00688-1
Baayen, R. H., Davidson, D. J., & Bates, D. M. (2008). Mixed-effects modeling with crossed random effects for subjects and items. Journal of Memory and Language, 59(4), 390-412. https://doi.org/10.1016/j.jml.2007.12.005
Bechara, A. (2013). Chapter 35-The neural basis of decision making in addiction. In A. Miller (Ed.), Biological research on addiction (pp. 341-352). Academic Press. https://doi.org/10.1016/B978-0-12-398335-0.00035-2
Beck, A. T., Steer, R. A., & Brown, G. K. (1996). BDI-II. The Psychological Corporation.
Bialleck, K. A., Schaal, H. P., Kranz, T. A., Fell, J., Elger, C. E., & Axmacher, N. (2011). Ventromedial prefrontal cortex activation is associated with memory formation for predictable rewards. PLoS One, 6(2). https://doi.org/10.1371/journal.pone.0016695
Boyer, T. W. (2006). The development of risk-taking: A multi-perspective review. Developmental Review, 26(3), 291-345. https://doi.org/10.1016/j.dr.2006.05.002
Caballero-Insaurriaga, J., Pineda-Pardo, J. A., Obeso, I., Oliviero, A., & Foffani, G. (2023). Noninvasive modulation of human corticostriatal activity. Proceedings of the National Academy of Sciences, 120(15), e2219693120. https://doi.org/10.1073/pnas.2219693120
Cao, Z., Bennett, M., Orr, C., Icke, I., Banaschewski, T., Barker, G. J., Bokde, A. L. W., Bromberg, U., Büchel, C., Quinlan, E. B., Desrivières, S., Flor, H., Frouin, V., Garavan, H., Gowland, P., Heinz, A., Ittermann, B., Martinot, J. L., Nees, F., … Whelan, R. (2019). Mapping adolescent reward anticipation, receipt, and prediction error during the monetary incentive delay task. Human Brain Mapping, 40(1), 262-283. https://doi.org/10.1002/hbm.24370
Carlson, J. M., Foti, D., Mujica-Parodi, L. R., Harmon-Jones, E., & Hajcak, G. (2011). Ventral striatal and medial prefrontal BOLD activation is correlated with reward-related electrocortical activity: A combined ERP and fMRI study. NeuroImage, 57(4), 1608-1616. https://doi.org/10.1016/j.neuroimage.2011.05.037
Chapman, J., Dean, M., Ortoleva, P., Snowberg, E., & Camerer, C. (2023). Econographics. Journal of Political Economy Microeconomics, 1(1), 115-161.
Chib, V. S., Yun, K., Takahashi, H., & Shimojo, S. (2013). Noninvasive remote activation of the ventral midbrain by transcranial direct current stimulation of prefrontal cortex. Translational Psychiatry, 3(6), e268. https://doi.org/10.1038/tp.2013.44
Crowne, D. P., & Marlowe, D. (1960). A new scale of social desirability independent of psychopathology. Journal of Consulting Psychology, 24(4), 349-354. https://doi.org/10.1037/h0047358
Damasio, A. R. (1996). The somatic marker hypothesis and the possible functions of the prefrontal cortex. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 351(1346), 1413-1420. https://doi.org/10.1098/rstb.1996.0125
Delgado, M. R., Beer, J. S., Fellows, L. K., Huettel, S. A., Platt, M. L., Quirk, G. J., & Schiller, D. (2016). Viewpoints: Dialogues on the functional role of the ventromedial prefrontal cortex. Nature Neuroscience, 19(12), 1545-1552. https://doi.org/10.1038/nn.4438
Dennison, J. B., Sazhin, D., & Smith, D. V. (2022). Decision neuroscience and neuroeconomics: Recent progress and ongoing challenges. Wiley Interdisciplinary Reviews: Cognitive Science, 13(3), 1-43. https://doi.org/10.1002/wcs.1589
Farahani, F., Kronberg, G., FallahRad, M., Oviedo, H. V., & Parra, L. C. (2021). Effects of direct current stimulation on synaptic plasticity in a single neuron. Brain Stimulation, 14(3), 588-597. https://doi.org/10.1016/j.brs.2021.03.001
Fields, E. C., Weber, K., Stillerman, B., Delaney-Busch, N., & Kuperberg, G. R. (2019). Functional MRI reveals evidence of a self-positivity bias in the medial prefrontal cortex during the comprehension of social vignettes. Social Cognitive and Affective Neuroscience, 14(6), 613-621. https://doi.org/10.1093/scan/nsz035
Gehring, W. J., & Willoughby, A. R. (2002). The medial frontal cortex and the rapid processing of monetary gains and losses. Science, 295(5563), 2279-2282. https://doi.org/10.1126/science.1066893
Gerlach, A. L., Andor, T., & Patzelt, J. (2008). Die bedeutung von unsicherheits-intoleranz für die generalisierte angststörung: Modellüberlegungen und Entwicklung einer deutschen version der unsicherheitsintoleranz-skala. Zeitschrift Fur Klinische Psychologie Und Psychotherapie, 37(3), 190-199. https://doi.org/10.1026/1616-3443.37.3.190
Gross, J., Junghöfer, M., & Wolters, C. (2023). Bioelectromagnetism in human brain research: New applications, new questions. The Neuroscientist, 29, 62-77. https://doi.org/10.1177/10738584211054742
Hämäläinen, M. S., & Ilmoniemi, R. J. (1994). Interpreting magnetic fields of the brain: Minimum norm estimates. Medical & Biological Engineering & Computing, 32(1), 35-42. https://doi.org/10.1007/BF02512476
Hiser, J., & Koenigs, M. (2018). The multifaceted role of the ventromedial prefrontal cortex in emotion, decision making, social cognition, and psychopathology. Biological Psychiatry, 83(8), 638-647. https://doi.org/10.1016/j.biopsych.2017.10.030
Holroyd, C. B., & Coles, M. G. H. (2002). The neural basis of human error processing: Reinforcement learning, dopamine, and the error-related negativity. Psychological Review, 109(4), 679-709. https://doi.org/10.1037/0033-295X.109.4.679
Junghöfer, M., Bradley, M. M., Elbert, T. R., & Lang, P. J. (2001). Fleeting images: A new look at early emotion discrimination. Psychophysiology, 38(2), 175-178.
Junghöfer, M., Elbert, T., Tucker, D. M., & Rockstroh, B. (2000). Statistical control of artifacts in dense array EEG/MEG studies. Psychophysiology, 37(4), 523-532. https://doi.org/10.1111/1469-8986.3740523
Junghofer, M., Winker, C., Rehbein, M. A., & Sabatinelli, D. (2017). Noninvasive stimulation of the ventromedial prefrontal cortex enhances pleasant scene processing. Cerebral Cortex, 27(6), 3449-3456. https://doi.org/10.1093/cercor/bhx073
Kimbrell, T. A., Dunn, R. T., George, M. S., Danielson, A. L., Willis, M. W., Repella, J. D., Benson, B. E., Herscovitch, P., Post, R. M., & Wassermann, E. M. (2002). Left prefrontal-repetitive transcranial magnetic stimulation (rTMS) and regional cerebral glucose metabolism in normal volunteers. Psychiatry Research: Neuroimaging, 115(3), 101-113. https://doi.org/10.1016/S0925-4927(02)00041-0
Klein-Flügge, M. C., Bongioanni, A., & Rushworth, M. F. S. (2022). Medial and orbital frontal cortex in decision-making and flexible behavior. Neuron, 110(17), 2743-2770. https://doi.org/10.1016/j.neuron.2022.05.022
Knutson, B., Fong, G. W., Bennett, S. M., Adams, C. M., & Hommer, D. (2003). A region of mesial prefrontal cortex tracks monetarily rewarding outcomes: Characterization with rapid event-related fMRI. NeuroImage, 18(2), 263-272. https://doi.org/10.1016/S1053-8119(02)00057-5
Kroker, T., Wyczesany, M., Rehbein, M. A., Roesmann, K., Wessing, I., & Junghöfer, M. (2022a). Noninvasive stimulation of the ventromedial prefrontal cortex modulates rationality of human decision-making. Scientific Reports, 12(1), 20213. https://doi.org/10.1038/s41598-022-24526-6
Kroker, T., Wyczesany, M., Rehbein, M. A., Roesmann, K., Wessing, I., & Junghöfer, M. (2022b). Noninvasive stimulation of the ventromedial prefrontal cortex reduces cognitive gambling biases via improved feedback learning. accepted at: Scientific Reports.
Lang, P. J., Bradley, M. M., Fitzsimmons, J. R., Cuthbert, B. N., Scott, J. D., Moulder, B., & Nangia, V. (1998). Emotional arousal and activation of the visual cortex: An fMRI analysis. Psychophysiology, 35(2), 199-210. https://doi.org/10.1017/S0048577298001991
Lee, D., Seo, H., & Jung, M. W. (2012). Neural basis of reinforcement learning and decision making. Annual Review of Neuroscience, 35, 287-308. https://doi.org/10.1146/annurev-neuro-062111-150512
Linden, D. E. J. (2005). The P300: Where in the brain is it produced and what does it tell us? The Neuroscientist, 11(6), 563-576. https://doi.org/10.1177/1073858405280524
Liu, X., Hairston, J., Schrier, M., & Fan, J. (2011). Common and distinct networks underlying reward valence and processing stages: A meta-analysis. Neuroscience & Biobehavioral Reviews, 35(5), 1219-1236. https://doi.org/10.1016/j.neubiorev.2010.12.012.Common
Maris, E., & Oostenveld, R. (2007). Nonparametric statistical testing of EEG- and MEG-data. Journal of Neuroscience Methods, 164(1), 177-190. https://doi.org/10.1016/j.jneumeth.2007.03.024
Montague, P. R., Hyman, S. E., & Cohen, J. D. (2004). Computational roles for dopamine in behavioural control. Nature, 431(7010), 760-767. https://doi.org/10.1038/nature03015
Navarrete, G., Santamaría, C., & Froimovitch, D. (2015). Small samples and evolution: Did the law of small numbers arise as an adaptation to environmental challenges? Frontiers in Psychology, 6(Feb), 5-7. https://doi.org/10.3389/fpsyg.2015.00029
Parvaz, M. A., Konova, A. B., Proudfit, G. H., Dunning, J. P., Malaker, P., Moeller, S. J., Maloney, T., Alia-Klein, N., & Goldstein, R. Z. (2015). Impaired neural response to negative prediction errors in cocaine addiction. Journal of Neuroscience, 35(5), 1872-1879. https://doi.org/10.1523/JNEUROSCI.2777-14.2015
Peyk, P., De Cesarei, A., & Junghöfer, M. (2011). ElectroMagnetoEncephalography software: Overview and integration with other EEG/MEG toolboxes. Computational Intelligence and Neuroscience, 2011, 861705. https://doi.org/10.1155/2011/861705
Poreisz, C., Boros, K., Antal, A., & Paulus, W. (2007). Safety aspects of transcranial direct current stimulation concerning healthy subjects and patients. Brain Research Bulletin, 72(4-6), 208-214. https://doi.org/10.1016/j.brainresbull.2007.01.004
Proudfit, G. H. (2015). The reward positivity: From basic research on reward to a biomarker for depression. Psychophysiology, 52(4), 449-459. https://doi.org/10.1111/psyp.12370
Rehbein, M. A., Kroker, T., Winker, C., Ziehfreund, L., Reschke, A., Bölte, J., Wyczesany, M., Roesmann, K., Wessing, I., & Junghoefer, M. (2023). Noninvasive stimulation reveals ventromedial prefrontal cortex function in reward prediction and reward processing. Frontiers in Neuroscience, 17, 1219029.
Rescorla, R. A. (1972). A theory of Pavlovian conditioning: Variations in the effectiveness of reinforcement and non-reinforcement. Classical Conditioning, Current Research and Theory, 2, 64-69.
Roesmann, K., Kroker, T., Hein, S., Rehbein, M., Winker, C., Leehr, E. J., Klucken, T., & Junghöfer, M. (2021). Transcranial direct current stimulation of the ventromedial prefrontal cortex modulates perceptual and neural patterns of fear generalization. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 10, 210-220. https://doi.org/10.1016/j.bpsc.2021.08.001
Schupp, H. T., Flaisch, T., Stockburger, J., & Junghöfer, M. (2006). Emotion and attention: event-related brain potential studies. Progress in Brain Research, 156, 31-51.
Sharot, T. (2011). The optimism bias. Current Biology, 21(23), R941-R945. https://doi.org/10.1016/j.cub.2011.10.030
Sparing, R., & Mottaghy, F. M. (2008). Noninvasive brain stimulation with transcranial magnetic or direct current stimulation (TMS/tDCS)-From insights into human memory to therapy of its dysfunction. Methods, 44(4), 329-337. https://doi.org/10.1016/j.ymeth.2007.02.001
Telzer, E. H. (2016). Dopaminergic reward sensitivity can promote adolescent health: A new perspective on the mechanism of ventral striatum activation. Developmental Cognitive Neuroscience, 17, 57-67. https://doi.org/10.1016/j.dcn.2015.10.010
Van den Berg, I., Franken, I. H. A., & Muris, P. (2010). A new scale for measuring reward responsiveness. Frontiers in Psychology, 1(Dec), 1-7. https://doi.org/10.3389/fpsyg.2010.00239
Wagner, S., Rampersad, S. M., Aydin, Ü., Vorwerk, J., Oostendorp, T. F., Neuling, T., Herrmann, C. S., Stegeman, D. F., & Wolters, C. H. (2014). Investigation of tDCS volume conduction effects in a highly realistic head model. Journal of Neural Engineering, 11(1), 016002. https://doi.org/10.1088/1741-2560/11/1/016002
Watson, D., Clark, L. A., & Tellegen, A. (1988). Development and validation of brief measures of positive and negative affect: The PANAS scales. Journal of Personality and Social Psychology, 54(6), 1063-1070. https://doi.org/10.1037//0022-3514.54.6.1063
Wichary, S., Magnuski, M., Oleksy, T., & Brzezicka, A. (2017). Neural signatures of rational and heuristic choice strategies: A single trial ERP analysis. Frontiers in Human Neuroscience, 11(Aug), 1-14. https://doi.org/10.3389/fnhum.2017.00401
Winker, C., Rehbein, M. A., Sabatinelli, D., Dohn, M., Maitzen, J., Roesmann, K., Wolters, C. H., Arolt, V., & Junghoefer, M. (2019). Noninvasive stimulation of the ventromedial prefrontal cortex indicates valence ambiguity in sad compared to happy and fearful face processing. Frontiers in Behavioral Neuroscience, 13(May), 1-16. https://doi.org/10.3389/fnbeh.2019.00083
Winker, C., Rehbein, M. A., Sabatinelli, D., Dohn, M., Maitzen, J., Wolters, C. H., Arolt, V., Junghofer, M., & Junghöfer, M. (2018). Noninvasive stimulation of the ventromedial prefrontal cortex modulates emotional face processing. NeuroImage, 175, 388-401. https://doi.org/10.1016/j.neuroimage.2018.03.067
Winker, C., Rehbein, M. A., Sabatinelli, D., & Junghofer, M. (2020). Repeated noninvasive stimulation of the ventromedial prefrontal cortex reveals cumulative amplification of pleasant compared to unpleasant scene processing: A single subject pilot study. PLoS One, 15(1), e0222057. https://doi.org/10.1371/journal.pone.0222057
Xue, G., Lu, Z., Levin, I. P., Weller, J. A., Li, X., & Bechara, A. (2009). Functional dissociations of risk and reward processing in the medial prefrontal cortex. Cerebral Cortex, 19(5), 1019-1027. https://doi.org/10.1093/cercor/bhn147
Yang, J., Dedovic, K., Guan, L., Chen, Y., & Qi, M. (2014). Self-esteem modulates dorsal medial prefrontal cortical response to self-positivity bias in implicit self-relevant processing. Social Cognitive and Affective Neuroscience, 9(11), 1814-1818. https://doi.org/10.1093/scan/nst181
Yeung, N., Holroyd, C. B., & Cohen, J. D. (2005). ERP correlates of feedback and reward processing in the presence and absence of response choice. Cerebral Cortex (New York, N.Y.: 1991), 15(5), 535-544. https://doi.org/10.1093/cercor/bhh153

Auteurs

Thomas Kroker (T)

Institute for Biomagnetism and Biosignalanalysis, University of Muenster, Muenster, Germany.
Otto Creutzfeldt Center for Cognitive and Behavioral Neuroscience, University of Muenster, Muenster, Germany.

Maimu Alissa Rehbein (MA)

Institute for Biomagnetism and Biosignalanalysis, University of Muenster, Muenster, Germany.
Otto Creutzfeldt Center for Cognitive and Behavioral Neuroscience, University of Muenster, Muenster, Germany.

Miroslaw Wyczesany (M)

Faculty of Philosophy, Jagiellonian University, Krakow, Poland.

Jens Bölte (J)

Otto Creutzfeldt Center for Cognitive and Behavioral Neuroscience, University of Muenster, Muenster, Germany.
Institute of Psychology, University of Muenster, Muenster, Germany.

Kati Roesmann (K)

Otto Creutzfeldt Center for Cognitive and Behavioral Neuroscience, University of Muenster, Muenster, Germany.
Institute for Clinical Psychology and Psychotherapy, University of Siegen, Siegen, Germany.

Ida Wessing (I)

Otto Creutzfeldt Center for Cognitive and Behavioral Neuroscience, University of Muenster, Muenster, Germany.
Department of Child and Adolescent Psychiatry, University Hospital Muenster, Muenster, Germany.

Markus Junghöfer (M)

Institute for Biomagnetism and Biosignalanalysis, University of Muenster, Muenster, Germany.
Otto Creutzfeldt Center for Cognitive and Behavioral Neuroscience, University of Muenster, Muenster, Germany.

Classifications MeSH