IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-51822-8.html
   My bibliography  Save this article

Direct stimulation of anterior insula and ventromedial prefrontal cortex disrupts economic choices

Author

Listed:
  • Romane Cecchi

    (Grenoble Institut Neurosciences
    Institut National de la Santé et de la Recherche Médicale
    Université Paris Sciences et Lettres)

  • Antoine Collomb-Clerc

    (Grenoble Institut Neurosciences
    Swiss Federal Institute of Technology (EPFL))

  • Inès Rachidi

    (Grenoble Institut Neurosciences
    University Hospital of Grenoble)

  • Lorella Minotti

    (Grenoble Institut Neurosciences
    University Hospital of Grenoble)

  • Philippe Kahane

    (Grenoble Institut Neurosciences
    University Hospital of Grenoble)

  • Mathias Pessiglione

    (Pitié-Salpêtrière Hospital
    Université de Paris)

  • Julien Bastin

    (Grenoble Institut Neurosciences)

Abstract

Neural activity within the ventromedial prefrontal cortex (vmPFC) and anterior insula (aIns) is often associated with economic choices and confidence. However, it remains unclear whether these brain regions are causally related to these processes. To address this issue, we leveraged intracranial electrical stimulation (iES) data obtained from patients with epilepsy performing an economic choice task. Our results reveal opposite effects of stimulation on decision-making depending on its location along a dorso-ventral axis within each region. Specifically, stimulation of the ventral subregion within aIns reduces risk-taking by increasing participants’ sensitivity to potential losses, whereas stimulation of the dorsal subregion of aIns and the ventral portion of the vmPFC increases risk-taking by reducing participants’ sensitivity to losses. Moreover, stimulation of the aIns consistently decreases participants’ confidence, regardless of its location within the aIns. These findings suggest the existence of functionally dissociated neural subregions and circuits causally involved in accepting or avoiding challenges.

Suggested Citation

  • Romane Cecchi & Antoine Collomb-Clerc & Inès Rachidi & Lorella Minotti & Philippe Kahane & Mathias Pessiglione & Julien Bastin, 2024. "Direct stimulation of anterior insula and ventromedial prefrontal cortex disrupts economic choices," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51822-8
    DOI: 10.1038/s41467-024-51822-8
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-51822-8
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-51822-8?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. You-Ping Yang & Xinjian Li & Veit Stuphorn, 2022. "Primate anterior insular cortex represents economic decision variables proposed by prospect theory," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    2. Yueqing Peng & Sarah Gillis-Smith & Hao Jin & Dimitri Tränkner & Nicholas J. P. Ryba & Charles S. Zuker, 2015. "Sweet and bitter taste in the brain of awake behaving animals," Nature, Nature, vol. 527(7579), pages 512-515, November.
    3. Li Wang & Sarah Gillis-Smith & Yueqing Peng & Juen Zhang & Xiaoke Chen & C. Daniel Salzman & Nicholas J. P. Ryba & Charles S. Zuker, 2018. "The coding of valence and identity in the mammalian taste system," Nature, Nature, vol. 558(7708), pages 127-131, June.
    4. Sébastien Ballesta & Weikang Shi & Katherine E. Conen & Camillo Padoa-Schioppa, 2020. "Values encoded in orbitofrontal cortex are causally related to economic choices," Nature, Nature, vol. 588(7838), pages 450-453, December.
    5. Mathias Pessiglione & Ben Seymour & Guillaume Flandin & Raymond J. Dolan & Chris D. Frith, 2006. "Dopamine-dependent prediction errors underpin reward-seeking behaviour in humans," Nature, Nature, vol. 442(7106), pages 1042-1045, August.
    6. Sébastien Ballesta & Weikang Shi & Camillo Padoa-Schioppa, 2022. "Orbitofrontal cortex contributes to the comparison of values underlying economic choices," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    7. Leland, Jonathan W. & Grafman, Jordan, 2005. "Experimental tests of the Somatic Marker hypothesis," Games and Economic Behavior, Elsevier, vol. 52(2), pages 386-409, August.
    8. Jean Daunizeau & Vincent Adam & Lionel Rigoux, 2014. "VBA: A Probabilistic Treatment of Nonlinear Models for Neurobiological and Behavioural Data," PLOS Computational Biology, Public Library of Science, vol. 10(1), pages 1-16, January.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Antoine Collomb-Clerc & Maëlle C. M. Gueguen & Lorella Minotti & Philippe Kahane & Vincent Navarro & Fabrice Bartolomei & Romain Carron & Jean Regis & Stephan Chabardès & Stefano Palminteri & Julien B, 2023. "Human thalamic low-frequency oscillations correlate with expected value and outcomes during reinforcement learning," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    2. He A Xu & Alireza Modirshanechi & Marco P Lehmann & Wulfram Gerstner & Michael H Herzog, 2021. "Novelty is not surprise: Human exploratory and adaptive behavior in sequential decision-making," PLOS Computational Biology, Public Library of Science, vol. 17(6), pages 1-32, June.
    3. Qi Wang & Jia-Jie Zhu & Lizhao Wang & Yan-Peng Kan & Yan-Mei Liu & Yan-Jiao Wu & Xue Gu & Xin Yi & Ze-Jie Lin & Qin Wang & Jian-Fei Lu & Qin Jiang & Ying Li & Ming-Gang Liu & Nan-Jie Xu & Michael X. Z, 2022. "Insular cortical circuits as an executive gateway to decipher threat or extinction memory via distinct subcortical pathways," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    4. Maël Lebreton & Karin Bacily & Stefano Palminteri & Jan B Engelmann, 2019. "Contextual influence on confidence judgments in human reinforcement learning," PLOS Computational Biology, Public Library of Science, vol. 15(4), pages 1-27, April.
    5. C. Nicolas & A. Ju & Y. Wu & H. Eldirdiri & S. Delcasso & Y. Couderc & C. Fornari & A. Mitra & L. Supiot & A. Vérité & M. Masson & S. Rodriguez-Rozada & D. Jacky & J. S. Wiegert & A. Beyeler, 2023. "Linking emotional valence and anxiety in a mouse insula-amygdala circuit," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    6. Sasa Teng & Fenghua Zhen & Li Wang & Jose Canovas Schalchli & Jane Simko & Xinyue Chen & Hao Jin & Christopher D. Makinson & Yueqing Peng, 2022. "Control of non-REM sleep by ventrolateral medulla glutamatergic neurons projecting to the preoptic area," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    7. Demetrio Ferro & Tyler Cash-Padgett & Maya Zhe Wang & Benjamin Y. Hayden & Rubén Moreno-Bote, 2024. "Gaze-centered gating, reactivation, and reevaluation of economic value in orbitofrontal cortex," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    8. Yihan Wang & Qian-Quan Sun, 2024. "A prefrontal motor circuit initiates persistent movement," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    9. Li Shen & Guang-Wei Zhang & Can Tao & Michelle B. Seo & Nicole K. Zhang & Junxiang J. Huang & Li I. Zhang & Huizhong W. Tao, 2022. "A bottom-up reward pathway mediated by somatostatin neurons in the medial septum complex underlying appetitive learning," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    10. Leo Chi U Seak & Simone Ferrari-Toniolo & Ritesh Jain & Kirby Nielsen & Wolfram Schultz, 2023. "Systematic comparison of risky choices in humans and monkeys," Working Papers 202316, University of Liverpool, Department of Economics.
    11. Stefano Palminteri & Emma J Kilford & Giorgio Coricelli & Sarah-Jayne Blakemore, 2016. "The Computational Development of Reinforcement Learning during Adolescence," PLOS Computational Biology, Public Library of Science, vol. 12(6), pages 1-25, June.
    12. Lun Wang & Min Gao & Qinglong Wang & Liyuan Sun & Muhammad Younus & Sixing Ma & Can Liu & Li Shi & Yang Lu & Bo Zhou & Suhua Sun & Guoqing Chen & Jie Li & Quanfeng Zhang & Feipeng Zhu & Changhe Wang &, 2023. "Cocaine induces locomotor sensitization through a dopamine-dependent VTA-mPFC-FrA cortico-cortical pathway in male mice," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    13. Chih-Chung Ting & Nahuel Salem-Garcia & Stefano Palminteri & Jan B. Engelmann & Maël Lebreton, 2023. "Neural and computational underpinnings of biased confidence in human reinforcement learning," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    14. Manuel Glauco Carbone & Icro Maremmani, 2024. "Chronic Cocaine Use and Parkinson’s Disease: An Interpretative Model," IJERPH, MDPI, vol. 21(8), pages 1-23, August.
    15. David Vaquero-Puyuelo & Concepción De-la-Cámara & Beatriz Olaya & Patricia Gracia-García & Antonio Lobo & Raúl López-Antón & Javier Santabárbara, 2021. "Anhedonia as a Potential Risk Factor of Alzheimer’s Disease in a Community-Dwelling Elderly Sample: Results from the ZARADEMP Project," IJERPH, MDPI, vol. 18(4), pages 1-12, February.
    16. Patricia L. Lockwood & Jo Cutler & Daniel Drew & Ayat Abdurahman & Deva Sanjeeva Jeyaretna & Matthew A. J. Apps & Masud Husain & Sanjay G. Manohar, 2024. "Human ventromedial prefrontal cortex is necessary for prosocial motivation," Nature Human Behaviour, Nature, vol. 8(7), pages 1403-1416, July.
    17. Lin Zhang & Beibei Sun & Fei Shu & Ying Huang, 2022. "Comparing paper level classifications across different methods and systems: an investigation of Nature publications," Scientometrics, Springer;Akadémiai Kiadó, vol. 127(12), pages 7633-7651, December.
    18. Chi Chen & Dilja Krueger-Burg & Livia de Hoz, 2019. "Wide sensory filters underlie performance in memory-based discrimination and generalization," PLOS ONE, Public Library of Science, vol. 14(4), pages 1-29, April.
    19. Zixuan Tang & Chen Qu & Yang Hu & Julien Benistant & Frederic Moisan & Edmund Derrington & Jean-Claude Dreher, 2023. "Strengths of social ties modulate brain computations for third-party punishment," Post-Print hal-04325737, HAL.
    20. Hanan Shteingart & Tal Neiman & Yonatan Loewenstein, 2012. "The Role of First Impression in Operant Learning," Discussion Paper Series dp626, The Federmann Center for the Study of Rationality, the Hebrew University, Jerusalem.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51822-8. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.