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

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  • 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
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    1. 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.
    2. 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.
    3. 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.
    4. 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.
    5. 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.
    6. 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.
    7. 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.
    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.
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