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Optimal level of human intracranial theta activity for behavioral switching in the subthalamo-medio-prefrontal circuit

Author

Listed:
  • Maëva Laquitaine

    (GIN)

  • Mircea Polosan

    (Grenoble Institut Neurosciences)

  • Philippe Kahane

    (Grenoble Institut Neurosciences)

  • Stephan Chabardes

    (Grenoble Institut Neurosciences)

  • Jérôme Yelnik

    (NeuroSpin center)

  • Sara Fernandez-Vidal

    (NeuroSpin center)

  • Philippe Domenech

    (NeuroSpin center
    Université Paris Cité)

  • Julien Bastin

    (GIN)

Abstract

The ability to switch between rules associating stimuli and responses depend on a circuit including the dorsomedial prefrontal cortex (dmPFC) and the subthalamic nucleus (STN). However, the precise neural implementations of switching remain unclear. To address this issue, we recorded local field potentials from the STN and from the dmPFC of neuropsychiatric patients during behavioral switching. Drift-diffusion modeling revealed that switching is associated with a shift in the starting point of evidence accumulation. Theta activity increases in dmPFC and STN during successful switch trials, while temporally delayed and excessive levels of theta lead to premature switch errors. This seemingly opposing impact of increased theta in successful and unsuccessful switching is explained by a negative correlation between theta activity and the starting point. Together, these results shed a new light on the neural mechanisms underlying the rapid reconfiguration of stimulus-response associations, revealing a Goldilocks’ effect of theta activity on switching behavior.

Suggested Citation

  • Maëva Laquitaine & Mircea Polosan & Philippe Kahane & Stephan Chabardes & Jérôme Yelnik & Sara Fernandez-Vidal & Philippe Domenech & Julien Bastin, 2024. "Optimal level of human intracranial theta activity for behavioral switching in the subthalamo-medio-prefrontal circuit," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-52290-w
    DOI: 10.1038/s41467-024-52290-w
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    References listed on IDEAS

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    1. Marije ter Wal & Artem Platonov & Pasquale Cardellicchio & Veronica Pelliccia & Giorgio LoRusso & Ivana Sartori & Pietro Avanzini & Guy A. Orban & Paul H. E. Tiesinga, 2020. "Human stereoEEG recordings reveal network dynamics of decision-making in a rule-switching task," Nature Communications, Nature, vol. 11(1), pages 1-12, December.
    2. 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.
    3. Sameer A. Sheth & Matthew K. Mian & Shaun R. Patel & Wael F. Asaad & Ziv M. Williams & Darin D. Dougherty & George Bush & Emad N. Eskandar, 2012. "Human dorsal anterior cingulate cortex neurons mediate ongoing behavioural adaptation," Nature, Nature, vol. 488(7410), pages 218-221, August.
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