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

Maëva Laquitaine, Mircea Polosan, Philippe Kahane, Stephan Chabardes, Jérôme Yelnik, Sara Fernandez-Vidal, Philippe Domenech () and Julien Bastin ()
Additional contact information
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
Julien Bastin: GIN

Nature Communications, 2024, vol. 15, issue 1, 1-12

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41467-024-52290-w

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