Intracerebral gamma modulations reveal interaction between emotional processing and action outcome evaluation in the human orbitofrontal cortex

Abstract

The orbitofrontal cortex (OFC) plays a key role not only in processing emotions but also in monitoring performance outcome. Although the neuroanatomical substrates underlying each of the two processes have been extensively investigated, they have predominantly been probed separately and therefore a precise knowledge of the functional overlap within the multiple OFC sub-portions involved is still lacking. Here, we explore the neural dynamics mediating performance monitoring and emotional processing using direct intracranial EEG (iEEG) recordings from multiple OFC sites of an epileptic patient. Neural activity was recorded during two experiments. The first task required processing of emotional faces and the second investigated action outcome evaluation based on a visual feedback on the subject's performance. Task-related neural dynamics were assessed using modulations of high frequency responses in the gamma-band (50–150 Hz). Our results reveal that processing negative facial emotions as well as receiving negative feedback both elicited gamma-band responses in the lateral OFC. By contrast, the mid-OFC was selectively activated for positive feedback. Furthermore, we also found significant gamma-band deactivation in the gyrus rectus during processing of negative feedback. Our findings provide novel evidence for an intricate valence-selective interaction between the networks mediating emotion processing and performance monitoring in human OFC and support the hypothesis of a tight relationship between gamma-band activity and behavior.