A crucial role of the frontal operculum in task-set dependent visuomotor performance monitoring

Abstract

For adaptive goal-directed action, the brain needs to monitor action performance and detect errors. The corresponding information may be conveyed via different sensory modalities; for instance, visual and proprioceptive body position cues may inform about current manual action performance. Thereby, contextual factors such as the current task set may also determine the relative importance of each sensory modality for action guidance. Here, we analysed human behavioural, functional magnetic resonance imaging (fMRI), and magnetoencephalography (MEG) data from two virtual reality (VR)-based hand-target phase matching studies to identify the neuronal correlates of performance monitoring and error processing under instructed visual or proprioceptive task sets. Our main result was a general, modality-independent response of the bilateral frontal operculum (FO) to poor phase matching accuracy, as evident from increased BOLD signal and increased gamma power. Furthermore, functional connectivity of the bilateral FO to the right posterior parietal cortex (PPC) increased under a visual vs proprioceptive task set. These findings suggest that the bilateral FO generally monitors manual action performance; and, moreover, that when visual action feedback is used to guide action, the FO may signal an increased need for control to visuomotor regions in the right PPC following errors.

Significance statement

The brain uses feedback from the senses to guide behaviour and correct errors. During hand movements, this feedback can come from seen and felt hand positions. Here, we used brain scanning to show that brain regions in the frontal operculum responded to action errors in a hand-target matching task, when either seen or felt hand positions are task relevant. Furthermore, when the seen hand position had to be prioritized for the task, these regions increased their communication with the right posterior parietal cortex, which is known to guide hand movements based on visual cues. These results suggest a crucial role for the frontal operculum in monitoring hand actions; in particular, when vision is task relevant.