A Crucial Role of the Frontal Operculum in Task-Set Dependent Visuomotor Performance Monitoring.

Felix Quirmbach,Jakub Limanowski

doi:10.1523/eneuro.0524-21.2021

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 analyzed human behavioral, functional magnetic resonance imaging (fMRI), and magnetoencephalography (MEG) data from two virtual reality-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 source-localized gamma power. Furthermore, functional connectivity of the bilateral FO to the right posterior parietal cortex (PPC) increased under a visual versus 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.

Highlights

To effectively perform goal-directed action in the environment, the brain needs to monitor motor 3 performance and detect errors, so that it can enable adaptive changes in behaviour (Diedrichsen, 4 2005; Klein et al, 2007; Suminski et al, 2007; Ullsperger et al, 2014)
In the MEG study, root mean square error 114 (RMSE) was significantly higher for incongruent than congruent trials in both data sets (ANOVA, F(1,17) = 30.026, p < 0.001); in the functional magnetic resonance imaging (fMRI) data, RMSE was higher for congruent than incongruent trials (F(1,15) = 6.820, p < 0.05)
The behavioural results and self-reports 293 showed that participants could follow the task instructions; that this induced the desired cognitive294 attentional task set; and that behaviour in the virtual hand (VH) vs RH tasks was comparable across fMRI and MEG 295 studies

Summary

Introduction

To effectively perform goal-directed action in the environment, the brain needs to monitor motor 3 performance and detect errors, so that it can enable adaptive changes in behaviour (Diedrichsen, 4 2005; Klein et al, 2007; Suminski et al, 2007; Ullsperger et al, 2014). Thereby regions like e.g. the frontal operculum (FO, anterior insular cortex, IC (Sridharan et al, 2008; Higo et al, 2011; Klein et al, 2013; Cieslik et al, 2015; Billeke et al, 2020)) may signal a need for increased cognitive control to the executive control network, consisting (among other regions) of the lateral prefrontal cortices, the PPC, supplementary motor area (SMA), and the inferior parietal lobule (Ullsperger et al, 2010; Uddin, 2021) This network, in turn, may direct attentional resources to the relevant stimuli, driving behavioural adaptions (Sridharan et al, 2008; Menon and Uddin, 2010)

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