The Brain in (Willed) Action: A Meta-Analytical Comparison of Imaging Studies on Motor Intentionality and Sense of Agency

Abstract

Voluntary actions can be fractionated in different phenomena: from the emergence of intentions and the ensuing motor plans and actions, to the anticipation and monitoring of their outcomes, to the appreciation of their congruency with intentions and to the eventual emergence of a sense of agency. It follows that motor intention and the sense of agency should occur at different stages in the normal generation of willed actions. Both these processes have been associated with a fronto-parietal motor network, but no study has investigated to what extent the two experiences can be dissociated for the brain regions involved. To this end, we assessed the PET/fMRI literature on agency and intentionality using a meta-analytic technique based on a hierarchical clustering algorithm. Beside a shared brain network involving the meso-frontal and prefrontal regions, the middle insula and subcortical structures, we found that motor intention and the sense of agency are functionally underpinned by separable sets of brain regions: an “intentionality network,” involving the rostral area of the mesial frontal cortex (middle cingulum and pre-supplementary motor area), the anterior insula and the parietal lobules, and a “self-agency network,” which involves the posterior areas of the mesial frontal cortex (the SMA proper), the posterior insula, the occipital lobe and the cerebellum. We were then able to confirm this functional organization by a subsequent seed-based fMRI resting-state functional connectivity analysis, with seeds derived from the intentionality/sense of agency specific clusters of the medial wall of the frontal lobe. Our results suggest the existence of a rostro-caudal gradient within the mesial frontal cortex, with the more anterior regions linked to the concept of motor intentionality and the brain areas located more posteriorly associated with the direct monitoring between the action and its outcome. This suggestion is reinforced by the association between the sense of agency and the activation of the occipital lobes, to suggest a direct comparison between the movement and its external (e.g., visual) consequences. The shared network may be important for the integration of intentionality and agency in a coherent appreciation of self-generated actions.

Anterior insula activity and the effect of agency on the Stimulus‐Preceding Negativity

“…Our prediction that greater activation of the anterior insulae would be observed on choice than no‐choice trials was a safe one given that many previous fMRI studies have obtained similar results (reviewed in Seghezzi et al, ; Sperduti et al, ). However, the finding of statistical equivalence in the effect for reward and punishment contexts differs from that of the most relevant previous study.…”

“…Of greatest immediate relevance was Segghezi and colleagues' () finding of a pair of cortical regions that displayed functional gradients for the activation foci reported in the 31 reviewed papers. In dorsomedial motor cortex (pre‐supplementary motor area and SMA proper) as well as in insular cortex (anterior and middle), activation foci associated with agency for motor intention and for sensory consequences were mapped progressively along an antero‐posterior dimension.…”

“…The meta‐analytic review of Seghezzi and colleagues () categorized relevant fMRI studies according to whether they focused on ownership of the action or of its consequences. The former category (“motor intention”) included experiments such as ours, in which the participant either chose which response to make or deferred to the computer's decision.…”

“…It has been suggested that one such function might be evaluating the consequences of voluntary actions in order to predictively guide future actions (Brass & Haggard, 2010). Extensive neuropsychological (Klein, Ullsperger, & Danielmeier, 2013) and neuroimaging research (Seghezzi et al, 2019;Sperduti et al, 2011) indicates that the insula plays a vital role in determining whether one is the agent of any such action.…”

“…Second, topographical analyses specifically indicate a maximum for the SPN choice effect at sites near the right anterior insula (Chen et al, ; Masaki et al, ; Mühlberger, Angus, Jonas, Harmon‐Jones, & Harmon‐Jones, ; Walentowska et al, ). Third, extensive prior fMRI research has linked insular cortex to the sense of agency (reviewed in Seghezzi, Zirone, Paulesu, & Zapparoli, ; Sperduti, Delaveau, Fossati, & Nadel, ). Among previous studies, two were particularly relevant to the fMRI experiment reported here in that they assessed valence (monetary gain vs. loss) in addition to agency (choice vs. no‐choice).…”