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.
Highlights
Volitional or voluntary actions are crucial components of our daily life and they could be defined as “self-initiated” or “selfgenerated” actions (Passingham et al, 2010)
We first performed an explorative meta-analysis of the existing neuroimaging literature on action awareness by means of a hierarchical clustering (HC) algorithm, in order to provide a quantitative review of the neuroimaging studies on motor intention and sense of self-agency
The portion of supplementary motor area (SMA) significantly associated with the sense of agency (SMA proper) was connected with the paracentral and postcentral gyrus bilaterally, the left middle cingulum, the right precentral gyrus and the right superior parietal lobule
Summary
Volitional or voluntary actions are crucial components of our daily life and they could be defined as “self-initiated” or “selfgenerated” actions (Passingham et al, 2010). Much of the functioning of the voluntary motor systems occurs without the need of any conscious thought, humans are aware that they intend to move and are responsible for the consequences of their own acts. Our intentions to produce a movement (the so-called “motor intention” or volition) and the feeling of controlling our own motor acts and, through them, the events in the external world (the so-called “sense of agency”), represent two crucial components of the action awareness for voluntary acts. We address two cognitive models that contextualized motor intention and sense of agency into different conceptual frameworks, from which distinct predictions about their neurofunctional underpinnings could be drawn. We introduce a formal meta-analysis of neuroimaging studies, that tested these neurofunctional predictions and the validity of functional anatomical assignations in terms of their replicability across studies and dissociability along the intentionality/agency axes
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