Dissecting the neurofunctional bases of intentional action.

Abstract

Here we challenge and present evidence that expands the <i>what</i>, <i>when</i>, and <i>whether</i> anatomical model of intentional action, which states that internally driven decisions about the content and timing of our actions and about whether to act at all depend on separable neural systems, anatomically segregated along the medial wall of the frontal lobe. In our fMRI event-related paradigm, subjects acted following conditional cues or following their intentions. The content of the actions, their timing, or their very occurrence were the variables investigated, together with the modulating factor of intentionality. Besides a shared activation of the pre-supplementary motor area (pre-SMA) and anterior cingulate cortex (ACC) for all components and the SMA proper for the when component, we found specific activations beyond the mesial prefrontal wall involving the parietal cortex for the <i>what</i> component or subcortical gray structures for the <i>when</i> component. Moreover, we found behavioral, functional, anatomical, and brain connectivity evidence that the self-driven decisions on whether to act require a higher interhemispheric cooperation: This was indexed by a specific activation of the corpus callosum whereby the less the callosal activation, the greater was the decision cost at the time of the action in the whether trials. Furthermore, tractography confirmed that the fibers passing through the callosal focus of activation connect the two sides of the frontal lobes involved in intentional trials. This is evidence of non-unitary neural foundations for the processes involved in intentional actions with the pre-SMA/ACC operating as an intentional hub. These findings may guide the exploration of specific instances of disturbed intentionality.