Dissecting the neurofunctional bases of intentional action

Abstract

Here we challenge and present evidence that expands the ,, and 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 component or subcortical gray structures for the 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.

Decoding Changes of Mind in Voluntary Action—Dynamics of Intentional Choice Representations

“…Nevertheless, in line with the idea that a medial frontal pathway is of particular importance for endogenous action selection (Passingham 1987;Brass and Haggard 2008;Soon et al 2008;Fried et al 2017;Zapparoli et al 2018), we found that MFC was the only area that represented endogenous components of both initial decisions and later decision reversals. More specifically, MFC encoded CoM in participants who more strongly considered endogenous information, but not in those who exclusively relied on external cues, i.e., target distance.…”

“…First, participants were required to generate an arbitrary endogenous decision for a visually presented face or house stimulus without any choice outcome being associated with rewards at this stage. We derived ROIs from previous studies and confirmed that initial voluntary decisions were encoded in MFC, precuneus, dlPFC and AG (Brass and Haggard 2008;Soon et al 2008;Bode et al 2011;Krieghoff et al 2011;Bode et al 2013;Soon et al 2013;Zapparoli et al 2018). Additionally, decisions could be decoded from visual cortex, presumably due to visual fixation of the chosen image, and attention to visual features of the chosen image (Krajbich et al 2010;Rens et al 2018;Voigt et al 2019).…”

Voluntary tic suppression and the normalization of motor cortical beta power in Gilles de la Tourette syndrome: an EEG study

“…There is a rich body of fMRI literature showing how internally and externally triggered actions are sub-served by partially different neural patterns. Studies comparing conditions in which subjects have to press a button at a moment of their own choice (internally triggered actions) to conditions in which subjects are prompted to press the button by a visual or acoustic cue (externally triggered actions) report greater activation of the SMA/preSMA associated with internally triggered actions (see Zapparoli et al, 2017Zapparoli et al, , 2018. On the contrary, externally triggered actions seem to be more associated with the activity of visual or auditory cortices, depending on the type of external trigger signal (Cunnington et al, 2002;Jenkins et al, 2000).…”

The context-dependent nature of the neural implementation of intentions

“…The notion of a context-invariant encoding of task information in a single brain region has long been challenged: It is known that different variables of tasks might be encoded in different regions across the cortex, supporting a distributed model of task encoding (Jahanshahi, 1998), which is in line with the Multiple Demand Network framework (Fedorenko, Duncan, & Kanwisher, 2013). Furthermore, when preparing actions the information about ‘what’ will be performed and ‘when’ it will be performed is encoded in dissociable brain regions (Soon, Brass, Heinze, & Haynes, 2008; Zapparoli et al, 2018), in line with Brass and Haggard’s (2008) distinction of the ‘what’, ‘when’ and ‘whether’ subprocesses of intentions (see also Krieghoff, Brass, Prinz, & Waszak, 2009; Momennejad & Haynes, 2012). Our results can be interpreted as an extension of this deviation from a singular process, or locus, by showing that the ‘what’ is not a discrete process either, but a process that depends on the context in which the action decision is made.…”