4.1 Keypress condition
The preparation of a simple finger keypress strongly involved prefrontal and premotor areas and less parietal and occipital areas. This result confirms literature that widely used this simple motor response in cognitive tasks, especially indicating that in speeded discriminatory response tasks (response time <500 ms), prefrontal and premotor areas interact with each other to proactively optimize the speed/accuracy trade-off (e.g., Perri et al 2014) using a proactive accelerator/brake (excitation/inhibition) system where the premotor area is the accelerator and the prefrontal area is the brake which is released (such as in a muscle car burnout) when the target trial (the green light in the muscle car example) is detected (Di Russo et al., 2017). Even though it requires more excitatory and inhibitory activity during the preparation phase, the Keypress condition requires less parietal and occipital preparatory activity likely because arm/body movements were substantially absent, so no analysis of the visual space aimed to coordinate the movement parameters with needs imposed by the surrounding visual environment is necessary.
4.2 Reaching condition
The Reaching condition tested here required strong involvement of parietal and premotor areas, a small contribution from the occipital areas, and no contribution from the prefrontal areas. The dominance of parietal areas in these movements confirms the previous literature indicating that brain activity related to arm-stretching, reaching anticipation, and direction planning based on a coordinate transformation (also when the behavior is not effectively carried out) are produced in parietal areas (Vandenberghe et al. 2001; Molenberghs et al. 2007; Inouchi et al., 2013; Caspari et al., 2018). The parietal cortex would integrate visual and proprioceptive elements to establish the trajectory of the arm toward the target (Vesia et al., 2008) and the object‘s distance from the body (Pitzalis et al., 2015). The parietal activity observed here for visually guided reaching actions was prevalently localized in the left hemisphere, contralateral to the arm used to perform the task. The localization of this activity confirms the previous literature (e,g., Culham et al., 2003; Johnson-Frey et al., 2005), showing that contralateral parietal areas are responsible for hand/arm control during reaching movement. The source analysis showed that this parietal activity is mainly situated dorsally in the anterior precuneus, where the human homologue of macaque area PEc was found (Pitzalis et al., 2019). Although only a few studies have been conducted to specifically investigate the functional role of this region in humans, there is strong evidence in literature for an important role of this region, and more specifically of the region likely hosting human area PEc, in a set of sensorimotor transformations needed to make a visual pointing toward a visual target on the screen (Pitzalis et al., 2019), or actually grasp a visually presented object (Sulpizio et al. 2020).
Some of the medial parietal areas traditionally attributed to reaching movements appeared to be silent, such as, for example, the V6A (Breveglieri et al., 2014; Hadjidimitrakis et al, 2017; Filippini et al., 2018). The reason for this lack of activity could be because the analysis concerned the pre-stimulus phase, i.e., the preparation of the response before stimulus onset. It is therefore possible to hypothesize that these areas are activated after stimulus onsets as previously shown (Pitzalis et al., 2015). Moreover, it has been shown that area V6A is modulated by the orientation of the hand aimed at grasping the object (Fattori et al., 2009; Galletti et al., 2022). In the present study, this parameter does not need to be controlled in a task where the goal of reaching is not grasping, and the location of the target is always the same.
Reaching-related activity was found also in the lateral portion of the occipital lobe, suggesting that the visual brain also plays a role in the cortical network underlying preparatory activity. The role of the occipital areas during movement preparation and execution confirms the action-specific perception theory postulating that perception essentially needed to link the environmental information with our ability to act within it (Witt, 2011; Kline et al., 2020). This lateral occipital cortex has been traditionally associated with the visual analysis involved in the representation and perception of objects (Malach et al., 1995). Note that this activity is present in both reaching and stepping (although in this latter less consistently) and its involvement could be related to the highly demanding task in terms of visual perception and recognition of the four stimuli configurations.
4.3 Reaching-Stepping condition
The Reaching -Stepping condition required strong involvement of occipital preparatory activity and contributions from the premotor, and the parietal areas. Although this ERP activity preceding externally-triggered stepping has never been reported before, our results are in line with the previous literature on the same topic. Indeed, several studies have described brain activity associated with stepping planning in the PPC and occipital areas (Evans et al., 2013; Kline et al., 2020), especially when the walk takes place in an enclosed space (Dalla Volta et al., 2015). A piece of evidence particularly relevant here is the ERP study from Berchicci and coworkers (2020) where subjects were asked step on a platform to investigate motor planning for forward and backward self-paced stepping. Results revealed premotor (during both forward and backward stepping), parietal (mainly during forward stepping) and prefrontal (during backward stepping) contributions. These different activation patterns can be explained by taking into consideration that the backward step is a more complex movement requiring major cognitive control and it can also be considered as an avoiding behavior, demanding inhibition, while the forward step is like an oriented-to-action behavior, a familiar and simple movement towards something, so it mainly requires the analysis of the surrounding space which strongly involves the parietal cortex. Moreover, the occipital activity was not dominant probably because interaction with objects was not required. The present source analysis showed that this parietal activity is bilateral and mainly situated dorso-medially in correspondence of cortical regions like the parieto-occipital sulcus (where area V6A is located) and the anterior precuneus (where the human homologue of macaque PEc is located). There is strong evidence in macaque and human literature for the important role of both these regions in a set of sensorimotor transformations needed to make stimulus-driven actions toward a visual target. In particular, the anterior precuneus plays a central role in visually guided locomotion, being implicated in controlling leg-related movements as well as the four limbs interaction with the environment. Human area PEc (hPEc; Pitzalis et al. 2019) responds to both arm and leg movements (although leg movements elicit stronger activations), is involved in implementing the sensorimotor transformations needed to grasp a visually presented object (Sulpizio et al. 2020) and is connected with somatosensory regions hosting a leg representation (area PE and primary somatosensory cortex). In addition, hPEc shows a sensitivity to self-motion compatible visual stimulation responding to the optic flow; a stimulus that gives the brain the illusion of self-movement when the body is actually stationary (Pitzalis et al. 2019, 2020). Human PEc shared similar properties with macaque PEc, an area specifically dedicated to visual-motor integration which makes possible the dynamic interaction with the surrounding environment (Breveglieri et al., 2008; Bakola et al., 2010; Hadjidimitrakis et al., 2015; Gamberini et al., 2018; Impieri et al., 2018), especially during ego-motion towards a goal involving legs. Macaque PEc responds to arm and, even more, to leg joint stimulation (Breveglieri et al. 2006, 2008), controls limb actions giving the necessary somatosensory information to accomplish the action and contains neurons with specific sensitivity to stimuli changing size and speed (Gamberini et al. 2018), similarly to what happens while walking. Collectively, these findings support the hypothesis that hPEc drives locomotion (Pitzalis et al., 2019; Maltempo et al., 2021) through its ability to combine and interact with somatosensory signals from the lower and upper parts of the body and visual signals from outside. Interestingly, evidence from a single case study showed that lesions affecting the medial portion of the left PPC and causing optic ataxia (i.e., a spatial impairment of visually guided reaching) similarly affects upper (arm) and lower (leg) effectors when visually guided actions are directed towards the same contralesional hemispace (Evans et al., 2013). Similarly to reaching condition, stepping-related activity was found also in the lateral portion of the occipital lobe, mainly on the right hemisphere. Interestingly, evidence from fMRI studies showed that the middle occipital gyrus and the intraparietal-transverse occipital gyrus may both be recruited, along with parietal and frontal areas, during a locomotion-related activity (Dalla Volta et al., 2015) as well as during hand and foot pointing movements (Pitzalis et al., 2019).
The found medial parietal activity can be explained by the need for visuomotor integration (Grill-Spector et al., 2001) before stepping toward a target. In fact, in the human dorsomedial parietal cortex it is possible to identify an area (PEc) specifically dedicated to visual-motor integration which makes possible the dynamic interaction with the surrounding environment (Breveglieri et al., 2008; Bakola et al., 2010; Hadjidimitrakis et al., 2015; Gamberini et al., 2018; Impieri et al., 2018), especially during ego-motion towards a goal involving legs. The PEc not only is connected with somatosensory regions hosting a leg representation (area PE and primary somatosensory cortex) and is active in pointing movements of both hands and feet, but also responds to visual stimulation through the optical flow (Pitzalis et al., 2019; 2020): a stimulus that gives the brain the illusion of self-movement when, in reality, the body is stationary. This area can, therefore, be considered on par with the PEc area that has previously been found in the macaque, in which it responds to arm and, even more, to leg joint stimulation (Breveglieri et al. 2006, 2008), controls limb actions giving the necessary somatosensory information and contains neurons with specific sensitivity to stimuli changing size and speed (Gamberini et al. 2018), similarly to what happens while walking. Collectively, these findings support the hypothesis that PEc drives locomotion preparation (Pitzalis et al., 2019; Maltempo et al., 2021) by its ability to combine and interact with somatosensory signals from the body and visual signals from outside.