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.