Abstract
Stimulus-driven actions are preceded by preparatory brain activity that
can be expressed by event-related potentials (ERP). Literature on this
topic has mainly focused on simple actions, such as the finger keypress,
finding activity in frontal, parietal, and occipital areas detectable up
to two seconds before the stimulus
onset. However, little is known
about the preparatory brain activity when the action complexity
increases, and specific brain areas designated to achieve movement
integration intervene. The main aim of this paper is to identify the
time course of preparatory brain activity associated with actions of
increasing complexity using ERP analysis and a visuomotor discrimination
task. Motor complexity was manipulated by asking nineteen volunteers to
provide their response by simply pressing a key or by adding to the
keypress arm extensions (reaching) alone, or in combination with a
standing step (involving the whole body).
Results showed that these actions
of increasing levels of complexity appear to be associated with
different patterns of preparatory brain activity. Specifically, the
simple keypress was characterized
by the largest motor excitatory preparation in premotor areas paralleled
by the largest prefrontal inhibitory/attentional control.
Reaching
presented a dominant parietal
preparation confirming the role of these integration areas in reaching
actions toward a goal. Stepping
was characterized by localized activity in the bilateral dorsomedial
parieto-occipital areas attributable to sensory readiness, for the
approaching stimulus. In conclusion, the brain is able to optimally
anticipate any stimulus-driven action modulating the activity in the
brain areas specialized in the preparation of that action type.
Keywords : action preparation, action complexity, brain
activity, pre-stimulus ERP
Introduction
Voluntary actions can be defined
as the materialization of thought through movement and massively involve
the brain from sensory to cognitive and motor areas (e.g., Flanders
2009). Most of these cortical involvements happen well before the
movement onset during the anticipatory/preparatory stages of action
processing. Understanding the neural activity that supports this
action-planning process is a long-standing challenge in neuroscience
(e.g., Nguyen, Breakspear & Cunnington, 2014). To study the brain
dynamics preceding voluntary actions, the event-related potential (ERP)
methods greatly contributed thanks to their high temporal resolution and
to the possibility of extracting the specific brain activity related to
a movement onset or stimuli requiring motor responses (e.g., Kornhuber
& Deecke, 1964; Shibasaki & Hallett, 2006).
Voluntary actions can be executed in response to either external stimuli
(here called externally-triggered or stimulus-driven actions) or
internal decisions (here called internally-triggered or self-paced
actions). While preparatory ERP associated with self-paced actions has
been widely studied for many types of movements, from simple finger
flexion to complex praxic movements, (e.g., Shibasaki & Hallett, 2006;
Wheaton et al., 2005), ERP preceding stimulus-driven actions has been
less investigated and, if any, only for tasks requiring just a finger
flexion (a keypress) as responses (for a review, Di Russo et al. 2017).
The time course of brain activity preceding any voluntary movement is a
slow-rise negative ramp that culminates at movement onset for self-paced
action or at stimulus onset for stimulus-driven actions. In both cases,
the main ERP component, named Bereitschaftspotential (BP) or Readiness
Potential (RP), has been localized in premotor brain areas reflecting
the necessary motor preparation (Shibasaki & Hallett, 2006) for any
movement, including jumping into an abyss (Nan et al., 2019). The timing
of the BP component has been described as having a bi-phasic trend, an
early “unconscious” phase, and a later “conscious” phase (e.g.,
Shibasaki & Hallett, 2006). While the early phase has been described as
an unspecific preparation associated with the intention to move (e.g.,
Lau et al., 2004), consciousness is deployed in the later phase to allow
last-minute changes and enable learning, in order to improve performance
(e.g., Deecke 2012; Dennet 2005; Mele 2007). For externally triggered
actions, larger late BP amplitude has been associated with faster
response time in speeded tasks (e.g., Di Russo et al., 2019).
For more complex movements such as reaching, grasping, or pantomimes,
additional activity in the posterior parietal cortex (PPC) has been
found in few studies (Wheaton et al., 2005a, b; Inouchi et al., 2013;
Bozzacchi et al., 2012) and named posterior BP (pBP). The pBP has been
described for self-paced, but not for externally-triggered movements.
In addition to the BP and the pBP, there are other two ERP components
preceding externally-triggered simple movements that were found in
visuomotor tasks. The prefrontal negativity (pN) and the visual
negativity (vN). The pN has been localized in the inferior prefrontal
gyrus and has been associated with cognitive preparation intended as
top-down cognitive control (mainly attentional and inhibitory) for the
upcoming actions (e.g., Berchicci et al., 2020). The BP and the pN have
been described as a form of accelerator/braking system based on
predictive internal models able to modulate the response accuracy/speed
trade-off in performance (e.g., Di Russo et al., 2017) and to regulate
the behavior proactively before the event (e.g., Aron, 2011).
The vN has been localized in the extrastriate visual areas and has been
associated with the sensory readiness reflecting top-down signals for
the allocation of preparatory sensory resources for upcoming events
(e.g., Bianco et al., 2020). The pN and the vN were just described in
tasks requiring simple movements (finger flexion) and have not yet been
studied for more complex movements performed by upper or lower limbs,
such as reaching or walking/stepping, respectively. For normative data
on these components see Di Russo et al. (2019).
Overall, all this evidence suggests that the brain activity preceding
any voluntary movement involves a cortical network focused not only on
anterior premotor and prefrontal areas but spanning also on more
posterior parietal and occipital
regions. The contribution of the
PPC preparatory activity for
stimulus-driven actions has been widely investigated in both human and
animal models (Teixeira et al.,
2014; Pilacinsky et al., 2018; Sulpizio et al., 2023). In macaque,
several studies (Fattori et al., 2001; Galletti et al., 1997, 1999) have
shown that neurons in the PPC become active well before the appearance
of any electromyographic movement-related activity, thus confirming the
role played by these areas in the planning of reaching (Batista &
Andersen, 2001; Battaglia-Mayer et al., 2000; Andersen & Buneo, 2002;
Connolly et al., 2003; Cui & Andersen, 2007; Fattori et al., 2005;
Snyder et al., 1998, 2000). More recent evidence showed that the macaque
medial parietal reaching-related V6A area (located on the
parieto-occipital sulcus, POc; Fattori et al., 2005, 2009) decodes the
position of the object towards which the arm movement is directed even
before the movement begins (Filippini et al., 2018). It follows that the
early representation of the action that takes place in the macaque PRR
(Parietal Reach region, which includes the V6A; Andersen & Buneo, 2002)
is not based exclusively on the position of the target or on action
patterns present in memory but contains proprioceptive and kinematic
information regarding the body movement that has yet to occur (Kuang et
al., 2016).
As repeatedly demonstrated, in humans the PPC plays a crucial role in
forming movement intentions (Desmurget et al., 2009) and visual
motor-imagery (Crammond, 1997; Sirigu et al., 1996; Sulpizio et al.,
2020). Importantly, the medial portion of human PPC has been considered
a main substrate for reach planning (e.g., Lindner et al., 2010;
Pitzalis et al., 2013; Tosoni et al., 2015), while the more anterior and
dorsal portion of human PPC is instead considered a main substrate for
reach and walk planning, that is whole body actions performed using both
upper and lower limbs (Heed et al., 2011, 2016; Leonè et al., 2014;
Pitzalis et al., 2019).
Overall, combining animal and human data, the general idea is that the
PPC integrates the contribution from both the visual areas and the motor
areas and uses both the visual information on the surrounding
environment and the context-independent motor programs to create action
plans useful for reaching the target using different effectors (eye,
arm, leg). This implies anticipating the consequences of the movement
and therefore choosing the most suitable action sequence (e.g., Teixeira
et al., 2014).
Based
on this background, the present study was aimed at verifying which
pattern of brain activity is associated with the prediction and
preparation of stimulus-driven actions requiring increasing levels of
motor complexity. The motor complexity was manipulated by asking
subjects to provide their response by a simple keypress (finger flexion)
or by adding additional movements such as long-range reaching movement
alone or in combination with a standing stepping movement. Thus, we
designed three task conditions (Keypress , Reaching ,Reaching-stepping ) with identical visual and cognitive complexity
(50/50 Go/No-go task) but with a different motor engagement. The
experiment is based on the general hypothesis that the greater the
movement complexity, the greater the need to integrate information of
different nature to perform it, so the greater the activation in a
specific functional circuit, mainly located in the parietal region,
delegated to joint inputs coming both from the occipital visual areas
and the frontal/prefrontal motor control areas. Using this experimental
design and specific comparison across conditions, it is possible to
identify the cortical activity mainly involved in motor control and the
ones combining somatosensory and visual information useful for complex
movement, involving larger body districts, and implying the correct
management of the surrounding space (Piserchia et al., 2017; Whitlock et
al., 2014).
The expectation is to identify modulation in amplitude and timing of the
BP, pBP, pN, and vN components as a function of the required involvement
of premotor, parietal, prefrontal, and visual areas preparatory activity
required by the three conditions, respectively.
We specifically expect that at
the least the early BP should be similar for all movements since the
intention to move should be common (e.g., Lau et al., 2004), The late BP
should be larger in the simplest task likely requiring less time to be
accomplished. For this reason, the pN should be also larger in the
simplest task (just requiring a keypress) because the mentioned
accelerator/braking system that modulates the response accuracy/speed
trade-off (e.g., Di Russo et al., 2017). In this vein, finer movements,
requiring inhibition of the rest of the body, should be more controlled
by the pN. The reaching preparation should be characterized by the pBP
specifically involved in the kind of actions (e.g., Teixeira et al.,
2014). Lower limb movements should be dominated by medial PPC activity
and visual-related readiness (the vN) for the management of the front
space (Berchicci et al., 2020; Piserchia et al., 2017; Whitlock et al.,
2014).
Methods