A parietal-premotor network for movement intention and motor awareness.

Abstract

It is commonly assumed that we are conscious of our movements mainly because we can sense ourselves moving as ongoing peripheral information coming from our muscles and retina reaches the brain. Recent evidence, however, suggests that, contrary to common beliefs, conscious intention to move is independent of movement execution per se. We propose that during movement execution it is our initial intentions that we are mainly aware of. Furthermore, the experience of moving as a conscious act is associated with increased activity in a specific brain region: the posterior parietal cortex. We speculate that movement intention and awareness are generated and monitored in this region. We put forward a general framework of the cognitive and neural processes involved in movement intention and motor awareness.

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A parietal-premotor network for
movement intention and motor
awareness
Michel Desmurget1,2and Angela Sirigu1,2
1Centre de Neuroscience Cognitive, UMR 5229, CNRS, Bron, France
2Universite ´ Claude Bernard, Lyon 1, Lyon, France
It is commonly assumed that we are conscious of our
movements mainly because we can sense ourselves
moving as ongoing peripheral information coming from
our muscles and retina reaches the brain. Recent evi-
dence, however, suggests that, contrary to common
beliefs, conscious intention to move is independent of
movement execution per se. We propose that during
movement execution it is our initial intentions that we
are mainly aware of. Furthermore, the experience of
moving as a conscious act is associated with increased
activity in a specific brain region: the posterior parietal
cortex. We speculate that movement intention and
awareness are generated and monitored in this region.
We put forward a general framework of the cognitive
and neural processes involved in movement intention
and motor awareness.
Conscious intention and motor awareness in cognitive
neuroscience
In recent years, the neural bases of our conscious experi-
ences have been extensively investigated using psycho-
physics [1,2], neuroimaging [3,4], anatomo-functional
correlations[5,6],transcranial
[7,8], electrophysiological analyses [9] and direct electrical
stimulation of the brain [10,11]. All these approaches have
led to the identification of a complex interconnected net-
work underlying conscious experience. This network is
organized around three major regions: the posterior par-
ietal cortex (PPC), the supplementary motor area (SMA)
and the premotor cortex (PMC). However, a general model
articulating the functioning of these neural nodes is still
lacking. Taking advantage of the most recent theoretical
and experimental advances in the field, we propose here a
general framework of the main cognitive and neural pro-
cesses involved in generating the experience of conscious
motor intention and movement awareness. This frame-
work is based on our current understanding of the neural
bases of: (i) conscious motor intention (the conscious desire
to act), (ii) conscious motor awareness (the subjective feel-
ing that we are moving) and (iii) veridical motor awareness
(the objective knowledge that we are actually moving).
Although the emergence of movement intention into
awareness is preceded by early unconscious processes
taking place probably in prefrontal and parietal areas
magneticstimulation
[12,13] (Box 1), we focus here on the conscious component
of movement and show that the conscious intention to
move is independent of movement execution and that
parietal areas are key in the generation and monitoring
of movement intention and awareness.
Conscious motor intention
The establishment of conscious motor intention as a valid
object of scientific investigation can be traced back to the
pioneering work of Benjamin Libet and colleagues, 25
years ago. These authors asked human subjects to fixate
a single clock hand rotating on a screen (Figure 1, top
panel). The task was to press a button with the right index
finger whenever the subjects ‘felt the urge’ to do so. After
this movement, at a random time, the clock stopped and
the subjects were required to report the position of the
clock’s hand at the time they first became aware of their
will to move (W-Judgment). The readiness potential (RP,
an electrophysiological marker of early movement prep-
aration) was recorded. The W-Judgement was found to
precede movement onset by around 200 milliseconds. At
the same time, the RP was found to precede the W-Judge-
ment byabout 1 second (Figure 1, middle panel). The latter
latency strongly suggests that movement preparation
anticipatestheconsciousintentiontomove.Similarresults
were provided by Haggard and Eimer [14] in a subsequent
studywhichusedamodifiedversionofLibet’sparadigm.In
this study, the subjects could choose whether to respond
with the left or the right index finger. In addition to the
classical RP, Haggard and Eimer also recorded the Later-
alized RP (LRP), as a more specific marker of motor
preparation (the LRP is thought to reflect the point in
time at which response side – left vs. right – is determined)
[15]. On average, the LRP was found to occur approxi-
mately800 milliseconds
Additional analyses also showed that the LRP began sig-
nificantly earlier for early than for late W-Judgments,
which was not the case for the RP. The authors concluded
that conscious intention arises after the initial stage of
motor preparation (linked to RP), at the time when a
specific motor network is selected for action. This selection
does not mean, however, that the elaboration of the actual
motor command precedes conscious intention. Indeed,
there is a 200–300 milliseconds duration between the
W-Judgment and the actual motor command [2,14,16].
beforemovementonset.
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Corresponding author: Sirigu, A. (sirigu@isc.cnrs.fr).
1364-6613/$ – see front matter ? 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.tics.2009.08.001
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This delay is similar to the time required to initiate simple
reactive movements in response to visual or auditory
stimuli [17–20]. This suggests that the motor output cor-
responding to the desired movement is not processed
before, but after the time of conscious intention.
From an anatomical point of view, the supplementary
and pre-supplementary motor areas (designated SMA
hereafter) have been described as the most likely source
for LRPs [15,21]. From this one may speculate that the
medial motor regions play a critical role in the building of
conscious intention. There is indirect evidence supporting
this view. In particular, the SMA is activated when sub-
jects attend to the time of their conscious intention to
perform a movement [3]. Also, this structure is known to
beacommonlyinjuredregioninpatientssufferingfromthe
anarchic hand syndrome [22,23]: a pathological condition
in which the executive and intentional systems are dis-
connected from each other, thus leading to the occurrence
of arm movements without conscious intention [4].
However, the best evidence linking the SMA to con-
scious intention comes from anelectrical stimulation study
performed by Fried and colleagues [10]. Fried and col-
leagues stimulated the medial surface of the cerebral
hemispheres of epileptic patients with subdural electrode
grids [10]. The results indicated that stimulations deliv-
ered within the SMA region triggered a need or an urge to
move that resembles a compulsive desire to act. Indeed,
patients felt as if they were not the agents of their move-
ments. They reported that a movement ‘was about to occur’
or that the arm ‘was going to move’. Slightly increasing the
intensity of the stimulation above the urge threshold
caused the evoked movements to actually occur. The proxi-
mity between the two events suggests that the urge to act
experienced by these patients reflects the imminence of a
movement. In agreement with this idea, stimulations of
the SMA evoke very precise movement intentions such as
an ‘urge to move the right leg inward’, ‘to lift the right
elbow’ or to ‘pronate the right forearm’. It has been pro-
posed that the SMA triggers the movement by suppressing
the inhibitory signal exerted on the primary motor cortex
(M1)[24].Thissuppressionmightbetheneuralcorrelateof
the urge-to-move feeling experienced by epileptic patients
during electrical stimulation of the SMA.
In addition to the data above, solid evidence also links
the feeling of conscious intention to the activity of the PPC.
It has been shown that selective lesions of this region can
cause alien hand movements [4]. Also, it has been reported
that patients with parietal lesions can lose the early sub-
jective experience of wanting to move. To establish this
result, Sirigu and colleagues [2] used Libet’s paradigm in
three groups of individuals: control subjects, patients with
cerebellar lesions and patients with posterior parietal
lesions (Figure 1, bottom). In agreement with previous
results [3,14,16], the W-Judgement was found to precede
movement onset by more than 250 milliseconds in control
subjects and cerebellar patients. However, in parietal
patients, the lag was only around 55 milliseconds. This
short delay suggests that the patients did not know about
their intention to move until movement release became
imminent.Itistemptingtorelatethislateconsciousnessto
the claim that the urge tomove experienced when the SMA
is electrically stimulated reflects the imminence of a move-
ment. One may speculate that healthy subjects rely on
early activity within the PPC intentional system to be
aware of their intentions to move, whereas parietal
patients have to wait until the release of the motor com-
mand by the SMA to access this subjective experience.
Support for this view can be found in a recent study
where direct electrical stimulation was applied over the
parietal cortex in patients undergoing awake surgery for
tumor removal [11] (Box 2). If the PPC is truly involved in
the generation of conscious intentions, then electrical
stimulation of this region should be accompanied by the
subjective experience of ‘wanting to move’. In accordance
with this prediction, stimulation of the right inferior par-
ietal lobule (Brodmann Areas – BA 40 and 39) triggered a
strong desire to move the contralesional hand, arm or foot
(Figure2).Inthesamevein,stimulationsoftheleftinferior
parietal lobule (BA 39) provoked an intention to move the
lips. Patients reported, for instance, ‘a will to move the
chest’ or ‘a desire to move the hand’, which demonstrates
the voluntary and endogenous character of the feelings
they experienced. Interestingly, in most patients these
intentions were much less specific than the precise inten-
tions reported by the SMA patients (see above). Parietal
(stimulated) subjects were generally unable to precisely
describe the type of movements they intended to do, even
when invited to do so. For instance, a typical exchange was
Box 1. Prior intention
As shown by the seminal study of Libet and colleagues, preparatory
motor activity, known as the ‘readiness potential’ (RP), starts at least
1 second before the emergence of any conscious intention to act
[16]. Converging evidence suggests that this preparatory activity is
not germinal. It is shaped by unconscious computations carried out
in a wide network related to intentional actions [12,61]. To identify
the key nodes of this network, researchers have investigated the
neural bases of self-generated actions. They identified, as relevant,
activations in a wide range of areas including the posterior parietal
cortex (PPC), the anterior cingulate cortex, the supplementary motor
area (SMA) and the dorsolateral prefrontal cortex (DLPFC) [62].
Activation in this latter region was the most likely to survive when
self-generated actions were contrasted with externally-triggered
responses (instead of a rest condition) [20,62]. Interestingly, the
DLPFC receives important projections from the frontopolar cortex
[63], a structure that has been shown to encode motor intentions up
to 10 seconds before they become conscious [13]. In addition, the
DLPFC projects to the SMA and PPC [64], two regions that have been
shown to generate conscious intentions when electrically stimu-
lated (see main text). Therefore, the early computations carried out
by the prefrontal cortex seem to represent the first stage in the
causal chain that renders our motor intentions available to
consciousness.
In addition to the data above, it is widely admitted that the basal
ganglia (BG) are important for producing intentional (self-gener-
ated) actions. However, evidence supporting this claim is rather
weak. Neuroimaging studies have identified significant responses in
the BG when the neural activations triggered by self-generated
movements were compared to a rest state. However, no higher
activation in the BG network was observed when self-generated
movements were contrasted directly with externally triggered
movements [20,62]. An absence of systematic involvement of the
BG for self-generated movements was also reported in electro-
physiological and inactivation studies in monkeys [65]. Finally, the
idea that akinesia, in patients with Parkinson disease, concerns self-
generated but not externally triggered movements has recently
been rebutted [17].
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as follows [11]: Patient: ‘I wanted to move my foot’. Exper-
imenter: ‘Which foot’. Patient (showing his left leg): ‘This
one’. Experimenter: ‘How did you want to move it?’.
Patient: ‘I don’t know, I just wanted to move it’. To account
for these observations it was suggested that the PPC
contains stored movement representations [25,26] and
that electrical stimulations activate these representations,
thus provoking a desire to move [11]. Under ecological
circumstances, early unconscious computations carried
out in the prefrontal regions might lead to the activation
of these representations (Box 1). Note that increasing the
intensity of the stimulations was never found to produce
actual motor responses in parietal regions.
To summarize, parietal cortex stimulation generates
conscious intentions to move. By contrast, stimulation of
the SMA triggers feelings of an urge to move that reflect
the imminence of a motor response. This contrasting pat-
tern of response suggests that intentions in the PPC are
related to motor prediction and selection, whereas the
feeling of an urge to move in the SMA is related to move-
ment preparation [11,27].
Motor awareness
The issue of motor awareness amounts to a very simple
question: how do we know we are moving? During the last
decade, this question has received much less attention
from researchers than the issue of conscious intention.
Nonetheless, several important findings have emerged.
At a phenomenological level, it was found that most of
the basic functioning of the motor system occurs without
awareness (for a review [28]). This means that the signal
weareaware ofwhenmakingamovementdoesnotemerge
from the movement itself, but rather from the predictions
we make about the movement in advance of action. The
best evidence supporting this claim comes from behavioral
experiments in which a mismatch is introduced between
the actual and perceived motor responses. This mismatch
is typically within the margin of flexibility of the motor
system: it is big enough to impose profound kinematic
corrections to the ongoing movement but small enough
to allow target acquisition. Under this type of protocol,
despite large changes in hand path and joint trajectories,
the subjects believe that they are executing the movement
as originally planned and they do not take into account the
sensory signals to update their conscious motor percep-
tions [28–30]. A study by Fourneret and Jeannerod illus-
trates this point [31]. Fourneret and Jeannerod instructed
human subjects to trace sagittal lines on a graphic tablet.
Visual feedback of the movement was available through a
mirror positioned above the tablet. In some trials, this
feedback was altered so that the line traced by the subjects
deviated to the right or the left by a variable amount (from
2 to 10 deg). To perform a straight movement, the subjects
had thus to produce a diagonal response. They were able to
do so quite easily. However, they kept reporting that their
movement was straight in the sagittal direction. In other
words, they remained unaware of their large motor adjust-
ments and ‘knew’ only about their original intention.
These observations are consistent with clinical reports
in deafferented patients. As shown in recent studies, these
patients exhibit normal motor awareness, even though
they have no perceptual awareness [32–34]. They can
report when they are moving and along which trajectory,
but cannot detect, for instance, that their hand has been
blocked at movement onset. The same type of dissociation
is observed in hemiplegic patients with anosognosia. Typi-
cally, some of these patients fail to recognize or appreciate
the severity of their motor deficit. Others try to ‘explain it
away’ by arguing, for instance, that they are tired or not
willing to move. Others finally, claim stubbornly that they
are moving normally, despite their paralysis [35,36]. In a
recent study, patients of this latter group were given false
visual feedback of movement in their left paralyzed arm,
through a prosthetic rubber hand [37]. Three conditions
were tested: (i) the patients were instructed to raise
their paralyzed arm, (ii) the patients were told that the
Box 2. Probing brain functions with electrical stimulations
Electrical stimulation has a long history in medical and fundamental
sciences [66]. Today, this procedure remains strongly advocated for
tumoral resections carried out in eloquent regions [67]. In these
resections, the neurosurgeon stimulates the cortical surface while
the patient performs various motor and cognitive tasks (e.g.
opening-closing hand; naming objects) (Figure I). Any reproducible
functional disturbance induced by the stimulation provokes the
interruption of the resection at the tested location.
The use of electrical stimulation for probing brain functions is not
without controversy, however. A major issue concerns the tendency
of electrical currents to spread through white matter bundles. This
diffusion is inevitable, even for single pulse stimulations [68].
However, in contrast to a common view, it does not follow an
anarchic path; the current spreads along physiologically meaningful
pathways [69–72]. The resulting effect is assumed to mimic the
normal function of the stimulated tissue [73]. In agreement with this
hypothesis, it has been demonstrated, for instance, that the
premotor neurons that trigger limb movements when electrically
stimulated are the same as the neurons activated during goal-
directed reaches [74]. Based on these data one might suggest that
the spread of current along white matter tracts is not a difficulty that
needs to be overcome, but a process that is essential to the
expression of the investigated function.
Figure I. Peri-operative brain stimulation with a bipolar electrode during awake
surgery for tumor removal (Image by courtesy of Dr Carmine Mottolese).
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experimenter would move their arm and (iii) no instruc-
tion. In contrast to hemiplegic patients without anosogno-
sia, paralyzed patients with anosognosia disregarded
visual information of their motionless rubber hand when
they had the intention to move, compared with when they
expectedtheexperimentertomovetherubberhand,orhad
no movement expectation at all. These findings clearly
support the idea that motor awareness derives from the
processing of motor intentions. The reason why these
patients cannot access a veridical awareness will be dis-
cussed in the next section.
Additional support for the idea that motor intention
shapes movement awareness was recently provided by the
Desmurget and colleagues’ cortical stimulation study
introduced in the previous section [11]. Two complemen-
tary pieces of evidence were reported. Electrical stimu-
lations of the PMC (BA 6) evoked overt mouth and
contralateral limb movements (Figure 2). However, in
the absence of visual feedback, the patients firmly denied
that they had moved. This denial was not due to a low level
of vigilance because patients during functional evalu-
ations, when they were well awake, talked and moved in
response to verbal commands. They also reported feelings
of tingling or itching, indicating that their ability to intro-
specton stimulation-induced experiences was preserved. A
contrasting pattern was identified for PPC when the sites
initially identified as intentional (see above) were stimu-
lated at higher intensities. In this case the subjects
reported that they had actually performed the actions they
had previously intended to do. However, no overt move-
ments and electromyographic activity were present. To
account for these findings it was suggested that higher
intensities of stimulation did not just prime a motor
representation to consciousness (giving rise to a movement
conscious intention), but also recruited the executive net-
work responsible for movement monitoring. This network
is assumed to rely on forward modeling: a process that
simulates the effect of the efferent output to estimate, in
Figure 1. Top panel: Illustration of Libet’s paradigm. The task is to press a button with the right index finger. (a) Participants watch a clock-hand rotating on a screen. (b)
They have to identify the instant when they ‘feel the intention to move’. (c) They actually press the button. (d) After a random delay, the clock stops and the subjects report
the position of the clock-hand, identified in step (b). Middle panel: In healthy subjects, the Readiness Potential (an electrophysiological marker of early movement
preparation) begins around 1.5 seconds before the conscious experience of wanting to move, which occurs itself around 240 milliseconds before movement onset. Bottom
panel: In patients with posterior parietal damage, the Readiness Potential is absent and the conscious experience of wanting to move precedes movement onset by only a
few tens of milliseconds. Data from [2].
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real time, the state of the motor apparatus [38–40]. There
is converging evidence that forward models are generated
in the posterior parietal lobe [1,41–43]. It might be the case
then that this structure mediates motor awareness by
instructing motor regions that the movement has started,
has stopped or is unfolding (Box 3).
To summarize, motor awareness does not emerge from
the sensory signals generated by the movement, but from
the predictions we make about the movement before action
onset. These predictions are generated within the PPC, in
the same regions where feelings of conscious intentions are
evoked. Based on these observations, one may suggest that
intentions and the prediction of what will result from
carrying out these intentions create our conscious experi-
encethatwearemoving.Indeed,whatreallymatterswhen
we initiate an action is the specific goal we have in mind.
Whether this goal is reached through a straight or curved
path, with a bell-shaped or asymmetrical velocity profile,
on the basis of an open or closed loop response is of little
importance [44–46]. Obviously, the neural mechanisms
underlying consciousness have more important things to
do than controlling the low-level executive details of our
actions. It may even seem optimal, in terms of neural
economy, to assume that a movement unfolds as planned
when it reaches its goal.
Veridical motor awareness
In ecological conditions, our motor predictions are gener-
ally highly reliable. We rarely see our hand going right-
ward or downward whenwe move it leftward or upward. In
the same vein, we seldom, if ever, face the surprise of
seeing our arm not responding to a motor command.
However, these unusual situations can occur as a result
of experimental manipulations [47–49] or brain lesions
[35,36]. When this happens, the motor control system
can no longer force the congruence between the desired
and actual sensory reafferences, as it does continuously for
errors of limited magnitudes [38–40,18]. In the presence of
such large, unmanageable errors, the validity of our
original predictions is challenged and we become aware
of our movements as they actually unfold. For instance,
subjects immediately detect strong force fields and large
prismatic displacement applied to an ongoing point-to-
point response. This motor awareness does not occur when
the same level of perturbation is reached gradually [50,51].
Although the neural bases of veridical motor awareness
remain largely unknown, recent evidence has emphasized
the potential role of the PMC. In particular, Berti and
colleagues [5] used magnetic resonance imaging to inves-
tigate the anatomical distribution of brain lesions in right-
brain-damaged patients with anosognosia for hemiplegia
(see above). Analyses identified the premotor cortex (area
6) as the most frequently damaged area related to this
disturbance. To explain their result, the authors suggested
that the brain mechanisms that normally compare the
expected and actual peripheral reafferences are damaged
in patients with anosognosia for hemiplegia, which pre-
vents these patients from knowing that they are not mov-
ing [5,52]. Arguments favoring this hypothesis can be
found in the observation that the PMC is involved in the
computation of an expected sensory signal [53] and
receives abundant peripheral inputs about the ongoing
movement [54,55]. Additional evidence comes from a
recent study in phantom pain [56]. As shown in this study,
the PMC is the main area activated during the feeling
of phantom pain, in agreement with the idea that this
Figure 2. Premotor and parietal sites evoking conscious intentions, illusory movements and unconscious movements when stimulated with a bipolar electrode during
awake brain surgery for tumor removal. Modified from [11].
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