Abnormalities in the Awareness and Control of Action

Author(s): Christopher D. Frith, Sarah-Jayne Blakemore and Daniel M. Wolpert

Source: Philosophical Transactions: Biological Sciences, Vol. 355, No. 1404 (Dec. 29, 2000), pp.
1771-1788
Published by: Royal Society
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 E THE ROYAL do 10.1098/rstb.2000.0734
SOCIETY

Abnormalities in the awareness and control

of action

Christopher D. Frithl*, Sarah-Jayne Blakemorel and Daniel M. Wolpert2

JWellcome Department of Cognitive Jeurology, and 2Sobell Department of .Aeurophysiology, Institute of JNeurology,
University College London, Queen Square, London WCJ/ 3BG, UK

Much of the functioning of the motor system occurs without awareness. Nevertheless, we are aware of some
aspects of the current state of the system and we can prepare and make movements in the imagination.
These mental representations of the actual and possible states of the system are based on two sources:
sensory signals from skin and muscles, and the stream of motor commands that have been issued to the
system. Damage to the neural substrates of the motor system can lead to abnormalities in the awareness of
action as well as defects in the control of action. We provide a framework for understanding how these
various abnormalities of awareness can arise. Patients with phantom limbs or with anosognosia experience
the illusion that they can move their limbs. We suggest that these representations of movement are based on
streams of motor commands rather than sensory signals. Patients with utilization behaviour or with
delusions of control can no longer properly link their intentions to their actions. In these cases the impair-
ment lies in the representation of intended movements. The location of the neural damage associated with
these disorders suggests that representations of the current and predicted state of the motor system are in
parietal cortex, while representations of intended actions are found in prefrontal and premotor cortex.

Keywords: motor control; awareness; prediction; abnormalities

kinds of sensory feedback that result from the movements

1. INTRODUCTION
generated by the motor commands. The basic task of the
In this review we will present a framework designed to motor control system is to manage the relationships
provide a coherent account of a number of disparate between motor commands and sensory feedback. This
observations concerning abnormalities in the awareness management is necessary for two reasons. First, it ensures
and control of action. Our framework is based on estab- that our movements achieve their goals. Second, it
lished models of normal motor learning and control (for a enables us to learn by experience to make more accurate
review, see Wolpert 1997). However, we are particularly and effective movements. Motor commands are trans-
concerned to explain abnormal experiences of motor formed into sensory feedback every time our musculo-
control such as phantom limbs and the passivity skeletal system interacts with the environment, since
phenomena associated with schizophrenia. In ? 2 we will every movement we make has immediate sensory
summarize the components of our model of motor control consequences. Activity in the musculoskeletal system
and learning. In ? 3 we will outline the application of this transforms efferent motor actions into reafferent sensory
model to a number of specific signs and symptoms of feedback. Once a sequence of motor commands has been
motor disorders. issued it is possible to predict the subsequent behaviour of
the motor system and the sensory consequences of that
behaviour. However, these predictions cannot be made
2. AN OUTLINE OF THE MOTOR CONTROL SYSTEM
solely from knowledge of the sequence of motor
A well-functioning motor system is an essential require- commands. An additional set of variables, called state
ment if we are to move through our environment safely, variables, also needs to be known. These are the config-
reach and grasp objects and learn new skills. Making urations of parts of the body, such as joint angles and
movements involves the production of an appropriate angular velocities and include the state of the system
sequence of muscle contractions. At the same time prior to the implementation of the motor commands.
sensory information is critical for deciding what move- These state variables provide the basis for internal models
ments to make and for observing the consequences of of the motor system. On the basis of the motor commands
those movements. Motor control and motor learning can and these state variables it is possible to determine the
best be understood in terms of an engineering system future behaviour of the system.
(Craik 1948). In this system the motor commands
emanate from controllers within the central nervous (a) Internal models of the motor system
system (CNS). The brain also has access to the various There is evidence that the CNS contains transforma-
tions, or internal models, which mimic aspects of one's
*Author for correspondence ([email protected]). own body and the external world (Wolpert et al. 1995;

Phil. Trans. R. Soc. Lond. B (2000) 355, 1771-1788 1771 C) 2000 The Royal Society
Received 13 March 2000 Accepted 13 April 2000

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 1772 C. D. Frith and others Abnormalities in awareness and control of action

Wolpert 1997). Here we shall be concerned with two actual sensory feedback. In contrast, externally
varieties of internal model, predictors and controllers generated sensations are not associated with any
(also known as forward and inverse models, respectively). efference copy and therefore cannot be predicted and
Whenever a movement is made, a motor command is will produce a higher level of sensory discrepancy.
generated by the CNS and a predictor estimates the As the discrepancy between predicted and actual
sensory consequences of that motor command. A sensation increases, so does the likelihood that the
controller, on the other hand, captures the relationship sensation is externally produced. By using such a
between the desired state and the motor command system it is possible to cancel out or attenuate sensa-
required to achieve that state. An important issue to stress tions induced by self-generated movement and
in our discussion of such representations is that they do thereby distinguish sensory events due to self-
not need to be detailed or accurate models of the external produced motion from sensory feedback caused by
world. Often an internal model need only provide a the environment, such as contact with objects. Such
rough approximation of some external transformation in a mechanism underlies the finding that the same
order to play a useful role. The function of predictors and tactile stimulus is perceived as much less intense
controllers requires that at least three states of the motor when it is self-applied in comparison with when it is
system are represented: the current state of the system, applied by another person (Weiskrantz et al. 1971).
the desired state of the system and the predicted state of The perceived intensity of a self-applied tactile
the system. stimulus increases with the degree of discrepancy
introduced between the predicted and actual sensory
(i) Predictors (forward models) feedback (Blakemore et al. 1999).
Predictors model aspects of the external world and of the (iii) Prediction can also be used to maintain accurate
motor system in order to capture the forward or causal rela- performance in the presence of feedback delays. In
tionship between actions and their outcomes (Ito 1970; most sensorimotor loops the feedback delays between
Jordan 1996; Wolpert et al. 1995). Every time a motor the issuing of a motor command and the perception
command is issued to make a movement, an efference copy of its sensory consequences are large. This is due to
of the motor command is produced in parallel. Based on the both neural transduction and processing delays,
efference copy, the predictor estimates the sensory which can be as long as 250 ms. These delays can
consequences of the ensuing movement. This prediction can result in inaccuracy if the motor system compares
be used in several ways (Miall & Wolpert 1996; Wolpert the desired outcome with the perceived outcome to
1997) and there is a substantial body of evidence that the determine the performance error. As the perceived
CNS makes use of such prediction. outcome is delayed relative to the actual outcome the
motor system will respond to a perceived error which
(i) Prediction is needed to anticipate and compensate may no longer exist, thereby generating a potentially
for the sensory effects of movement. For example, inappropriate response. A predictor can be used to
during eye movements an efference copy of the estimate the actual outcome of the motor command
motor command is used to predict the effects of the without delay and compare this with the desired
movement (Von Helmholtz 1886; Sperry 1950; Von outcome. Such internal feedback of the estimated
Holst & Mittelstaedt 1950). In order to determine outcome of an action is available before the true
the location of an object relative to the head, its sensory feedback (Miall et al. 1993).
retinal location and the gaze direction must be (iv) Prediction also plays a critical role in a process that
known. As the eye muscles are thought to contain no integrates sensory and motor information in order to
sensory receptors used to determine the gaze estimate the current state of the system. The state of
direction, Von Helmholtz (1886) proposed that the the motor system is not directly observable by the
gaze direction is determined by predicting the eye CNS, which has access only to the outgoing motor
location based on the efference copy of the motor commands and the subsequent sensory feedback.
command going to the eye muscles. Using this Instead, the state has to be estimated by observing
estimate of eye position together with the object's these signals. To produce optimal estimates, two
retinal location, its true position in space can be deter- processes can be used. The first uses a predictor to
mined. When the eye is moved without using the eye estimate the next state of the system. The second
muscles (for example, by gently pressing on the eyelid process uses sensory feedback to modify this estimate
with the finger), the retinal location of objects (Wolpert et al. 1995; Wolpert 1997). By using both
changes, but the predicted eye position is not updated, sources of information the uncertainty of the state
leading to the perception that the world is moving. estimate can be reduced. The recognition that the
(ii) Prediction can also be used to filter sensory informa- representation of a limb position depends not only on
tion, attenuating the component that is due to self- current sensation but also on predictions based on
movement (reafference) from that due to changes in motor commands can explain a number of the
the outside world. The sensory consequences of self- bizarre experiences associated with abnormalities of
generated movements are predicted from the effer- the motor system (see ? 3 (b) ).
ence copy produced in parallel with the motor
command. Self-produced sensations can be correctly (ii) Controllers (inverse models)
predicted from motor commands. As a result there Controllers provide the motor commands necessary to
will be little or no sensory discrepancy resulting achieve some desired outcome. For a simple reaching and
from the comparison between the predicted and grasping movement, the first step would be to plan the

Phil. Trans. R. Soc. Lond. B (2000)

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 Abnormalities in awareness and control of action C. D. Frith and others 1773

trajectory to be followed by the hand in order to reach goal

the desired final position. The trajectory represents the
desired configuration of the body at each point in time.
The muscle activations necessary to achieve this trajec- desired
tory depend on the dynamic parameters of the body such state

as the inertia and link lengths of the body segments. The affordances
controllers must learn to generate the appropriate motor
commands such that the muscle activations achieve the ntrollers
(perception to
desired trajectory. The controllers, therefore, receive a
movement)
desired configuration of the body and produce motor
commands which should achieve this configuration
Recently it has been proposed that our ability to interact
predict icted
(movement to prdce

with many different objects in a variety of different envir- perception) state

mtor
onments relies on a 'divide-and-conquer' strategy.
commands
Complex tasks are decomposed into simpler subtasks, each
learned by a separate controller (Ghahramani & Wolpert
movement
1997; Wolpert & Kawato 1998; Blakemore et al. 1998a).
Therefore, rather than having a single controller, multiple actual state

controllers develop, each tuned to a particular sensori- sensory

motor context. At any given time, one or a subset of these
controllers contributes to the final motor command. The
contribution each controller makes to the final motor estimated
actual
command is determined by two distinct processes. The state
first uses sensory contextual information (affordances),
such as the visual appearance of an object, to select Figure 1. The basic components of a motor control system
controllers prior to movement initiation. For example, the based upon engineering principles.

apparent size and weight of an object would determine

whether we try to pick it up with a precision grip or a
(iii) Predicted next state of the system. This representa-
power grip. The second process uses the errors in the
tion provides an estimate of the future state of the
predictions made by a set of predictors each tuned to a
system derived from the predictors.
different context. As these predictors capture distinct
(iv) Motor commands. These are derived from the
dynamic behaviours of the motor system, their prediction
controllers and are fine-tuned by sensory informa-
errors can be used during movement to determine in
tion (affordances) about the current state of the
which context the motor system is acting and thereby
world (e.g. visual information about the position and
switch between controllers during a movement. For
shape of the object that is to be grasped).
example, when we pick up a milk bottle which appears
(v) Sensory feedback. This is the consequence of the
full, but is in fact empty, we select the inappropriate
action performed, plus any environmental events.
controller based on the visual information, but are able to
switch controllers when the predicted outcome of our Comparisons of these representations provides error
action does not match the actual outcome. This modular signals that can be used to improve the functioning of the
learning system, known as the multiple paired predictor- predictors and the controllers.
controller model (Wolpert & Kawato 1998), is capable of
(i) Errors derived from differences between the desired
learning to produce appropriate motor commands under
and the actual state of the system can be used to
a variety of contexts and can switch rapidly between
improve the functioning of the controllers.
controllers as the context changes. These features are
(ii) Errors derived from differences between the
important for a full model of motor control and motor
predicted and the actual state of the system can be
learning, as the human motor system is capable of very
used to improve the functioning of the predictors.
flexible, modular adaptation.
(iii) Errors derived from differences between the desired
and the predicted state of the system can be used to
(b) Motor representations
improve the functioning of the controllers during
Our outline of the motor control system postulates
mental practice.
several kinds of motor representation. These are listed
below and shown graphically in figure 1. In terms of this model the performance of a simple
action involves the following stages. Current wishes and
(i) Actual state of the system. The actual state of the plans are used to formulate the desired state (instanta-
system is not directly available to the CNS. Instead an neous goal) of the system. The controllers generate appro-
estimated actual state of the system is inferred on the priate motor commands on the basis of the difference
basis of the stream of motor commands and sensory between the actual state and the desired state. Computa-
feedback. For simplicity we will refer to the estimated tion by the controllers is 'fine-tuned' by the context in
state as the actual state as it represents the best esti- which the action is occurring. For example, if the action
mate of the actual state available to the CNS. requires the grasping of an object, knowledge of the shape
(ii) Desired state of the system. This representation holds and position of the object provides 'affordances' which
the instantaneous goal of the system. allow a more accurate computation of the appropriate

Phil. Trans. R. Soc. Lond. B (2000)

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1774 C. D. Frith and others Abnormalities in awareness and control ofaction

motor commands (Greeno 1994). Once the motor (e.g. Rizzolatti et al. 1987; Corbetta 1998). During the
commands have been computed the predictors calculate performance of covert attention tasks activity is observed
the expected state of the system. Subsequently, or in in areas which overlap with those seen during motor
parallel with this process the action is performed. Once imagery tasks: ACC, SMA, lateral premotor cortex
the movement has been made the new state of the system (frontal eye fields) and intraparietal sulcus (IPS)
can be estimated on the basis of sensory feedback and (Corbetta et al. 1993; Nobre et al. 1997).
knowledge of the motor commands that have been
executed. If there are discrepancies between the new state (ii) Limited awareness of affordances and motor commands
and the desired and predicted states then modifications These observations confirm that we can be aware of
can be made to the predictors and controllers and further intended movements and can perform movement
actions can be performed to correct the situation. sequences in imagination. Furthermore, this motor
imagery has specific neural correlates. There are a
(c) Awareness of motor representations number of other observations, however, which demon-
One major concern in this paper is to consider the strate that the motor control system can also function in
extent to which we are aware of the functioning of some the absence of awareness. Goodale et al. (1986) (see also
aspects of our motor control system (see also Jeannerod Bridgeman et al. 1981) report a pointing experiment in
1994). Here we shall review evidence indicating which which the target occasionally jumped several degrees,
components of the motor control system outlined in ? 2(b) unnoticed by the subjects. Nevertheless the subjects were
are available to consciousness and which are not. able to adjust the trajectory of their moving hand to the
target position. In this case the subjects were aware
(i) Motor imagery and motor preparation neither of the sensory information that elicited the move-
The awareness of selecting and controlling our actions ment correction nor of the change in the motor
is a major component of consciousness. We can also programme that was elicited. In another experiment
readily imagine making movements in the absence of any involving reaching and grasping, Castiello et al. (1991)
overt behaviour. Furthermore this mental activity can found that awareness of an unexpected target jump
have detectable consequences. First, mental practice of occurred more that 200ms after the motor system had
various tasks can lead to a significant improvement in initiated an appropriate movement correction. Further-
subsequent performance (for a review, see Feltz & more, appropriate grasping movements can be made even
Landers 1983). Mental training affects several outcomes when conscious perception of the object to be grasped is
of motor performance such as muscular strength (Yue & incorrect. In the Ebbinghaus (Tichener) Circles Illusion
Cole 1992), movement speed (Pascual-Leone et al. 1995) two identical circles appear to be of different sizes
and temporal consistency (Vogt 1995). Second, prolonged because of the context in which they occur. The strength
performance of tasks in the imagination can lead to of this illusion can be measured by asking subjects to
marked physiological changes. Subjects who performed or adjust the size of the circles until they appear to be iden-
mentally simulated leg exercise increased heart rate and tical. However, the size of this illusion is greatly reduced
respiration rate in both conditions (Decety et al. 1991). if it is measured in terms of the distance between the
Third, changes in brain activity associated with move- finger and thumb when grasping the central circles
ments made in the imagination can readily be detected (Aglioti et al. 1995). The result from studies of this illusion
using brain imaging techniques such as positron emission and others (e.g. Gentilucci et al. 1996) suggests that there
tomography. Decety et al. (1994) asked subjects to imagine can be a dissociation between our perception of objects
grasping three-dimensional objects presented to them. and the information which the sight of objects (their
Stephan et al. (1995) compared execution of a sequence of affordances) provides to fine-tune our reaching and
joystick movements with imagining making such a grasping movements. An extreme example of this lack of
sequence. These studies showed that the brain regions awareness is provided by the case of D.F. described by
activated during motor imagery are a subset of those Milner & Goodale (1995). D.F. was unaware of the
activated during motor execution. Jeannerod (1994) shapes of objects and was unable to describe them or to
argued that motor imagery is closely related to motor discriminate between them, but she could nevertheless
preparation. Preparing a movement in advance and produce appropriate grasping actions based on the shapes
holding it in readiness while waiting for a signal to of which she was unaware. A similar pattern of behaviour
release the movement engages the same processes as those has been observed in another patient by Perenin &
involved in imagining making that movement. Brain Rossetti (1996).
imaging studies of motor preparation and motor imagery In terms of the model for motor control presented in
highlight activity in the anterior cingulate cortex (ACC), ?2(b) these results suggest that we are not aware of the
the anterior supplementary motor cortex (SMA), inferior precise details of the motor commands that generate our
lateral premotor cortex and inferior parietal lobe (Decety actions, nor of the way in which immediate sensory infor-
et al. 1994; Stephan et al. 1995; Krams et al. 1998). Since mation (affordances) is used to fine-tune these
these areas are engaged by motor preparation and motor commands. Thus, it would appear that our awareness of
imagery they are presumably involved with representa- our actions and of the sensory information on which these
tions of intended and predicted movements. It has been actions are based is derived from other sources. There are
argued that covert attention, that is attending to a likely to be good reasons for this separation. For example,
particular object without actually moving the eyes or the we have suggested (Frith 1995) that representations used
hand towards it, is equivalent to mentally reaching for for reaching an object need to be coded in egocentric
that object with the eyes (foveation) or the hand coordinates, while representations for reporting the

Phil. Trans. R. Soc. Lond. B (2000)

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 Abnormalities in awareness and control of action C. D. Frith and others 1775

position of an object need to be in coordinates that are An extreme example of a lack of awareness of action
independent of a personal view. To reach for an object it is resulting from predictability comes from overlearned
necessary to know where that object is in relation to our tasks. With sufficient practice many tasks can become
hand, not in relation to other objects in the environment. 'automatic' and can performed without any need to think
There are many different frames of reference that could about the actions required to perform the task. This
be used for representing the position of an object automaticity can be proved by showing that a second,
(Andersen 1995). Some possibilities include the position of attention-demanding task can be carried out at the same
the object on the retina (retinotopic coordinates), the time as the overlearned task without impairing perfor-
position of the object relative to the head (head-centred mance (e.g. Passingham 1996). While performing such
coordinates; Vetter et al. 1999), and the position of the tasks we are not aware of the actual state of our motor
object relative to the shoulder (shoulder-centred coordi- system, nor are we aware of our intended actions or their
nates; Flanders et al. 1992). Animal studies suggest that predicted consequences.
cells exist which code in terms of each of these different A more specific example of a reduced awareness of
coordinate systems. Cells of this type tend to be found in the actual state of the system, or at least of the sensory
parietal cortex (Colby et al. 1995; Andersen et al. 1997). feedback that indicates the actual state of the system
This brain region has a major role in the control of move- comes from studies of tickling. It is well known that the
ments, including reaching and grasping with limbs and intensity of the tactile experience when we tickle
eyes (Rizzolatti et al. 1997). Evidence from the behaviour ourselves is greatly reduced in comparison with the
of cells in this region suggests that its role in motor sensation when someone else tickles us (Weiskrantz et al.
control derives in part from an ability to translate from 1971). Corresponding to this reduction in tactile sensa-
one coordinate system to another. For example, to use tion is a reduction of activity in somatosensory cortex
visual cues to make a limb movement necessitates a trans- (Blakemore et al. 1998b). This phenomenon occurs because
lation from retinotopic to body-centred coordinates self-generated tactile sensation can be predicted from the
(Jeannerod et al. 1995). The appropriate reach depends on motor commands that generated the movements that
where our arm is in relation to the target, and is indepen- created the sensations. This prediction is based on a
dent of where we happen to be looking. Thus, in the rather precise specification. Thus, the perceived intensity
region of parietal lobe concerned with reaching, objects of a self-generated tactile sensation is markedly affected
are represented, not in terms of what they are, but in by small deviations in the timing or trajectory of the
terms of how they may be reached (equivalent to the tactile stimulus from the movement that generated it
dorsal 'how' pathway of Milner & Goodale (1995)). (Blakemore et al. 1999). For example, if there is a delay of
For such representations to be maintained the coordi- 100ms between the movement and the tactile stimula-
nates associated with each object must be altered, not tion, then the perceived intensity of the tactile stimulation
only when the objects move, but also every time we move increases even though the subject is unaware of the delay.
our eyes, limbs or body (Kalaska & Crammond 1992; In some circumstances we are unaware of even quite
Galletti et al. 1993). Consistent with this is the evidence large deviations of actual movements from those
that the receptive fields of cells in some regions of parietal expected. This seems to happen as long as the desired
cortex are 'remapped' prior to eye or limb movements state is successfully achieved. For example, Fourneret &
(e.g. Duhamel et al. 1992). Awareness of these constant Jeannerod (1998) gave false feedback about the trajectory
remappings would be confusing. In addition awareness of of an arm movement so that subjects, who could not see
the remapping is unnecessary. The changes in representa- their arm or hand, had to make considerable deviations
tion that result from our own movements are entirely from a straight movement in order to generate a straight
predictable on the basis of those movements and therefore line on a computer screen. The subjects could achieve the
do not require our attention. It seems plausible that to be desired result of drawing a straight line by making
aware of representations which changed every time we deviant movements. However, verbal reports indicated
moved our bodies, or even our eyes, would be a positive that they were unaware that they were making deviant
disadvantage. Indeed, the mechanisms that underlie our movements. It seems then that we are largely unaware of
conscious perception seem designed to maintain stability sensory feedback about the actual state of our motor
and to emphasize the unexpected. system as long as our intentions have been achieved. In
most cases successful achievement implies that sensory
(iii) Limited awareness of the actual state of the motor system feedback has been correctly predicted, but in some
In the outline of the motor control system presented in circumstances we remain unaware even of unexpected
?2(b) a major role is played by representations of the sensory feedback. When we come to consider abnormal-
predicted state of the system that will result from ities in the control of action (? 3 (a,b)) we shall see that a
intended acts. In most situations, especially those that are major insight derived from the engineering model is that
routine, the actual state of the motor system will corre- estimates of the current state of the system are not only
spond closely to the state predicted before the action was derived from sensory inputs, but also from the preceding
performed. If awareness puts an emphasis on the unex- stream of motor commands. In many situations informa-
pected, then we would predict that there would be only tion from this latter stream seems to be more important
limited awareness of the actual state of the motor system in determining the experience of the patient.
whenever this has been successfully predicted in advance.
We may only be aware of the actual sensory consequences (iv) The timing of awareness
of our movements when they deviate from what we In addition to examining which aspects of the motor
expect. control system are accessible to awareness attempts have

Phil. Trans. R. Soc. Lond. B (2000)

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1776 C. D. Frith and others Abnormalities in awareness and control of action

also been made to investigate the time at which awareness goal

emerges during the generation of an action. Libet et al.
lesion
(1983) and McCloskey et al. (1983) asked normal volun-
teers to estimate the time at which they initiated a finger desired
movement (i.e. the time at which the finger started to state

move). This reported time of awareness consistently

anticipated the actual starting time of the movement by
50-80 ms. If transcranial magnetic stimulation is applied specification
to the motor cortex then there is a substantial delay in the of movement
initiation of a movement, but there is a far smaller delay
in the perceived time of initiating the movement
(Haggard & Magno 1999). These observations imply that
our awareness of initiating a movement is not derived
from sensory signals arising in the moving limb. This
l ascttateal lsTat
information will not be available until after the limb has
started moving. In terms of the model of motor control
we are formulating here, the most likely representation actual
state
relating to awareness of movement initiation is the
predicted state of the system (e.g. the predicted position
Figure 2. The underlying disorder leading to optic ataxia.
of the limb and associated sensations; see also Haggard
The fine tuning of grasping actions afforded by the precise
et al. 1999). This can be formed as soon as the predictors
shape and position of objects is no longer available to the
have calculated the expected sensory consequences of
patient. The patient is aware that actions are clumsy.
making the intended movement.
More controversial are stiidies in which volunteers try
to indicate the time at which they are aware of having the some cases the problem resides principally in an abnorm-
'urge' to make a movement (Libet et al. 1983). This can ality of awareness rather than an abnormality of control.
precede the production of the movement by ca. 300 ms
and might correspond to the formation of the representa-
3. ABNORMALITIES OF THE PERCEPTION
tion of the intended position of the limb that precedes
AND CONTROL OF ACTION
motor preparation. Haggard & Eimer (1999) asked
subjects to indicate theltime at which 'they first began to (a) Abnormalities in the control of action while
prepare the movement' and rplated this to various compo- awareness remains unimpaired
nents of the motor readiness potential. In this study (i) Optic ataxia and otherforms of apraxia
subjects moved either their left or their right index finger. Patients with optic ataxia (Balint's syndrome) (Bailint
Haggard & Eimer (1999) found that the onset of the 1909, translated by Harvey 1995; Perenin & Vighetto
lateralized readiness potential, rather than earlier compo- 1988) have difficulty grasping objects which they can see
nents of the readiness potential, covaried with the quite clearly. Their difficulty has at least three compo-
perceived time at which preparation of the movement nents: the arm fails to extend correctly in space, the wrist
began. This observation suggests that the awareness of fails to rotate to match the orientation of the object to be
preparing to move is associated with the exact specifica- grasped, and the hand fails to open in anticipation of
tion of the movement (i.e. which finger will be moved) gripping the object (Jeannerod et al. 1994). However,
rather than some more abstract representation of action. although clumsy, the attempted movement matches the
In terms of our framework of the motor system, specifica- patient's intentions and the patient is aware of having a
tion of the goal of the movement seems not to be sufficient problem with reaching, although this is often attributed to
for awareness of preparing to move. Awareness of a problem with vision rather than a problem with move-
preparing to move requires that the controllers have ment. In terms of our characterization of the motor
completed the specification of the sequence of motor system the problem in optic ataxia occurs because the
commands needed to make the movement. Awareness of controllers are not properly finely 'tuned' by the
initiation of the movement, on the other hand, has to wait immediate context (i.e. the affordances offered by the
further until the predictors have specified the sensory shape of the object to be grasped). All other aspects of the
consequences of the movement. It is these predicted control of movement and the awareness of that control
consequences that form our awareness of initiating the remain intact (figure 2).
movement. However, the controllers do not rely solely on the
In this brief review we have presented evidence that immediate affordances provided by the sight of the object
some, but not all aspects of the motor control system are that is to be grasped in order to derive an appropriate
accessible to awareness. In the remainder of this paper we sequence of motor commands. Relevant information is
will discuss a variety of human movement abnormalities also available from memory and can be used in the
and attempt to convince the reader that the model of the absence of affordances. As a result some patients can
motor system illustrated in figure 1 provides a useful and grasp a well-known object such as a lipstick more accu-
unifying framework for understanding these various rately than an unknown object of exactly the same shape
disorders. We shall also suggest that to understand these (Jeannerod et al. 1994). In this example the information
disorders it is important to consider the patient's aware- used by the controllers comes from long-term knowledge
ness of different aspects of the motor control system. In about objects. Relevant information is also available from

Phil. Trans. R. Soc. Lond. B (2000)

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 Abnormalities in awareness and control of action C. D. Frith and others 1777

short-term memory, although this is not as useful as reaching (Clower et al. 1996). There is as yet little
actual sight of the object. If vision of the object to be evidence that other forms of apraxia can be related to
grasped is removed for only a few seconds then the specific lesions, largely because there is so little agreement
reaching and grasping of normal subjects is impaired as to how to classify the different forms of apraxia.
(Goodale et al. 1994; Rossetti 1998). The information
available in short-term memory in this situation may be (ii) The 'anarchic hand'sign
derived from representations about the position and Patients showing the anarchic hand sign (sometimes
nature of the object rather than representations specifi- known as the alien hand sign, see Marchetti & Della
cally tailored for grasping the object. Patient D.F., who Salla (1998)) have a hand that moves 'of its own accord'
could grasp objects without being able to recognize them, without the will of the patient. In one case it was noted
completely lost her ability to grasp objects after a short that the patient had picked up a pencil and 'had been
delay during which the object was not visible. In contrast, scribbling with the [affected] right hand ... She then
the reaching behaviour of a patient with optic ataxia can indicated th at she had not herself initiated the original
improve after a short delay in the dark (Milner et al. action of the right arm ... She experienced a feeling of
1999). Presumably this is because, for this patient, infor- dissociation from the actions of the right arm, stating ...
mation about the object in short-term memory, although that "it will not do what I want it to do"' (Goldberg et al.
not ideal for grasping, is better than the faulty informa- 1981, p. 685). In another case the patient's 'left hand
tion provided by the sight of the object. would tenaciously grope for and grasp any nearby object,
Optic ataxia is one of many forms of apraxia: difficulties pick and pull at her clothes, and even grasp her throat
in making voluntary movements in the absence of a during sleep . .. . She slept with the arm tied to prevent
primary motor defect. In terms of our model, apraxia nocturnal misbehaviour. She never denied that her left
occurs when there is insufficient information for the arm and hand belonged to her, although she did refer to
controllers to construct an appropriate sequence of motor her limb as though it were an autonomous entity' (Banks
commands. This suggestion relates closely to the sugges- et al. 1989, p. 456). Typically the anarchic hand grasps
tion of Pause et al. (1989, p. 1599) that 'the motor disability objects in its vicinity in an inappropriate manner; it will
... does not lie in the loss of kinetic memory to perform grasp doorknobs or pick up a pencil and scribble with it.
movements, but in the loss of their evocation by appro- Patients clearly recognize that there is a discrepancy
priate sensory stimuli'. Because relevant information between what the hand is doing and their desired actions.
comes from many different sources there can be many The patients are upset by the actions of the hand and will
different forms of apraxia. We have already mentioned often try to prevent it from moving by grasping it firmly
patients who can grasp a lipstick (information derived with the other hand.
from long-term knowledge), but not a neutral cylinder of In many ways the patient with an anarchic hand
the same shape (information derived from immediate sight shows the converse problem to the patient with optic
of the object). Other patients are unable to produce an ataxia. We have just reviewed (? 3(a) (i)) the evidence
action to command, e.g. they cannot obey the command that the parietal cortex contains representations of the
'to blow', but, when presented with a lit candle will blow it various objects in our immediate environment in terms of
out. In these cases information can be used from the sight the appropriate movements needed to reach and grasp
of the object, but not from verbal commands. De Renzi et them. The patient with optic ataxia fails to form these
al. (1982) have formally demonstrated other such dissocia- representations and therefore has difficulties with
tions, finding patients who can mime the use of an object reaching and grasping. In the patient with an anarchic
to verbal instruction, but cannot imitate the same gesture hand these representations are activated inappropriately.
when performed by someone else, and also finding patients The sight of an object is sufficient to elicit the movement
with the opposite pattern of disorder. even though this does not fit with the patient's current
In ? 2(c) (ii) we discussed the need to translate between goals. In terms of our characterization of the motor
different coordinate frames in order to use visual informa- system, the movements of the anarchic hand occur
tion to generate movements (Andersen 1995). Patients because the effects of the affordances supplied by the
with apraxia seem to have lost the ability to translate immediate visual environment are no longer inhibited by
certain kinds of information into coordinates appropriate the currently intended action (figure 3). However, the rest
for constructing actions. We also mentioned the evidence of the system is intact. Representations of the intended
from animal studies that the parietal cortex may have a and actual positions of the hand are available, so that
major role in translating from one coordinate frame to patients know that the behaviour of the hand does not
another (Colby & Duhamel 1996). Apraxia can occur conform with their intentions.
after damage to many brain regions, but is particularly What is the brain mechanism which prevents us from
associated with damage to the parietal lobe (De Renzi & responding to every graspable object in our environment?
Lucchelli 1988). With regard to optic ataxia, lesions in the The anarchic hand sign is often associated with unilateral
superior parietal cortex (or more precisely in the IPS damage to the SMA contralateral to the anarchic hand
between BA7 and 39) impair the ability to make accurate (Goldberg et al. 1981). The anterior part of the SMA is
reaching and grasping movements in both man (Perenin considered to one of a number of 'higher-order' motor
& Vighetto 1988) and monkey (Gallese et al. 1997; Rush- areas in contrast to areas, such as the primary motor
worth et al. 1997) (for a discussion of the precise location cortex, with are directly concerned with execution
of the critical area in parietal cortex see Passingham (Pickard & Strick 1996). In contrast to executive motor
(1998)). Imaging studies of grasping in healthy volunteers regions, the anterior SMA does not show increasing
also implicated the IPS in the control of visually guided activation with increasing force (Dettmers et al. 1995). On

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1778 C. D. Frith and others Abnormalities in awareness and control of action

(There is some evidence that the anarchic hand is often

associated with damage to the anterior corpus callosum
1 ~~~~lesion as well as the SMA (Parkin 1996). In these cases the
desired discrepancies unwanted actions of the anarchic hand often consist of
interference with the actions of the other hand, rather

affordances (
than unintended grasping behaviour. For example, the
anarchic left hand might undo buttons that the right
hand had just done up. This behaviour would also be
specification explained in terms of a failure of inhibition. However, in
of movement './
these cases the inhibition arises from signals concerning
the behaviour of the hand selected for performing the
\ | . Iedcte action. These inhibitory signals fail to be transmitted
through the corpus callosum.)
We have argued that patients with optic ataxia and the
anarchic hand have disorders of motor control, but no
associated disorder in their awareness of the motor
v~~~~~ -
system. This is because the impairment concerns the
actual
state mechanisms by which the controller constructs and selects
the precise movements required for an action. These
Figure 3. The underlying disorder leading to an anarchic processes are not available to consciousness. In ? 3(b) we
hand. The actions of the hand are no longer controlled by the
shall consider syndromes in which motor impairments are
intentions of the patient. Instead the hand makes stereotyped
associated with abnormalities of awareness.
responses to objects in the environment. The patient is aware
of the discrepancies between intentions and the actions of the
hand.
(b) Abnormalities of motor control and awareness
(i) Phantom limbs
After amputation of all or part of a limb many patients
the other hand, unlike executive motor regions the report that they experience a phantom limb. Although
anterior SMA is activated specifically in tasks requiring they know that there is no limb they still feel the presence
selection between different movements (Deiber et al. 1991), of it (Ramachandran & Hirstein 1998). Some patients
especially when these movements have to be made only in report being able to move their phantoms voluntarily,
the imagination and not actually executed (Stephan et al. while others experience their phantom as paralysed and
1995). When the precise timing of events is investigated cannot move it even with intense effort. If the limb was
there is evidence that some neurons in the anterior SMA paralysed before amputation the phantom normally
are active during movement preparation, but not during remains paralysed. If not, then typically immediately
movement execution (Rizzolatti et al. 1990). Ball et al. after amputation patients can generate movement in the
(1999) using combined electroencephalography and func- phantom. However, with time they often lose this ability
tional magnetic resonance imaging observed a sharp (Ramachandran 1993). Some finger amputees experience
drop in activity in an area referred to as intermediate their phantom fingers only when they flex the fingers in
SMA that coincided with a sharp increase in activity in the intact hand as when making a fist or grabbing a cup.
primary motor cortex just before execution of a move- There is frequently a latency of 2-3 s before the phantom
ment. They suggest that the function of this region of the emerges and when the normal fingers are extended again
SMA may be essentially inhibitory, so that a movement the phantom takes 2-3 s to disappear (Ramachandran
can only be initiated by primary motor cortex when 1993). In these cases the position of the phantom is deter-
activity in the anterior SMA drops. This would account mined by the actions of the contralateral limb and there
for the preferential activation of the anterior SMA when is a marked delay in the formation of the phantom.
movements are imagined because in such cases execution The existence of phantom limbs has long seemed
must be inhibited. Such a role for the anterior SMA could deeply mysterious. How is it possible to experience a limb
explain why an 'anarchic hand' should be released when in a particular position in space when there is no limb
this region is damaged. and, as a result, the brain is no longer receiving any
The major projections to motor cortex (area 4) come relevant somatosensory or proprioceptive information?
from lateral and medial premotor areas (area 6, including There is now substantial evidence for neural plasticity in
the SMA) and from parietal cortex (areas 5 and 7b in the mature human brain. After amputation of a limb
the monkey, probably equivalent to areas 5 and 40 in there is reorganization of the deafferented region of
man; see Passingham 1993). This pattern of projections is cortex. As a result stimulation of the skin of distant areas
consistent with the idea that signals arising in parietal such as the face or the chest can elicit sensation in a
cortex enable motor cortex to generate appropriate phantom arm (Ramachandran et al. 1992; Aglioti et al.
reaching and grasping movements to any object in the 1994; Kew et al. 1997). Thus the experience of the presence
immediate environment, while signals arising in the SMA of a phantom limb can be supported by somatosensory
permit selection of the one movement appropriate to signals coming from other parts of the body. The presence
current intentions. Unilateral damage to what is probably of proprioceptive signals from other limbs can also
a rather circumscribed region of the SMA releases explain how a patient can experience a phantom in the
inappropriate reaching and grasping in the contralateral positions occupied by the intact contralateral limb.
hand, creating an anarchic hand. However, these mechanisms cannot explain cases in

Phil. Trans. R. Soc. Lond. B (2000)

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 Abnormalities in awareness and control of action C. D. Frith and others 1779

which the position of the phantom is not determined by 1978). Unfortunately the precise location of the lesion in
the positions of other limbs or cases in which the patient this case was not specified.
can voluntarily move the phantom. Our explanation of
these phenomena is that the estimated position of a limb (ii) Missing limbs
is not solely based on sensory information, but also on the After peripheral deafferentation of a limb the patient
stream of motor commands issued to the limb muscles. will often develop a phantom even though the deaffer-
On the basis of these commands the predictor can esti- ented limb is still present. This phantom may be
mate the new position of the limb before any sensory contained within the real limb, but, in some circum-
feedback has been received. Indeed, as we have already stances, may become separated from the limb and
argued, the normal experience of the limb is often based become supernumerary (e.g. Kew et al. 1997, subject 2).
on this predicted state, rather than the actual state. Even However, in other cases patients do not develop phan-
in the absence of a limb, streams of motor commands can toms, but rather are unaware of the existing limb unless it
still be issued. If these commands lead to the prediction can be seen. We are not aware of any systematic compar-
of movement then the phantom will be experienced as ison of deafferented patients who develop phantoms with
moving. However, the motor control system is designed to those in whom the limb fades. However, a study of cases
adapt to changing circumstances. Since the limb does not reported in the literature suggests that the critical differ-
actually move there is a discrepancy between the ence lies in whether or not the deafferented limb is also
predicted and the actual consequences of the motor paralysed. The cases described by Kew et al. (1997) who
commands. With time the predictors will be modified to developed phantoms had limbs that were deafferented
reduce these discrepancies. At this point the issuing of a and paralysed. In contrast the patient described by Cole
stream of motor commands will not lead to the prediction (1991) was completely deafferented for touch, but was not
of a change in limb position. Such adaptation in the paralysed and achieved a remarkable degree of motor
predictors could explain why patients eventually lose the control which was largely based on visual feedback. This
ability to move their phantoms. patient never developed a phantom, but for him and his
Such adaptation of the predictors would also explain body it was literally 'out of sight, out of mind' (Cole
how Ramachandran & Rogers Ramachandran (1996) 1991).
were able to reinstate voluntary movement of the phantom Most deafferented patients in whom the motor output
by providing false visual feedback of a moving limb corre- system remains intact are unwilling to attempt move-
sponding to the phantom. This was achieved by placing a ments because they are so inaccurate. Rothwell et al.
mirror in the midsaggital plain. With the head in the (1982) demonstrated that a patient with peripheral
appropriate position it was possible for the patient to see deafferentation was unable to make automatic reflex
the intact limb at the same time as the mirror reflection of corrections to movements and was unable to sustain
this limb. This reflection so closely resembles the missing constant levels of muscular contraction or maintain long
limb that the patient has the strong illusion of seeing the action sequences in the absence of visual feedback. The
missing limb. If the intact limb is moved then the patient lack of a sensation of the current position of the limb is
receives from the mirror visual feedback of movement in not only a problem for checking the success of movement
the missing limb. For most patients moving their hand in through feedback. It also creates a problem because the
this mirror box rapidly leads to the perception that they computation by the controllers of the appropriate move-
are now able to move the phantom limb again. In some ment requires that the starting position of the limb must
cases this perception continues even when the mirror box be known.
is no longer being used. Similar problems can occur after brain damage in
In a reformulation of the proposals of Ramachandran somatosensory areas as a result of which the patient can
& Rogers Ramachandran (1996), we suggest that the no longer experience the limb contralateral to the lesion.
false visual feedback supplied by the mirror box allowed Jeannerod et al. (1986) described a patient with hemi-
the predictors to be updated. In consequence the anaesthesia after damage involving the right inferior
efference copies produced in parallel with the motor parietal lobe. The patient could initiate simple single-
commands now generated changes in the predicted posi- component movements, but could not make complex
tion of the missing limb corresponding to what the multicomponent movements with his left hand in the
patient had seen in the mirror. absence of visual feedback. Wolpert et al. (1998) describe
Ramachandran & Hirstein (1998) proposed that an interesting variant of this phenomenon. Patient P.J.
dynamic images of the body are formed in the parietal had a large cyst in the left parietal lobe and reported the
lobes and provide the basis for the experience of phantom experience of the position and presence of her right limbs
limbs. This formulation resembles our suggestion that fading away over seconds if she could not see them. Her
parietal cortex is involved in the representation of experience of a constant tactile stimulus or a weight also
predicted limb positions. However, as we have seen, the faded away, but changes in such sensations could be
parietal lobe contains representations of limb positions in detected. Slow reaching movements to peripheral targets
terms of many different coordinate systems. Which of with the right hand were inaccurate, but reaching move-
these particular coordinate systems relates to the experi- ments made at a normal pace were unimpaired. In this
ence of phantoms and the precise locations for such repre- case there seemed to be a circumscribed problem with the
sentations remains to be determined. Evidence that representation of the current limb position in that it could
phantom limbs are represented in the parietal cortex not be maintained in the absence of changing stimulation.
comes from the observation that a phantom limb patient In all these cases of deaffierentation without paralysis,
lost his phantom after a right parietal stroke (Sunderland visual signals provide the only sensory information for

Phil. Trans. R. Soc. Lond. B (2000)

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1780 C. D. Frith and others Abnormalities in awareness and control of action

making accurate movements. They provide information The extra phantom limb experienced by the patient
about the position of a limb prior to movement and of Hari et al. (1998) emerged after a subarachnoid
provide feedback about the accuracy of the movement. haemorrhage leading to an infarction in the right frontal
As a result the motor control system will learn to ignore lobe including damage to the most anterior region of the
somatosensory and proprioceptive signals when right SMA. However, brain scans suggested that there
predicting the outcome of movements or estimating the was also a congenital abnormality in the corpus
current state of the system. It will learn to base such esti- callosum.
mates solely on the stream of motor commands and In our discussion of the anarchic hand sign (? 3(a) (ii))
upon visual information. In the absence of visual signals we suggested that the SMA, in particular the anterior
the estimates cannot be made and the experience of the part, has a major role in initiating movements and inter-
limb fades away. acts with the parietal cortex in order to ensure that the
In patients with deafferentation and paralysis no move- movement initiated corresponds to the desired action.
ments can be made and so the system has no chance to The case described by Hari et al. (1998) in which damage
learn to attend to one modality of sensation rather than to the anterior SMA was associated with an extra
another. The experience of a phantom can therefore be phantom left arm suggests that this interaction between
driven by sensations from other limbs that have been SMA and parietal cortex may also ensure integration
remapped into the deafferented cortical region. between representations of predicted and actual limb
positions. Damage to the anterior SMA can result in a
(iii) Supernumerary limbs failure of this integration.
Patients sometimes report experiencing one or more
supernumerary limbs in addition to their real ones (iv) Anosognosia
(Vuilleumier et al. 1997). Of particular interest is the A patient with anosognosia is unaware of some impair-
patient described by Hari et al. (1998) who reported experi- ment that has resulted from brain damage (Babinsky
encing an additional left arm. The extra arm occupied the 1914). Here we shall be concerned only with those patients
position vacated by the real left arm a minute or so in whom the impairment concerns the motor control of a
previously. The felt position of the phantom extra arm limb. Such patients typically have right-hemisphere
mirrored the voluntary (but not passive) movements of the damage leading to paralysis (or weakness) on the left side
right arm. Experience of the extra arm ceased if the usually associated with hemianaesthesia. In ? 3(b) (ii) we
patient moved her left arm or looked at it or had it touched. argued that this combination provides the appropriate
The estimated position of a limb is based on integrating circumstances for the development of a phantom limb.
information from motor commands and sensory feedback. However, these patients, rather than developing a
Failure to integrate these two sources of information phantom limb, develop the false belief that there is
could lead to the experience of two limbs rather than one. nothing wrong with the paralysed limb. For example, the
At the time of initiating action the patient of Hari et al. left side of Mrs ED.'s body was completely paralysed as
(1998) has the normal awareness of movement based on the result of a stroke.
the representation of the predicted position of the arm.
Doctor: 'Mrs ED., can you walk?'
However, the representation of the estimated actual
ED.: 'Yes.'
position of the arm fails to get updated on the basis of the
Doctor: 'Can you move your hands?'
motor commands. This discrepant representation of the
F.D.: 'Yes.'
estimated position of the arm emerges into awareness
Doctor: Are both hands equally strong?'
some time after the movement has been completed
ED.: 'Yes, of course they are.'
leading to the experience of an extra arm. Correct
(Ramachandran 1996, p. 124)
updating of this representation occurs on the basis of
signals from the somatosensory or visual system. Sometimes patients will attempt to 'explain away' the
However, false updating can also occur based on motor lack of movement in the paralysed limb.

commands controlling the right limb. This false updating Doctor: 'Mrs L.R., why aren't you using your left arm.'
must be based on motor commands rather than sensory
L.R.: 'Doctor, these medical students have been prodding
feedback since passive movements of the right arm do not me all day and I'm sick of it. I don't want to use my left
affect the phantom. Presumably the effect of signals arm.'
concerning movements of the right limb are normally (Ramachandran 1996, p. 125)
suppressed when they are discrepant from the motor
In some cases the patient will claim to have moved a
commands driving the left limb. We are suggesting that
limb to command even though no movement has
movement of the phantom in this case derives from motor
occurred.
signals relating to the contralateral limb. This is different
from the mechanism underlying the phenomenon Doctor: 'Can you clap?'
described by some amputees in which the fingers of the F.D.: 'Of course I can clap.'
phantom follow the movements of fingers on the contra- Doctor: 'Will you clap for me?'
lateral hand. In these cases it is assumed that the experi- The patient proceeded to make clapping movements with
ence is driven by somatosensory and proprioceptive her right hand as if clapping with an imaginary hand
signals from the contralateral fingers. If this is so, then near the midline.
movements of the phantom in amputees should be experi- Doctor: 'Are you clapping?'
enced whether the contralateral finger movements are F.D.: 'Yes, I am clapping.'

active or passive. (Ramachandran 1996, p. 124)

Phil. Trans. R. Soc. Lond. B (2000)

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 Abnormalities in awareness and control ofaction C. D. Frith and others 1781

This disorder is often associated with unilateral neglect goal

for the left side of space. Geschwind (1965) suggested that
no discrepancy
anosognosia arises from a disconnection such that sensory
feedback (both somatosensory and visual), indicating that desired
the limb is not working, is no longer available to a left- state

hemisphere monitoring system. However, making sure affordances

that the paralysed left arim can be seen in the right visual
field does not alter the denial of impairment. Heilman specification
et al. (1998) have proposed a 'feed-forward' theory of \of movement/ '
anosognosia. According to this account anosognosic
patients receive no signals indicating movement failure
because the comparator which contrasts intended and
actual movements receives no signal that a movement has
A= ~~~~predicted
been intended. Because patients do not try to move the
paralysed limb they never discover that it is paralysed.
While this account can explain denial of impairment, it is
not clear how it can explain cases, such as the one
described above, in which the patient apparently experi-
discrepancies
ences having made a movement when none has actually ignored
occurred. lesion
How is it possible to experience a limb movement
when none has actually occurred? On the basis of our Figure 4. The underlying disorder leading to anosognosia.
The patient formulates the action needed to fulfil his intention
review of evidence concerning the normal awareness of
and is aware that the action initiated is appropriate. No
motor control we suggested that awareness of initiating a
information about the actual position of the limb is available
movement was based on a representation of the predicted
to indicate that no action has actually occurred.
consequences of making that movement, rather than its
actual consequences. A representation of the predicted
consequences of a movement can be formed as long as the of the limb. The lack of a discrepancy between intended
controllers can compute the appropriate motor and predicted positions indicates success. Contrary
commands and the predictors can derive from these the information derived from sensory feedback concerning
expected consequences. Thus, a patient with a paralysed actual limb positions is not available, since the relevant
limb would have the normal experience of initiating a brain regions have been damaged or else this contrary
movement with that limb as long as the controller and information is neglected (figure 4). As a result the
predictor were functioning normally. However, to estimated position of the limb is based on sequences of
continue to believe that he or she had initiated that motor commands and not upon sensory feedback.
movement would require further abnormalities in the Anosognosia is usually associated with damage to the
system. First, there would have to be a failure to register right hemisphere, especially the parietal lobe. However,
the discrepancy between the predicted consequences and there is, as yet, no information about the precise location
the actual consequences of the movement that was of the lesions that lead to the illusion that a paralysed
initiated. We have already quoted the work of Fourneret limb is being moved normally. Damage to the parietal
& Jeannerod (1998) demonstrating that normal people lobe is most frequently associated with apraxia rather
can have a remarkably limited awareness of the actual than anosognosia and apraxic patients can sometimes
form of the movements they have made. Thus, the patient show features of anosognosia. For example, Sirigu et al.
with anosognosia is showing, in exaggerated form, a (1999) studied three patients with apraxia while they
tendency already present in the normal state. The exag- performed gestures to command (e.g. extend index and
geration of this tendency could be related to the neglect of little finger). On some trials the patients saw their own
the left side of space often shown by such patients. hand performing the gesture, but on other trials they saw
Second, there would have to be a failure to update the the hand of an experimenter performing the same or a
operations of the predictor. With experience the predictor different gesture. On nearly 90% of trials in which the
should learn that the motor commands issued by the patients saw the experimenter making accurately the
controller result in minimal movements of the paralysed gesture that they were trying to make they believed that
limb. In the patient with anosognosia this updating does they were observing their own hand even though they
not occur. had actually made a very clumsy gesture. In these cases
We suggest, then, that the false experience of move- false visual feedback elicited a form of anosognosia.
ment reported by patients with anosognosia occurs However, the patients were not generally anosognosic.
because, while representations of the desired and When they saw their own hand they recognized and were
predicted positions of the limb are appropriate, the distressed by the clumsiness of their gestures. Further-
patient is not aware of the discrepant representation of more, the lesions in these cases were in the left parietal
the actual position of the limb. The controllers issue the cortex, which is typical for apraxia, rather than the right
appropriate motor commands, but, due to paralysis, do parietal cortex, which is typical for anosognosia.
not generate a limb movement. However, the predictors In another experiment Sirigu et al. (1996) investigated
have estimated, on the basis of these commands and from the effects of parietal lobe lesions (both left- and right-
past experience prior to brain damage, the new position sided) on the time needed to make imaginary movements.

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1782 C. D. Frith and others Abnormalities in awareness and control of action

How long we take to make movements in the imagination elicits a stereotyped action which is inappropriate in the
depends upon the functioning of the predictor, not upon wider context. For example, if there is a glass within
the actual state of the system. Sirigu et al. (1996) showed reach of the patient, he will grasp it. If a bottle of water is
that a patient with unilateral damage to the motor cortex placed on the desk he will grasp this too and then pour
showed strong correlations between the time to make water into the glass and drink it. Such behaviour is not
actual movements and the time to make imaginary move- shown by normal subjects put in the same situation or by
ments with both the intact and the impaired hand. For patients with posterior lesions.
the impaired hand the times for actual and imagined
'If the examiner asks the patient why he grasped the
movements were much slower. In this case the predictor
objects and used them, then the answer is always the
had been updated to take account of the changed abilities
same, "You held them out to me, I thought I had to use
of the impaired hand. In contrast patients with parietal
them."
lesions did not show this close link between actual and
The examiner then ... gives the instruction, "You are
imagined movements in the limb contralateral to the
mistaken; from now on don't grasp any of the objects I
lesion. In these cases the discrepancies between predicted
will show you, and in no case must you use them."
and actual movements have not been used to update the
After about 20-30 s, during which time the patient's
estimates made by the predictors.
attention has to be distracted ... the behaviour remains
Clearly damage to parietal cortex can impair awareness
unchanged. If the examiner asks if the patient remembers
of the actual state of the motor system and also lead to failure
the instruction, the latter replies, most of the time, "It's
to take note of discrepancies between the actual and
true, I remember."
predicted states of the system. However, though these
"Then why [did you grasp the objects]?"
problems may be necessary for anosognosia they do not
"Because you held out the objects to me and I thought I
seem to be sufficient. Another consequence of parietal
had to reach and grasp them."' (Lhermitte 1983, p. 246)
lesions is unilateral spatial neglect. This syndrome, espe-
cially in its perceptual form, is usually associated with Much more complex actions can also be elicited by the
lesions in the right inferior parietal lobe (Vallar & Perani environment in which the patient finds himself.'Patient 1
1986) and is often associated with anosognosia. Patients with ... came to see me at my apartment .... We returned to
neglect fail to notice or respond to objects and events in their the bedroom. The bedspread had been taken off and the
left hemifield. Neglect of this kind would allow even visual top sheet turned back in the usual way. When the patient
evidence that a movement had not been made to be ignored. saw this he immediately began to get undressed [including
Ramachandran (1996) considered that the accounts of taking off his wig]. He got into bed, pulled the sheet up to
anosognosia of the kind outlined above are not sufficient to his neck and prepared to go to sleep.' (Lhermitte 1986,
explain the extent to which anosognosic patients can p. 338).
ignore the wealth of evidence indicating that they are On the surface this behaviour is very similar to that
paralysed. He proposes that there are additional factors at associated with the anarchic hand. Actions are elicited by
work which enable patients to ignore sensory anomalies. objects in the environment even though such actions are
These factors have parallels with those associated with not appropriate. However, there is an additional problem
delusions and confabulations. Confabulations are more which is reflected in the patient's experience of this
usually associated with memory impairments. The patient disorder of control. The patient showing utilization
recollects past events which did not and, indeed, could not behaviour does not perceive a discrepancy between his
have happened. The patient seems to be unaware of the actions and his intentions. He is not upset by the actions
impossibility of what he or she is reporting. Such problems and he does not develop strategies to prevent the actions
are typically associated with damage to the right frontal occurring. On being asked why he performed the actions
cortex (Burgess & Shallice 1996), which is believed to have the patient will'rationalize', saying that he performed the
a role in monitoring the consequences of action at a high action because he thought that is what the examiner
level. There is evidence that this role also applies to the wanted him to do. Our formulation of utilization beha-
motor system. For example, if a normal volunteer is viour is that the patient's actions are involuntarily elicited
performing a task with two hands, but one hand is hidden by objects in the environment, but that the patient
behind a mirror, then the illusion is created that both erroneously experiences these actions as intended.
hands are seen, when, in fact, the subject is viewing a Problems with the experience of intention are not
single hand and its mirror image. In this case, if the task is unique to these patients. Normal three-year-old children
to move the hands out of phase, the visual feedback falsely do not distinguish between an intentional movement and
indicates that the hands are moving in phase. Performance a knee-jerk reflex. Only at five years do children state
of this somewhat disturbing task in which there is a discre- that the knee-jerk reflex was unintended (Schultz et al.
pancy between expectations derived from intended move- 1980). Three-year-old children, however, do state that
ments and what is actually seen, elicits activity in right their movement was unintended in the interlaced finger
dorsolateral prefrontal cortex (Fink et al. 1999). It is plau- game. In this task the child can see that the designated
sible that damage to this region might result in failure to finger remains stationary while the wrong finger moves.
respond to such discrepancies. The child has a clear goal which has not been achieved.
The lack of success is taken to indicate a lack of intention.
(v) Utilization behaviour In the case of the knee-jerk reflex there is no simple prior
Some patients with damage to the frontal lobes show goal, and thus a judgement cannot be made as to whether
'utilization behaviour' (Lhermitte 1983) in which the or not the movement was successful. Smith (1978)
patient uses objects inappropriately. The sight of an object suggested that, without an explicitly stated goal, the

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 Abnormalities in awareness and control of action C. D. Frith and others 1783

goal lesion
The high-level control system we are describing here is
based on the supervisory attentional system developed by
no intention to be Shallice (1988, pp. 328-352) to explain the behaviour of
discrepant with
patients with frontal lobe lesions. These patients have no
e d ---------- -------------- -/ problems in routine situations, but have difficulty coping
affordances with novel tasks. With such tasks they may make
inappropriate routine responses (a form of utilization
behaviour) or they may fail to respond. This response
sp c fcationX ,/ failure occurs because, in novel situations it is not only
\of movement/ './
necessary to inhibit inappropriate responses elicited by
objects in the environment, but also to initiate responses
when there is no external stimulus to elicit them.
While there is good evidence that this high-level
control system is instantiated in prefrontal cortex (Shal-
/"movement lice 1988), it has proved more difficult to relate particular
components of this system to specific regions within
actual prefrontal cortex. Imaging studies suggest that dorso-
state lateral prefrontal cortex (BA46 and 9) is particularly
involved in selection between alternative actions when
Figure 5. The underlying disorder leading to utilization there are no external cues to indicate which action is the
behaviour. The patient does not form any intentions and so most appropriate (Jahanshahi & Frith 1998). However,
makes stereotyped responses to objects in the environment. utilization behaviour seems to more concerned with
The patient is not aware that these responses are failure to inhibit inappropriate movements rather than a
inappropriate. failure select appropriate ones. There is some evidence
that the lesions that produce utilization behaviour are
default judgement is that actions are intended. Only by more likely to involve the ACC (Degos et al. 1993). Such
the age of five can the child form the much more abstract lesions are also associated with difficulties in inhibiting
goal of 'not moving' in order to interpret the knee-jerk routine responses, for example, inhibiting saccades to
reflex correctly. peripheral stimuli (Paus et al. 1991).
A corollary of this argument is that, if an explicit goal There is also, as yet, little evidence concerning brain
is formed just prior to an action which achieves that goal, areas concerned with awareness of intended actions. In
then the action will be perceived as intended. Wegner & one of the few relevant imaging studies Jueptner et al.
Wheatley (1999) have used just this technique to elicit the (1997) trained volunteers until they could perform a
erroneous perception of intended action in normal adults. paced sequence of button presses routinely and without
A subject and a confederate simultaneously used a single thought. The volunteers were then scanned, either while
mouse to control the position of a pointer on a screen. If performing this task in routine mode, or when deliber-
the attention of the subject was drawn to an object on the ately thinking of which button had to be pressed next in
screen shortly before the pointer stopped near that object, the sequence. The requirement to be aware of their
then the subject frequently believed that he had intention- intended action increased activity in dorsolateral
ally moved towards the object even though in reality his prefrontal cortex and in the ACC (BA32). There are no
arm had been moved passively by the confederate. As direct connections between these regions and motor
long as the action did not conflict with some explicitly cortex, so that their influence on movement is mediated
formed goal then the action was perceived as intended. via their connections with premotor regions including the
These results suggest that the experience of an action SMA (Lu et al. 1994). On the basis of their study of
as intended depends on the relationship between the patients with medial frontal lesions, Paus et al. (1991)
action and a prior goal. If the action does not match the concluded that the ability to inhibit routine responses
goal then the action is unintended. If, however, there is depends upon input from the ACC to the SMA. Thus, the
no prior goal then, by default the action is perceived as same system has been implicated both in the awareness of
intended. In these terms utilization behaviour can be intended actions and in the inhibition of routine actions.
explained as resulting from a failure to represent goals. These proposals are also in accord with our suggestion
We suggest that the problem causing utilization behaviour that utilization behaviour is caused by damage to an
occurs at an earlier stage in the development of an action earlier stage in the system that generates actions than that
than that causing the anarchic hand. The problem has associated with the anarchic hand.
two components. First, there is no awareness of goals and
intended actions (figure 5). The patient is not aware of (c) Abnormalities in the perception of action while
what he is going to do until after he has done it. Second, the control of action is largely intact
inappropriate responses elicited by objects in the environ- (i) Delusions of control; passivity experiences associated with
ment are not inhibited. These components can be related schizophrenia
if we assume that a lack of awareness of intentions reflects Many patients with schizophrenia describe 'passivity'
a failure to develop such intentions. Responses to objects experiences in which actions, thoughts or emotions are
in the environment are normally inhibited until an made for them by some external agent rather than by
intention has been developed. The system that develops their own will. 'My fingers pick up the pen, but I don't
intentions also inhibits inappropriate responses. control them. What they do is nothing to do with me.'

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1784 C. D. Frith and others Abnormalities in awareness and control ofaction

goal false delusions of control, the awareness of the sensory conse-

discrepancy no quences of the movement precedes the awareness of initi-

ating the movement, which is in the opposite order to the
discrepancy
desired normal experience of our own agency. We suggest that, in
state the presence of delusions of control, the patient is not
affordances aware of the predicted consequences of a movement and
is therefore not aware of initiating a movement.
There is nothing obviously abnormal in the motor
specification l
control of these patients. This suggests that accurate
representations of predicted states are available and used
by the motor system. However, these representations are
ofmovement/ f not available to awareness. A number of experiments
confirm that there are subtle problems consistent with a
lack of awareness of predicted actions. These patients fail
to make rapid error corrections based on awareness of
discrepancies between intended and predicted limb posi-
actual tions, although they have no difficulty correcting errors
state
based on visual feedback about actual limb positions
abnormality
(Malenka et al. 1982; Frith & Done 1989). These patients
have difficulty remembering the precise details of actions
Figure 6. The underlying disorder leading to delusions of made in the absence of visual feedback (Mlakar et al.
control. The patient formulates the action appropriate to his
1994; Stirling et al. 1998). They also have difficulty
intention and the action is successfully performed. The
distinguishing between correct visual feedback about the
patient is aware that the action matches the intention, but
position of their hand and false feedback when the image
has no awareness of initiating the action or of its predicted
of the hand they see is in fact that of another person
consequences. The patient feels as if his intentions are being
monitored and his actions made for him by some external attempting to make the same movements as the patient
force. (Daprati et al. 1997).
Jeannerod (1999) suggested that conscious judgement
about a movement requires a different form of representa-
'The force moved my lips. I began to speak. The words tion from that needed for comparisons of predictions and
were made for me.' (Mellors 1970, p. 18). In most cases the outcomes within the motor system. Following Barresi &
actions made when the patient 'feels' that he is being Moore (1996) (see also Frith 1995) he suggests that
controlled by alien forces are not discrepant with his conscious judgements about movements require 'third-
intentions. Thus the patient may be correctly performing person' information while control of movement depends
the task set by the experimenter (e.g. making random upon private 'first-person' information. In terms of this
movements of a joystick) at the same time as having the formulation he suggests that schizophrenic patients fail to
experience of passivity (see Spence et al. 1997). The monitor the third-person signals that enable them to
patient does not try to correct these 'controlled' actions or make judgements about their own actions. We would
prevent them from occurring. Clearly actions are being suggest, rather, that, in schizophrenia, something goes
correctly selected and irrelevant affordances are being wrong with the mechanism that translates the first-person
suppressed. representations that are involved in motor control into the
We have previously suggested that these abnormal third-person representations that are needed for conscious
experiences arise through a lack of awareness of intended monitoring of the motor control system. This is part of
actions (Frith 1987). However, this formulation is incon- more general problem that these patients have in escaping
sistent with the patients' ability to follow the commands from a first-person, egocentric view of the world.
of the experimenter, to avoid showing utilization Spence et al. (1997) used brain imaging to identify
behaviour, and to correct errors on the basis of sensory brain regions associated with the experience of delusions
feedback about limb positions (which requires compar- of control. They scanned schizophrenic patients with and
ison of intended actions and their consequences). Instead without such delusions while they performed a response
we suggest that the experience of alien control arises from selection task. The presence of delusions of control was
a lack of awareness of the predicted limb position associated with overactivity in right inferior parietal
(figure 6). As a result the patient is not aware of the exact cortex. We suggest that this overactivity reflected a
specification of the movement. He is aware of his goal, of heightened response to the sensory consequences of the
the intention to move and of the movement having movements the patients were making during scanning.
occurred, but he is not aware of having initiated the Normally activity associated with sensory stimulation is
movement. It is as if the movement, although intended, much reduced if this stimulation is the direct conse-
has been initiated by some external force. In a variation quence of our own movements (Blakemore et al. 1998b).
on this theme Spence (1996) suggested that the problem is This is because the sensory consequences of our move-
to do with the timing of awareness. Normally we are ments can be predicted. In the presence of delusions of
aware of initiating a movement ca. 80 ms before the move- control, modulation of sensory areas based on such
ment actually begins and, therefore well before any predictions fails, and the regions are overactive.
sensory feedback resulting from the movement (Libet et Although the patient is making an active movement, the
al. 1983). Spence suggested that, in the presence of brain activity and the associated experience resembles

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 Abnormalities in awareness and control of action C. D. Frith and others 1785

that seen with passive arm movements (Weiller et al. which motor control depends. We have devoted much
1996). attention to the abnormalities of control associated with
We have already discussed (? 2(c) (ii)) the evidence that various neurological and psychiatric disorders. Careful
the parietal cortex has a major role in the control of consideration of these abnormalities provides important
action which depends upon forming representations in evidence linking awareness of control to the underlying
many different coordinate systems (e.g. retinotopic, head components of the system. Indeed, we consider that these
centred, body centred, etc.). As yet, however, we have not abnormalities cannot be properly understood without
considered in any detail the nature and location of the taking into account the subjective experience of the
subset of these representations that are available to patients. As yet the physiological underpinnings of the
consciousness. Such consideration is crucial for under- motor control system are understood only in the broadest
standing abnormalities in the awareness of the motor terms. However, there is a rapidly increasing body of
system as observed in anosognosia and delusions of evidence from studies of patients with circumscribed
control. Frith (1995) andJeannerod (1999) theorized that lesions and from functional brain imaging studies to aid
representations suitable for awareness need to be in in generating a more detailed account. On the basis of
viewer-independent or 'third-person' coordinates, and not this evidence it is now possible to explore the brain
in the private, egocentric coordinates that a more suited systems concerned specifically with awareness of the
for the direct control of movement. Is there any evidence different aspects of the motor control system.
for segregation of these kinds of representation in parietal In this paper we have only considered relatively simple
cortex? We have already presented evidence that there is motor functions such as reaching and grasping or
a general lack of awareness of the details of motor learning sequences of movements. However, the control
commands and their fine-tuning by affordances as in system we have described, involving representations of
reaching and grasping. The IPS seems to have a major desired and predicted states and models for generating
role in this activity as revealed by single-cell neuro- these states, could apply equally well to much more
physiology, imaging studies and the effects of lesions. Of difficult problems. It is simple, in principle, to extend the
particular interest is the observation that optic ataxia, concept of internal models of the motor system to internal
which is caused by lesions to the IPS, is defined by models of the external world, of other people's mental
problems with reaching and grasping, but is not asso- processes, or of states of one's own mind. For example,
ciated with any disorder of awareness. In contrast, rather than changing the position of an arm, one might
imaging studies of motor preparation and motor imagery, wish to change someone else's belief about the world. Of
which emphasize awareness of motor representations, course, we have no direct knowledge of their belief, we
tend to activate the inferior parietal lobe (supramarginal have to estimate this just as we have to estimate the
gyrus, BA40; Stephan et al. 1995; Krams et al. 1998). current position of our own limbs. Given an estimate of a
Lesions in this region, particularly in the right hemi- person's current belief, a controller could used to compute
sphere, are associated with disorders of awareness such as the behaviour (or speech) we need to adopt in order to
neglect and anosognosia (Vallar & Perani 1986). This is produce the required change. A predictor could be run to
also the region that is overactive when patients with check whether this behaviour would indeed produce the
schizophrenia are experiencing delusions of control. desired change in the belief of the other person. Similar
Given that schizophrenic patients do not have funda- analysis could be applied to the control of many aspects
mental problems with the control of action it seems of the external world.
unlikely that the brain abnormality associated with
delusions of control is located in parietal cortex where the
This work was funded by the Wellcome Trust. We are grateful to
overactivity is observed. It is more likely that the damage
Richard Passingham, Patrick Haggard and Richard Frackowiak
involves the system that normally modulates activity at for their comments on earlier drafts of this paper.
this site. Fletcher et al. (1999), for example, provide
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