Brain (2000), 123, 860879

I NVI TED REVI EW

Limb apraxias
Higher-order disorders of sensorimotor integration
Ramon C. Leiguarda
1
and C. David Marsden
2

1
Raul Carrea Institute of Neurological Research, FLENI, Correspondence to: Ramon C. Leiguarda, Raul Carrea
Buenos Aires, Argentina,
2
University Department of Institute of Neurological Research, FLENI, Montaneses
Clinical Neurology, Institute of Neurology and National 2325, Buenos Aires (1428), Argentina
Hospital for Neurology and Neurosurgery, London, UK E-mail: rleiguar@eni.org.ar

Deceased
Summary
Limb apraxia comprises a wide spectrum of higher-order for the control of movements; somatosensory trans-
formation for posture; visual transformation for grasping; motor disorders that result from acquired brain disease
affecting the performance of skilled, learned movements. and internal representation of actions. Evidence from
anatomical and functional brain imaging studies suggests At present, limb apraxia is primarily classied by the
nature of the errors made by the patient and the pathways that the organization of the cortical motor system in
humans is based on the same principles. Imitation of through which these errors are elicited, based on a two-
system model for the organization of action: a conceptual postures and movements also seems to be subserved by
dedicated neural systems, according to the content of the system and a production system. Dysfunction of the
former would cause ideational (or conceptual) apraxia, gesture (meaningful versus meaningless) to be imitated.
Damage to these systems would produce different types whereas impairment of the latter would induce ideomotor
and limb-kinetic apraxia. Currently, it is possible to of ideomotor and limb-kinetic praxic decits depending
on the context in which the movement is performed and approach several types of limb apraxia within the
framework of our knowledge of the modular organization the cognitive demands of the action. On the other hand,
ideational (or conceptual) apraxia would reect an of the brain. Multiple parallel parietofrontal circuits,
devoted to specic sensorimotor transformations, have inability to select and use objects due to the disruption
of normal integration between systems subserving the been described in monkeys: visual and somatosensory
transformations for reaching; transformation of functional knowledge of actions and those involved in
object knowledge. information about the location of body parts necessary
Keywords: limb apraxia; object-oriented behaviour; parietofrontal circuits; sensorimotor integration
Abbreviations: AIP anterior intraparietal area; IPL inferior parietal lobule; MIP medial intraparietal area; PM
premotor cortex; SMA supplementary motor area; SPL superior parietal lobule; STS superior temporal sulcus
Introduction
Limb apraxia comprises a wide spectrum of higher-order motorsensory decit that could fully explain the abnormal
motor behaviour. This is not a negative approach, for praxic motor disorders that result from acquired brain disease
affecting the performance of skilled and/or learned errors are well dened clinically and kinematically and can
be superimposed on elementary motor disorders such as movements with the forelimbs, with or without preservation
of the ability to perform the same movement outside the weakness, rigidity, tremor, dystonia and ataxia (Heilman and
Rothi, 1985; Roy and Square, 1985; De Renzi, 1989; Poizner clinical setting in the appropriate situation or environment. An
impairment in gesturing cannot be termed apraxia, however, if et al., 1990, 1995).
De Renzi and co-workers (De Renzi et al., 1982) and it results from a language comprehension disorder or from
dementia, or if the patient suffers from any elementary Geschwind and Damasio (Geschwind and Damasio, 1985)
Oxford University Press 2000
Limb apraxia 861
emphasized the signicance of the stimulus by means of to multiple modications and is still under debate. Advances
in behavioural motor neurophysiology over recent decades which the learned movement is normally elicited: for the
overwhelming majority of clinical situations, one can use the have provided mounting evidence that focal inactivation of
functional nodes within distributed modular networks causes, following operational denition of apraxia: (i) failure to
produce the correct movement in response to a verbal in monkeys, highly selective motor and sensorimotor
abnormalities, such as grasping decits after injections of command, or (ii) failure to imitate correctly a movement
performed by the examiner, or (iii) failure to perform a muscimol in the anterior intraparietal area (AIP) (Gallese
et al., 1997). Lesion studies have demonstrated that a similar movement correctly in response to a seen object, or (iv)
failure to handle an object correctly (Geschwind and selective dysfunction may appear in humans (Binkofski et al.,
1998). Furthermore, functional neuroimaging studies have Damasio, 1985). Thus, at present, limb apraxia is basically
classied by both the nature of the errors made by the patient shown activation in normal subjects of nodes similar to those
making up the networks dened neurophysiologically in and the means by which these errors are elicited.
Skilful differs from unskilful motor behaviour because (i) monkeys, and interference over such functional areas with
transcranial magnetic stimulation produces effects similar to its performance is characterized by preprogrammed processes;
(ii) it is context-dependent; and (iii) individual differences those observed in inactivation and lesion studies (Fadiga
et al., 1995; Rizzolatti et al., 1996; Gerloff et al., 1997). increase with the degree of skill (Halsband and Freund, 1993;
Schlaug et al., 1994; Brooks et al., 1995). Therefore, we will discuss limb apraxia in this context in a
modest attempt to open new avenues for the future The learning of a skilful motor behaviour is initially subject
to conscious, cognitive, even verbal control, and such control understanding of these complex higher-order motor disorders.
diminishes progressively as a function of practice to give
way to automatic processes (Halsband and Freund, 1993).
The cerebral representation of learned motor skills would Development of concepts of limb apraxia
Contemporary ideas concerning apraxia stem from the change with extended practice and automatization and would
become independent from areas involved in the initial classical work of Liepmann (Liepmann, 1900, 1905, 1908,
1920). He posited that the idea of the action, or movement acquisition and performance of novel motor tasks (Roland,
1984; Brooks et al., 1995), as well as from the cerebral formulae, containing the spacetime form picture of the
movement were stored in the left parietal lobe. In order to commissures, allowing them to be controlled by either
hemisphere (Zaidel and Sperry, 1977). PET studies in humans carry out a skilled movement, the spacetime plan has to be
retrieved and associated via cortical connections with the have provided evidence for the non-unitary mechanism of
motor learning. During the early phases of learning, changes innervatory pattern stored in the left sensorimotorium (the
precentral and postcentral gyri and the pes of the superior, occur mainly in the parietal association cortex, premotor
cortex (PM) and primary motor and sensory cortices. middle and inferior frontal convolutions), which conveys the
information about the formulae to the left primary motor However, when an everyday skill has been well established
and overlearned, its execution becomes largely relegated to areas. When the left limb performs the movement, the
information has to be transmitted from the left to the right the supplementary motor area (SMA), primary sensory motor
cortex, basal ganglia and cerebellum (Roland, 1984; Seitz sensorimotorium through the corpus callosum to activate the
right motor cortex (Liepmann, 1905, 1908, 1920). Liepmann et al., 1990; Grafton et al., 1992; Passingham, 1997) without
the participation of higher-order parietal and frontal conceived ideational apraxia as a disruption of the space
time plan or its proper activation, so that it was impossible association cortices. Thus, it is apparent that at least two
cerebral systems can become operative to represent a motor to construct the idea of the movement. In contrast, in
ideomotor apraxia the spacetime plans are intact but can no plan depending on the level of practice and according to the
complexity of the cognitive demands placed on the brain longer guide the innervatory engrams which implement the
movements because they are disconnected from them; the (Grafton et al., 1995).
In this review we will rst briey describe the development patient knows what to do but not how to do it. Limb-kinetic
apraxia appears when the disruption of the innervatory of concepts of limb apraxia, the evaluation of limb praxis
and the interhemispheric differences in the control of praxic engrams interferes with the selection of the required muscle
synergies to perform the skilled movement (Liepmann, 1920). skills, and will then present the relevant clinical aspects of
apraxic syndromes as well as their possible anatomofunctional Ideomotor and limb-kinetic apraxia frequently coexist, and
were both considered by Liepmann to be motor apraxias substrates. We then depart from the currently more widely
accepted neuropsychological models to work out the different (Liepmann, 1920).
Geschwind followed Liepmanns interpretations and types of limb praxic decits within the framework of our
present knowledge concerning the distributed modular advanced a neuronal system for limb praxis similar to that
proposed by Wernicke for language processing (Wernicke, organization of the brain (Houk and Wise, 1995; Gallese
et al., 1997; Rizzolatti et al., 1998). 1874; Geschwind, 1965). The verbal command is rst
registered in Wernickes area. Information ows subsequently Since its original denition by Steinthal (Steinthal, 1871),
the classication of limb praxic disorders has been subject to the ipsilateral motor association cortex, probably via the
862 R. C. Leiguarda and C. D. Marsden
arcuate fasciculus. The right hand is controlled through the the body in the peripersonal space (e.g. carving a turkey) or
in body-centred space (e.g. brushing the teeth), or they may information going to the primary motor cortex, whereas
control of the left hand needs the information to be transmitted require the integration of actions in both spaces (e.g. the
actions involved in drinking). rst to the right motor association cortex via the corpus
callosum. Thereafter, Heilman and Rothi (Heilman and Rothi, Analysis of the performance of patients is based on both
accuracy and error patterns (Table 2). Patients with ideational 1985) and Rothi and colleagues (Rothi et al., 1991) proposed
that the movement formulae or visuokinaesthetic motor apraxia have difculty mainly in sequencing actions, whereas
patients with conceptual apraxia commit content errors: the engrams were stored in the left inferior parietal lobule (IPL),
and that they were translated into an innervatory pattern in movement itself is performed well but the target of the action
is wrong or the patient performs the movement without the the SMArather than in the convexity of the PM, as Geschwind
had previously proposed (Geschwind, 1965). benet of a tool. Ideomotor apraxia patients show primarily
temporal and spatial errors, which are more evident when In 1985, Roy and Square advanced a model for the
organization of action based on the operation of a two-part they are performing transitive gestures. Errors in limb-kinetic
apraxia represent slowness, coarseness and fragmentation, system involving both conceptual and production components
(Roy and Square, 1985). The conceptual systeminvolves three particularly of manipulative movements; the decit affects
simple and complex nger and hand movements, regardless types of knowledge relevant to limb praxis: (i) knowledge of
objects and tools in terms of the actions and functions they of whether they involve the use of an object.
Three-dimensional motion analysis of the spatiotemporal serve; (ii) knowledge of actions independent of tools or
objects but in which the use of tools and objects may be characteristics of gestural movements has provided an
accurate method to capture objectively the nature of the incorporated; and (iii) knowledge relevant to the organization
of single actions in a sequence. On the other hand, the praxis errors observed in clinical examination (Poizner et al.,
1990, 1995; Clark et al., 1994). Patients with ideomotor production system incorporates a sensory motor component
of knowledge, as well as encompassing the perceptual motor apraxia, resulting from focal left hemisphere lesions (Poizner
et al., 1990, 1995; Clark et al., 1994), or different processes for organizing and executing action. According to
this model, dysfunction of the praxis conceptual system asymmetrical cortical degenerative syndromes (Rapcsak
et al., 1995; Leiguarda and Starkstein, 1998), have shown would give rise to conceptual or ideational apraxia, whereas
impairment of the praxis production system would induce slow and hesitant build-up of hand velocity, irregular and
non-sinusoidal velocity proles, abnormal amplitudes, ideomotor apraxia.
alterations of the plane of motion and of the direction and
shapes of wrist trajectories, decoupling of hand speed and
trajectory curvature, and loss of interjoint co-ordination. All Evaluation of limb praxis
A systematic evaluation of limb praxis is critical in order (i) these studies have evaluated gestures, such as carving a
turkey or slicing a loaf of bread, which mainly involve the to identify the presence of apraxia; (ii) to classify correctly
the nature of the limb praxis decit according to the errors transport or reaching phase of the movement. However, the
majority of transitive gestures included in most apraxia committed by the patient; and (iii) to gain insight into
the underlying mechanism of the patients abnormal motor batteries are prehension (reaching and grasping) movements,
which reect proximal (transport) and distal limb control behaviour, which may be further dened by kinematic analysis
(Table 1). (grasping) as well as the coupling of transport and grasping
components. Several types of transitive movements are used in the
evaluation of praxis, and it is not an uncommon nding that The analysis of prehension movements provides further
insight into the specic neural mechanisms underlying distinct apraxic patients perform some but not all movements in a
particularly abnormal fashion and/or that individual types of limb praxic disorders. Although few, the studies that
have been designed to explore these components of the action differences appear in some but not all components of a given
movement. Therefore, the dissimilar complexity and features system in patients with apraxia have provided consistent
results. Charlton and colleagues evaluated an apraxic patient of transitive movements should be considered if praxic errors
are to be analysed and interpreted accurately. For instance, and demonstrated that the co-ordination of the transport
and grasp component and the grasp component itself were (i) movements may or may not be repetitive in nature (e.g.
hammering versus using a bottle-opener to remove the cap markedly abnormal (Charlton et al., 1988). Caselli and
colleagues and Leiguarda and colleagues studied patients of a bottle); (ii) an action may be composed of sequential
movements (e.g. reaching for a glass and taking it to the lips with progressive apraxia resulting from corticobasal
degeneration and Alzheimers disease (Caselli et al., 1999; when drinking); (iii) a movement may primarily reect
proximal limb control (transport) (as in transporting the wrist Leiguarda et al., 2000). Compared with controls, apraxic
patients show disruption of both the transport and grasp when carving a turkey), proximal and distal limb control (as
in reaching and grasping a glass of water) or primarily distal phases of the movements as well as the uncoupling of
transport from grasping. Furthermore, manipulating nger control (as when the patient is asked to manipulate a pair of
scissors); and (iv) movements may be performed away from movements during exploration of an object has revealed
Limb apraxia 863
Table 1 Assessment of limb praxis
1. Evaluation of the praxis production system
Intransitive movements Non-representational (e.g. touch your nose, wriggle your ngers).
Representational (e.g. wave good-bye, hitch-hike).
Transitive movements (E.g. use a hammer, use a screwdriver) under verbal, visual and tactile
modalities.
Imitation of meaningful and meaningless movements, postures and sequences.
2. Evaluation of the praxis conceptual system
Multiple step tasks (E.g. prepare a letter for mailing).
Tool* selection tasks To select the appropriate tool to complete a task, such as a hammer for a
partially driven nail.
Alternative tool selection To select an alternative tool such as pliers to complete a task such as
tasks pounding a nail, when the appropriate tool (e.g. hammer) is not available.
Gesture recognition tasks To assess the capacity to comprehend gestures either verbally (to name
gestures performed by the examiner) as well as non-verbally (to match a
gesture performed by the examiner with cards depicting the tool or
object

corresponding to the pantomime).

Source: De Renzi, 1989; Rothi and Heilman, 1997. *Tool: implement with which an action is
performed (e.g. hammer, screwdriver);

object: the recipient of the action (e.g. nail, screw).
abnormal workspace and breakdown of the temporal proles control purposeful skilled movements of the limbs on both
of the scanning movements in patients with limb-kinetic sides of the body (Liepmann, 1905), every subsequent study
apraxia (Leiguarda et al., 2000). Thus, exploration of the on limb apraxia has conrmed the dominance of the left
kinematics of reaching, grasping and manipulating not only hemispheric in praxis (Basso et al., 1980; De Renzi et al.,
provides information regarding the specic neural subsystems 1980, 1982; Kertesz and Ferro, 1984). However, apraxia, as
involved in patients with different types of praxic disorders
tested by the imitation of gestures and object use pantomime,
of the limbs, but may also help in the further understanding
has been found in ~50% of patients with left hemisphere
of how these systems are integrated with those involved in
damage and in 10% of those with right hemisphere damage,
the representations of objects.
which means that in many subjects praxic functions have
Patients with apraxia exhibit several types of sequential
bilateral representations (De Renzi, 1989).
errors, such as deletions, transpositions, additions,
Liepmann himself was cautious enough to point out that
perseverations and unrelated types of substitutions (Roy and
the right hemisphere may also possess some praxic skills,
Square, 1985; Rothi and Heilman, 1997). Abnormalities in
especially for the left half of the body (Liepmann, 1920).
sequencing movements have been reported more commonly in
Since then, the possibility that in right-handers the right
patients with parietal, frontal and basal ganglion involvement
hemisphere may have some capacity to control complex
(Kimura and Archibald, 1974; Luria, 1980; Kolb and Milner,
skilled movements has also been posited by several authors
1981; De Renzi et al., 1983; Benecke et al., 1987; Harrington
as a likely explanation for the sparing of certain left-hand
and Haaland, 1992; Halsband et al., 1993). Luria emphasized
praxic functions after callosal or left hemisphere lesions
the role of the frontal lobes in controlling actions requiring
(Geschwind and Kaplan, 1962; Zaidel and Sperry, 1977;
the sequencing of different movements over time (Luria,
Kertesz and Ferro, 1984; Graff-Radford et al., 1987). Most
1980). Kolb and Milner studied meaningless movement
of the errors exhibited by ideomotor apraxia patients are seen
sequences in a group of epileptic patients with cortical
equally in left and right hemisphere-damaged patients when
ablations, and found that those with left parietal lesions were
they pantomime non-representative and representative/
more impaired than those with right or left frontal lesions
intransitive gestures, but are observed predominantly for
(Kolb and Milner, 1981). Similar results were found by
left hemisphere-damaged patients when they pantomime
Kimura and by De Renzi and colleagues using a multiple
transitive movements, because it is this action which is
hand movement task and the imitation of three unrelated
carried on outside the natural context (Haaland and Flaherty,
movements carried out in a sequence (Kimura, 1982; De
1984). Schnider and colleagues also emphasized that the
Renzi et al., 1983). Patients with frontal or parietal lesions
motor dominance of the left hemisphere reected by
had decits in sequencing movements, but the impairment
ideomotor apraxia refers to spatially and temporally complex
in those with frontal damage became evident only with more
movements performed in an articial context (Schnider et al.,
complex sequences (Kimura, 1982).
1997). Moreover, Rapcsak and colleagues have suggested
that the left hemisphere is dominant not only for the abstract
Interhemispheric differences in the control of
performance (pantomiming to verbal command) of transitive
movements but also for the imitation of meaningless praxic skills
movements (Rapcsak et al., 1993). Since Liepmann postulated that the left hemisphere of right-
handed subjects contains the movement formulae that The left hemisphere also seems to be dominant for
864 R. C. Leiguarda and C. D. Marsden
Table 2 Types of praxis error
I. Temporal
S Sequencing: some pantomimes require multiple positionings that are performed in a
characteristic sequence. Sequencing errors involve any perturbation of this sequence including
addition, deletion or transposition of movement elements as long as the overall movement
structure remains recognizable.
T Timing: this error reects any alterations from the typical timing or speed of a pantomime and
may include abnormally increased, decreased, or irregular rate of production or searching or
groping behaviour.
O Occurrence: pantomimes may involve either single (i.e. unlocking a door with a key) or
repetitive (i.e. screwing in a screw with a screwdriver) movement cycles. This error type reects
any multiplication of single cycles or reduction of a repetitive cycle to a single event.
II. Spatial
A Amplitude: any amplication, reduction, or irregularity of the characteristic amplitude of a target
pantomime.
IC Internal conguration: when pantomiming, the ngers and hand must be in specic spatial
relation to one another to reect recognition and respect for the imagined tool. This error type
reects any abnormality of the required nger/hand posture and its relationship to the target tool.
For example, when asked to pretend to brush the teeth, the subjects hand may close tightly into
a st with no space allowed for the imagined toothbrush handle.
BPO Body-part-as-object: the subject uses his/her nger, hand or arm as the imagined tool of the
pantomime. For example, when asked to smoke a cigarette, the subject might puff on his or her
index nger.
ECO External conguration orientation: when pantomiming, the ngers/hand/arm and the imagined
tool must be in a specic relationship to the object receiving the action. Errors of this type
involve difculty orienting to the object or in placing the object in space. For example, the
subject might pantomime brushing the teeth by holding their hand next to their mouth without
reecting the distance necessary to accommodate an imagined toothbrush. Another example
would be when asked to hammer a nailthe subject might hammer in differing locations in
space, reecting difculty in placing the imagined nail in a stable orientation or in a proper
plane of motion (abnormal planar orientation of the movement).
M Movement: when acting on an object with a tool, a movement characteristic of the action and
necessary to accomplish the goal is required. Any disturbance of the characteristic movement
reects a movement error. For example, when asked to pantomime using a screwdriver, a subject
may orient the imagined screwdriver correctly with respect to the imagined screw, but instead of
stabilizing the shoulder and wrist and twisting at the elbow the subject stabilizes the elbow and
twists at the wrist or shoulder.
III. Content
P Perseverative: the subject produces a response that includes all or part of a previously produced
pantomime.
R Related: the pantomime is an accurately produced pantomime associated in content with the
target. For example, the subject might pantomime playing a trombone for a target of a bugle.
N Non-related: the pantomime is an accurately produced pantomime not associated in content with
the target. For example, the subject might pantomime playing a trombone for a target of shaving.
H The patient performs the action without a real or imagined tool. For example, when asked to cut
a piece of paper with scissors, he or she pretends to rip the paper.
IV. Other
C Concretization: the patient performs a transitive pantomime not on an imagined object but
instead on a real object not normally used in the task. For example, when asked to pantomime
sawing wood, the patient pantomimes sawing on his or her leg.
NR No response.
UR Unrecognizable response: the response shares no temporal or spatial features of the target.
Source: Rothi and Heilman, 1997.
movement sequencing. Several clinical studies have shown movement from memory (Harrington and Haaland, 1992).
Rushworth and colleagues have further proposed that the that impairment in sequencing is particularly apparent for
left hemisphere-damaged patients when the tasks place left hemisphere is not only dominant in learning to select
movements in a sequence but also in learning to select a demands on memory (Jason, 1983; Roy and Square, 1994).
However, when the temporal aspects of sequencing, reecting limb movement that is appropriate for the use of an object
(Rushworth et al., 1998). These learning processes would response preparation and programming, are considered, left
hemisphere-damaged patients exhibit decits in movement depend on different but adjacent response selection systems,
both lateralized to the left hemisphere. The system composed sequencing even though they are not required to select the
Limb apraxia 865
of the lateral premotor and parietal cortex, basal ganglia, The terminology applied to behavioural disturbances
arising from the disruption of the conceptual system for thalamus and white matter fascicles would participate in the
selection of limb movement responses, whereas an adjacent praxis has been confusing. Pick coined the term ideational
apraxia to denote the inability to carry out a series of acts systemintegrated by lateral area 8 and possibly interconnected
parietal regions, thalamus, striatum and white matter fascicles involving the utilization of several objects (e.g. preparing a
letter for mailing), although his rst case also showed would be concerned with the selection of object-oriented
responses (Rushworth et al., 1998). The process of motor impairment in the use of single objects (Pick, 1905). As we
have already seen, Liepmann, as well as De Ajuriaguerra attention has also been lateralized to the left hemisphere, so
left hemisphere-damaged patients would exhibit abnorm- and colleagues, Hecaen and Poeck, advanced a similar
concept and attributed it to damage to the left parieto- alities in the sequencing of movements due to inability to
shift the focus of motor attention from one movement in the occipital or temporoparietal regions (Liepmann, 1920; De
Ajuriaguerra et al., 1960; Hecaen, 1972; Poeck, 1983). sequence to the next (Rushworth et al., 1997b).
In conclusion, it seems quite likely that the interhemispheric However, other authors use the term to denote failure to use
single tools appropriately. Denny-Brown considered differences in the control of praxic skills depend largely on
the context in which the movement is performed and on the ideational apraxia as an agnosia for object use (Denny-
Brown, 1958), and De Renzi and co-workers interpreted it cognitive requirements of the task: that is, when a single
movement and/or a sequence of object-oriented movements as an inability to remember the general conguration of the
action when attempting to use a tool (De Renzi, 1989). are performed outside the usual context and depend on higher-
level cognitive abilities for planning and self-monitoring the To overcome this confusion, Ochipa and colleagues have
suggested restricting the term ideational apraxia to the action, the left hemisphere emerges as the dominant one
(Kimura and Archibald, 1974; Kimura, 1982; Haaland and failure to sequence correctly a series of acts leading to an
action goal, and introducing the term conceptual apraxia to Harrington, 1996; Rushworth et al., 1997b, 1998).
denote precisely the loss of different types of toolaction
knowledge (Ochipa et al., 1992).
Ideational apraxia in its pure form is an unusual disorder,
Types of limb apraxia
although the presence of associated aphasia in many patients
probably masks this type of praxic decit. Ideational apraxia Ideational or conceptual apraxia
Patients with impairment of the conceptual system exhibit is characterized by impairment in carrying out sequences of
actions requiring the use of various objects in the correct primarily content errors in the performance of transitive
movements (e.g. the patient pantomimes shaving for a target order so as to achieve an intended purpose. They recognize
single objects well and name them correctly, but they may of toothbrushing or uses the toothbrush as if it were a shaver),
because they are unable to associate tools and objects with be unable to recognize correct and incorrect sequences of
actions represented in photographs (Poeck, 1983). the corresponding action. They may also lose the ability to
associate tools with the objects that receive their action; thus, Although Poeck and Lehmkuhl maintained that patients
with ideational apraxia quite often are able to correctly when a partially driven nail is shown, the patient may select
a pair of scissors rather than a hammer from an array of manipulate single objects (Poeck and Lehmkuhl, 1980),
when these patients were systematically investigated they tools to perform the action. Not only are patients unable to
select the appropriate tool to complete an action, but they were also found to be impaired in demonstrating the use of
single objects (De Renzi, 1989). De Renzi and Lucchelli may also fail to describe the function of a tool or point to a
tool when the function is described by the examiner, even tested 20 left brain-damaged patients with a single object
and with a multiple-object test, and found that performance when the patient names the tool properly when it is shown to
him/her. Patients with conceptual apraxia lose the mechanical in the two tests was strongly correlated. Omission (the patient
neglects to spread the paste on a toothbrush), misuse (the advantage afforded by tools (mechanical knowledge). For
example, when asked to complete an action and the patient uses a key as a hammer) and mislocation (the patient
holds a pen upside down) were the most frequent errors (De appropriate tool is not available (e.g. a hammer to drive a
nail), they may not select the most suitable tool for that Renzi and Lucchelli, 1988). These errors were observed
whether the test involved a single object or multiple objects. action (e.g. a spanner) but rather one which is inadequate
(e.g. a screwdriver) (Ochipa et al., 1992; Heilman et al., Thus, it appears that strict differentiation between ideational
and conceptual apraxia, as Ochipa and colleagues have 1997). These patients may also be impaired in the sequencing
of tool/object use (Pick, 1905; Liepmann, 1920; Poeck, 1983). proposed (Ochipa et al., 1992), may not be possible in every
patient, because in many cases object use is impaired even Patients with ideational or conceptual apraxia are disabled
in everyday life, because they use tools/objects improperly, outside the context of sequence.
Heilman and colleagues evaluated patients with focal they misselect tools/objects for an intended activity, perform
a complex sequential activity (e.g. make espresso coffee) in hemisphere lesions for decits in the conceptual praxis system
(Heilman et al., 1997). The main conclusions of their study a mistaken order or do not complete the task at all (Foundas
et al., 1995). were as follows: (i) in some patients, dissociation was
866 R. C. Leiguarda and C. D. Marsden
observed between tests assessing different types of tool abnormalities) and spatial errors (i.e. abnormal amplitude,
action knowledge, which suggests the possible existence of improper spatial orientation of objects and movements,
subtypes of conceptual apraxia; (ii) dissociation between abnormal hand and limb conguration, use of body parts as
conceptual apraxia and ideomotor apraxia was found, objects) (Table 2). The movements are incorrectly produced
suggesting independent systems for praxis knowledge and but the goal of the action can usually be recognized.
praxis production, although the two systems appeared to be Occasionally, however, the performance is so severely
closely related because both types of apraxia frequently
deranged that the examiner cannot recognize the movement.
coexisted; (iii) most patients with conceptual apraxia had
Transitive movements are more affected than intransitive
damage in the left hemisphere; and (iv) among patients with
ones on pantomiming to commands. Acting with tools/objects
left hemisphere damage, only about half exhibited ideomotor
is carried out better than pantomiming their use, but in most
apraxia and conceptual apraxia. Although there were no
instances movements are not normal. Patients with ideomotor
specic anatomical areas in the left hemisphere that were
apraxia usually improve on imitation when performance is
damaged in the group with apraxia and spared in the non-
compared with responses to verbal commands, although some
apraxic group, the parietal and frontal association areas,
patients may nd similar difculties in the two types of
together or separately and with or without subcortical
task (Heilman and Rothi, 1985; De Renzi, 1989). The
involvement, were affected in most patients (Heilman et al.,
improvement in performance observed when the patient
1997). Similar ndings were described by De Renzi and
actually uses the tool/object might result from the advantage
Luchelli: parietal, temporal and parietotemporal lesions were
provided by visual and tactilekinaesthetic cues emanating
found in 10 of their patients, frontal lesions in six and
from the tool/object and/or by the fact that in this condition
frontotemporal, parietofrontal, basal ganglion and occipital
the patient is performing the movement in a more natural
lesions in one patient each (De Renzi and Luchelli, 1988).
context and is therefore less dependent on the left hemisphere.
It is still unclear what kind of knowledge about an object
The tactile kinaesthetic information provided by holding the
is necessary for its use (Roy and Square, 1985; Ochipa et al.,
tool/object may not only help to establish the postural context
1992; Buxbaum et al., 1997; Goldenberg and Hagmann,
but also facilitate a correct hand position for the gesture
1998; Moreaud et al., 1998). Object recognition seems to be
(Frank and Earl, 1990).
subserved mainly by a viewpoint-independent mechanism
Since the rst formal report of apraxia by Liepmann
which relies on the occipitotemporal system (or ventral
(Liepmann, 1900), it has been widely accepted that apraxic
stream) but is complemented by a viewpoint-dependent
patients show a voluntaryautomatic dissociation, which
mechanism which relies on the occipitoparietal system (or
means that the patient does not complain about the decit
dorsal stream). A third system, centred on the IPL, would
and that the execution of the movement in the natural context
be additionally involved in the binding of information from
is relatively well preserved; the decit appears mainly in the
the two visual systems (for review, see Turnbull et al., 1997).
clinical setting when the patient has to represent explicitly
The study by Faillenot and colleagues, which showed that
the content of the action outside the situational props.
the dorsal stream participates in object perception whenever
However, recent studies have demonstrated that even patients
it is required for object-oriented action (Faillenot et al.,
with ideomotor apraxia may manifest decits when interacting
1997), supports this notion. Moreover, it has also been
with their everyday environment (for review, see Cubelli and
proposed that the left dorsolateral frontal cortex subserves the
Della Sala, 1996).
interaction between object/tool manipulation and functional
Unilateral lesions of the left hemisphere in right-handed
knowledge, since this region becomes activated in a task
patients produce bilateral decits, usually less severe in the
involving the recognition of man-made tools (Perani et al.,
left than in the right limb (Liepmann, 1920; Heilman and
1995).
Rothi, 1985; De Renzi, 1989). Ideomotor apraxia is commonly
Thus, it might be posited that the use and selection of
associated with damage to the parietal association areas, less
objects/tools depends on the integration of systems involved
frequently with lesions of the PM and SMA, and usually
in the functional knowledge of actions (i.e. reaching, grasping,
with disruption of the intrahemispheric white matter bundles
manipulating, sequencing) with those devoted to the
which interconnect them, as well as with basal ganglion and
knowledge of objects and tools. Disruption of these complex
thalamic damage.
integration processes may lead to different types of ideational
Liepmanns original postulate about the crucial role played
or conceptual praxic decits.
by the dominant parietal lobe in the genesis of apraxia
(Liepmann, 1900) has been largely conrmed by subsequent
studies (Morlaas, 1928; De Ajuriaguerra et al., 1960; Kolb
Ideomotor apraxia
and Milner, 1981; De Renzi et al., 1983; Faglioni and Basso, Ideomotor apraxia has been thought to reect a disturbance
1985). Lesions centred in the supramarginal gyrus, the in programming the timing, sequencing and spatial
superior parietal lobe and the underlying white matter would organization of gestural movements (Rothi et al., 1991). As
cause ideomotor apraxia through damage of the parietal described above, patients with ideomotor apraxia exhibit
mainly temporal (i.e. irregular speed, sequencing associative areas or by interrupting pathways connecting
Limb apraxia 867
these areas with the premotor cortex (Liepmann, 1908; association of apraxia with large corticosubcortical lesions
in the suprasylvian, perirolandic region of the left dominant Geschwind, 1965; Heilman and Rothi, 1985).
After the parietal lobes, the PM and the SMA are the hemisphere (Kertesz and Ferro, 1984; Alexander et al., 1992;
Schnider et al., 1997), but no specic lesion site which regions that play the most important role in praxis (Liepmann,
1905; Morlaas, 1928; Kleist, 1931; De Ajuriaguerra et al., correlated with apraxia. Smaller apraxia-producing lesions
have been reported to be located in the parietal lobe (Faglioni 1960; Geschwind, 1965; Hecaen, 1972). Surprisingly,
however, only a few well-documented cases of ideomotor and Basso, 1985), the deep central paraventricular region
(Kertesz and Ferro, 1984), the deep anterior two-thirds of apraxia with PM (Faglioni and Basso, 1985; Raymer et al.,
1999) and SMA lesions (Watson et al., 1986; Marchetti and the paraventricular white matter (Alexander et al., 1992),
and even the basal ganglia and thalamus (Pramstaller and Della Sala, 1997) have been described. Two possible reasons
for the paucity of reports are as follows: (i) most premotor Marsden, 1996).
Papagno and colleagues found 10 apraxic non-aphasic and lesions have also involved the primary motor cortex, causing
a contralateral paresis or paralysis; therefore, if a detailed 129 aphasic, but not apraxic, patients among a cohort of 699
patients with vascular lesions in the left hemisphere (Papagno and properly oriented clinical evaluation were not carried
out, the mild or subtle spatial and temporal errors that the et al., 1993). Seven of the apraxic non-aphasic patients had
subcortical lesions (in the frontal and parietal white matter patient may have committed when performing with the non-
dominant limb would not have been captured; and (ii) a in six patients and the caudate nucleus in one), whereas in
the other three the lesion also encroached upon the cortex; defect caused by a unilateral dominant premotor lesion may
be compensated for largely by the contralateral hemisphere, these latter cases had more severe ideomotor apraxia. On the
other hand, most of the aphasic non-apraxic patients had because of the close interaction between the two frontal
lobes during the performance of a unilateral movement, as predominantly pure cortical lesions. These ndings further
support the role of white matter damage and the interruption demonstrated by functional studies (Roland and Zilles, 1996).
Heilman and colleagues and Rothi and colleagues studied of corticocortical and corticosubcortical connections in the
causation of apraxia. patients with ideomotor apraxia resulting from anterior and
posterior lesions on the left hemisphere, and found that
only those patients with a damaged parietal lobe displayed
impairment in the recognition of gestures (Heilman et al., Callosal apraxia
Patients with naturally occurring or surgically caused callosal 1982; Rothi et al., 1985). Therefore, the authors suggested
the existence of posterior and anterior forms of ideomotor lesions involving the genu and body (Liepmann and Maas,
1907; Sweet, 1941; Watson and Heilman, 1983; Graff- apraxia, with and without gesture-recognition disturbances,
respectively. However, most of the studies designed to Radford et al., 1987; Leiguarda et al., 1989) or only the
body of the corpus callosum (Kazui and Sawada, 1993) may correlate action-recognition decits with lesion location have
revealed the involvement of many structures other than the develop unilateral apraxia of the non-dominant limb whose
characteristics vary according to the type of test given and parietal lobe, including the frontal and temporal lobes, and
even the basal ganglia (Ferro et al., 1983; Rothi et al., 1985, the lateralization pattern of praxic skills in each patient.
Some patients could not correctly pantomime to verbal 1986; Varney and Damasio, 1987; Wang and Goodglass,
1992). commands with their left hand but performed normally on
imitation and object use (Geschwind and Kaplan, 1962; Recently, the basal ganglia and thalamus have also been
included in the modular neural network which mediates Gazzaniga et al., 1967; Zaidel and Sperry, 1977), whereas
others could not use their left hand on command, by imitation praxis (Sharpe et al., 1983; Goldenberg et al., 1986; Della
Sala et al., 1992; Pramstaller and Marsden, 1996; Leiguarda or while holding the object (Liepmann and Maas, 1907;
Watson and Heilman, 1983; Leiguarda et al., 1989; Kazui et al., 1997). Pramstaller and Marsden reviewed 82 cases of
deep or subcortical apraxia and found that (i) most of the and Sawada, 1993). Moreover, a few patients could not
pantomime to verbal commands and while holding the object patients had lesions on the left hemisphere; (ii) small isolated
lesions of the putamen and thalamus or lesions restricted to but performed fairly well on imitation (Graff-Radford et al.,
1987) or improved over time on imitation and object use the lenticular nucleus, with or without caudate or thalamic
involvement, were uncommon; (iii) the majority of patients (Watson and Heilman, 1983). Thus, the most enduring callosal
type of praxic defect is demonstrated when verbalmotor sustained larger lesions with damage to the basal ganglia
and/or thalamus together with the internal capsule and tasks, such as pantomiming to command, are used (Graff-
Radford et al., 1987). periventricular and peristriatal white matter, interrupting
association bres, in particular those of the superior
longitudinal fasciculus and frontostriatal connections; and
(iv) ideomotor apraxia was present in most patients, orofacial Modality-specic or disassociation apraxias
The modality-specic (De Renzi et al., 1982) or disassociation apraxia was less common and ideational apraxia was rare.
Most studies exploring a possible clinicalanatomical (Rothi and Heilman, 1997) apraxias are those types of praxic
decits exhibited by patients who commit errors only, or correlation for ideomotor apraxia have found a strong
868 R. C. Leiguarda and C. D. Marsden
predominantly, when the movement is evoked by one but the motion becomes amorphous (Liepmann, 1908). Fruitless
attempts usually precede wrong movements, which in turn not all modalities. Thus, the impairment of patients who
are frequently contaminated by extraneous movements. performed abnormally only under verbal commands was
Imitation of nger postures is also abnormal and some attributed to a left hemisphere lesion most likely affecting
patients use the less affected or normal hand to reproduce
the audio-verbal inputs to the parietal lobe (Heilman, 1973;
the posture requested. The severity of the decit is consistent,
De Renzi et al., 1982) or to a callosal lesion (Geschwind
exhibiting the same degree in everyday activities as in
and Kaplan, 1962; Gazzaniga et al., 1967). Patients who
the clinical setting; thus, there is no voluntaryautomatic
performed poorly to seen objects but were able to pantomime
dissociation (Kleist, 1907, 1931; Liepmann, 1908; Faglioni
gestures normally to verbal command have been reported as
and Basso, 1985; Denes et al., 1998).
having lesions interrupting the ow of visual information
Most authors have dismissed limb-kinetic apraxia as merely
towards the parietal lobe (Assal and Regli, 1980; De Renzi
the expression of basic motor (pyramidal) decits
et al., 1982; Pena-Casanova et al., 1985; Pilgrim and
(Geschwind, 1965; Heilman and Rothi, 1985; De Renzi,
Humphreys, 1991). On occasion, praxic decits may be
1989). However, Luria (Luria, 1980) and Freund (Freund,
conned to the tactile modality (Renzi et al., 1982). Finally,
1992) both recognized the category and, following Kleist
patients have been reported who, unlike those with ideomotor
(Kleist, 1931), attributed it to damage to the PM cortex. We
apraxia improving on imitation, were more impaired when
also agree that limb-kinetic apraxia is a higher-order motor
imitating than when pantomiming to command (Ochipa et al.,
disorder over and above a corticospinal or basal ganglion
1994), or could not imitate but performed awlessly under
decit, which would mainly result from frontal lobe damage
other modalities (Mehler, 1987; Goldenberg and Hagmann,
centred on the PM cortex, most likely associated with parietal
1997; Merians et al., 1997). The decits may be restricted
and/or basal ganglion involvement.
solely to the imitation of meaningless gestures with preserved
Limb-kinetic apraxia is an uncommon type of praxic decit
imitation of meaningful gestures. Furthermore, patients may
which has been scantily reported with focal lesions (Faglioni
show abnormal imitation of hand postures but with normal
and Basso, 1985). We believe there are basically two possible
imitation of nger conguration (Goldenberg and Hagmann,
explanations. First, most PM lesions also involve the
1997). The anatomical correlates of imitation decits have
precentral cortex, and, therefore, the contralateral paresis or
not been studied specically, although abnormal performance
paralysis precludes the expression of the praxic decit.
on imitation was found in patients with parietal, frontal,
Secondly, bilateral activation of the PM cortex and SMA is
temporal, subcortical or basal ganglion lesions (Hermsdorfer
often observed with unilateral movements (Roland and Zilles,
et al., 1996).
1996); thus, a unilateral lesion would not be enough for
the decit to become clearly manifested, since bilateral
involvement would most likely be necessary. As a matter of
Limb-kinetic apraxia
fact, all recently pathologically conrmed cases of limb-
Limb-kinetic apraxia is a controversial type of praxis disorder
kinetic apraxia have shown a degenerative process such as
which has been largely neglected. Recently, however, renewed
corticobasal degeneration and Picks disease, involving the
interest has arisen mainly from the study of patients with
frontal and parietal cortices (Fukui et al., 1996) or,
corticobasal degeneration and the syndrome of primary predominantly, the PM cortex (Tsuchiya et al., 1997).
progressive apraxia (Okuda et al., 1992; Fukui et al., 1996;
Tsuchiya et al., 1997; Denes et al., 1998).
The anatomofunctional substrates of limb
This type of apraxia was originally described by Kleist,
praxis
who called it innervatory apraxia to stress the loss of hand
The fact that most studies exploring possible clinical
and nger dexterity resulting from inability to connect and
anatomical correlations for different types of limb apraxia
to isolate individual innervation: the patient is unable to
have failed to unveil a consistent and specic lesion site for
manipulate scissors and shows a complete failure when trying
the disorder strongly suggests that praxic functions are
to knot a thread, . . . the decit being proportional to the
distributed across several distinct anatomofunctional neural
innervatory complexity, the greater the innervatory
systems working in concert, but each one controlling specic
complexity of hand functions, the greater the disorder
processes (i.e. parietofrontal systems and reaching/grasping,
(Kleist, 1907).
frontostriatal system and sequential motor events). Damage
The decit is conned mainly to nger and hand
to these systems would produce selective praxic-related
movements contralateral to the lesion, regardless of its
decits depending on the context of the movement and the
hemispheric side, with preservation of power and sensation.
cognitive demand of the action.
Manipulatory nger movements are affected predominantly,
but in most cases all movements, either complex or routine,
Parallel parietofrontal circuits for sensorimotor independently of the modality that evokes them, are coarse
and mutilated. The virtuosity given to movements by practice integration
is lost and they become clumsy, awkward and rough: for Recent anatomical and functional studies have identied in
primates a series of segregated parietofrontal circuits, working many motions, the starting point cannot even be found, or
Limb apraxia 869
in parallel and each one involved in a specic sensorimotor Moreover, it has been proposed that neurons in F7 also
contribute to the spatial localization of external stimuli for transformation process: that is, their function is to transform
the sensory information encoded in the coordinates of the reaching movements (Rizzolatti et al., 1998).
The SMA proper (F
3
), as part of one of the SPfrontal sensory epithelia (e.g. retina, skin) into information for
movements (Rizzolatti et al., 1998). The transformation circuits, appears to play an important role in the control of
posture, in particular in the postural adjustments that precede process involves parallel mechanisms that simultaneously
engage functionally related parietal and frontal areas linked voluntary movements. The pre-SMA (F
6
) receives substantial
projections from the prefrontal lobe, suggesting that it is by reciprocal corticocortical connections, supplemented by
additional local computations (Wise et al., 1997; Rizzolatti involved in the control of potential actions encoded in the
parietofrontal circuits. Its degree of activity would depend et al., 1998). The posterior parietal cortex comprises a
multiplicity of areas, each involved in the analysis of on external contingencies and motivational factors (Rizzolatti
et al., 1998). particular aspects of sensory information (i.e. somatosensory,
visual, auditory, vestibular). The coordinate system may vary The skilful handling of objects requires the use of visual
information to encode the intrinsic properties of the object in different parts of the parietal cortex according to the nature
of the actions evoked by sensory input (Kalaska et al., 1997). (size and shape) and to produce appropriate patterns of
hand and nger movements. This visuomotor transformation The motor cortex, in turn, is also made up of many areas,
each containing an independent representation of body process takes place in a circuit made up by the IPL and the
PM ventral cortex (PMv), as well as by their interconnection movement and playing a specic role in motor control
according to its afferent and efferent connections. The with the basal ganglia and cerebellum. This circuit may be
considered as a lateral subsystem devoted to grasping and proposed functions of the main circuits originating from the
superior parietal lobule (SPL) include visual and hand manipulation, parallel to the medial subsystem involved
in the transport phase of reaching (Jeannerod et al., 1995). somatosensory transformation for reaching (medial
intraparietal area, MIP-F
2
), somatosensory transformation for Recent neurophysiological studies in monkeys have
disclosed several classes of neurons involved in hand actions reaching (PEc/PEip-F
2
), somatosensory transformation for
posture (PEci-F
3
) and transformation of body part location located in the IPL. Some neurons were activated by the
sight of objects during xation, representing perception of data into information necessary for the control of body part
movements (PE-F
1
). The circuits originating in the IPL are egocentric distance to the visual target, while others showed
precise correspondence between the pattern of hand devoted to visuomotor transformation for grasping (AIP-
F
5
), the internal representation of actions (PF-F
5
), coding movements and the spatial characteristics of the object to
be manipulated. Still other manipulation-related neurons peripersonal space for limb and neck movements (VIP-F
4
)
and visual transformation for eye movements (LIP-FEF) (Fig. discharged only when the monkey used the real object or
tool (Taira et al., 1990; Sakata et al., 1995). 1) (Rizzolatti et al., 1998).
The parietofrontal circuits subserving the transport Area F5 lies in the rostral part of the ventral premotor
cortex (PMv) and it is reciprocally connected with the AIP. (reaching) phase of movements towards an object originate
in the SPL. Several areas in the monkeys SPL use visual as It is also connected with the hand area of M1, and is therefore
specically related to distal movements (Matelli et al., well as somatosensory information for movement
organization, whereas others are mainly involved in the 1985). Hand neurons discharge during specic goal-related
movements such as grasping, tearing, manipulation and analysis of somatosensory stimuli for planning and controlling
arm movements. Lacquaniti and colleagues showed that area holding, whereas others are specic for a particular movement
in relation to certain types of hand grip (e.g. precision grip 5 (dorsal SPL) cell activity signalled arm postures and
movements in a body-centred frame of reference (Lacquaniti or nger prehension) (Rizzolatti et al., 1988). Thus, different
populations of neurons might encode different motor acts et al., 1995). About 70% of the neurons have tuning functions
that cluster around distance, azimuth (horizontal position) or (schemas). Some schemas represent general categories of
actions, such as grasping, holding and tearing; others indicate elevation (vertical position); the global reconstruction of a
limb position can be accomplished by the summation of how the objects are to be grasped (e.g. held and torn) and
the effectors (ngers) appropriate for the action; whereas still individual contributions in a population of neurons
(Lacquaniti et al., 1995). The SPL is the major source of other schemas are concerned with the temporal co-ordination
of the action. The motor schemas form a basic vocabulary projections to the dorsal premotor cortex (PMd). The PMd
is somatotopically organized and seems to play a key role in from which many dexterous movements can be constructed
as co-ordinated control programmes (Jeannerod et al., 1995). trajectory planning. As cells in the primary motor cortex,
PMd cells are tuned to movement direction, with a tendency The nal updating of the motor (or sensorymotor) schemas
related to the physical properties of an object seems to be to follow the position of the arm in space (Johnson et al.,
1996; Kalaska et al., 1997). On the other hand, numerous based on afferent information about specic mechanical
events in the skinobject contact areas during manipulation studies have described signal- and set-related activity in the
rostral PMd (F7), indicating a role in movement preparation (Johansson and Cole, 1992).
Graziano and Gross have suggested that a general principle and in the conditional selection of action (Passingham, 1993).
870 R. C. Leiguarda and C. D. Marsden
Fig. 1 (A) Lateral and mesial views of the cerebral hemisphere of macaque monkey. The intraparietal
sulcus has been opened (shaded grey) to show areas located in its medial and lateral bank. (B)
Simplied diagram of the organization of the parallel parietofrontal circuits for sensorymotor
integration. The parcellation of the agranular frontal cortex is dened according to the scheme used by
Matelli and colleagues in their studies of monkeys (Matelli et al., 1985, 1991). F
1
corresponds to the
primary motor cortex (M1), F
2
and F
7
correspond to the dorsal premotor cortex (PMd) and F
4
and F
5
to the ventral premotor cortex (PMv). F
6
and F
3
correspond to the presupplementary motor area (SMA)
and SMA proper, respectively. The arm is represented in F
1
, F
2
, F
3
, F
4
and F
5
, whereas the leg is
represented only in F
1
, F
2
and F
3
. F
6
and F
7
are almost devoid of corticospinal neurons. In the
posterior parietal lobe there are also multiple representations of the arm, leg and face. All parietal areas
are dened according to Pandya and Seltzer (Pandya and Seltzer, 1982), except those buried within the
intraparietal sulcus (IPs), which are dened according to physiological data (Rizzolatti et al., 1998).
CG cingulate gyrus; FEF frontal eye-eld; L lateral ssure; LIP lateral intraparietal area;
PE dorsal part of area 5; PEc posterior part of PE; PEci posterior part of cingulate sulcus;
PEip rostral part of the medial bank of IPs; PF anterior part of the convexity of IPL; POs
parieto-occipital sulcus; PFr prefrontal cortex; VIP ventral intraparietal area; V6a visual area 6
in the rostral bank of the POs. The monkey IPL is not homologous to human IPL since it is devoid of
Brodmann areas 39 and 40.
of sensorymotor integration is that the space surrounding VIP and the putamen respond both to tactile stimulation of
the face, arm or trunk, and to the presentation of visual the body be represented by body part-centred coordinates
(Graziano and Gross, 1998). Cells within PMv, areas 7b and stimuli. These areas are monosynaptically connected and
Limb apraxia 871
appear to form a system for the representation of the in the IPL. Gallese and colleagues found decits mainly
restricted to the grasping phase in monkeys with inactivation peripersonal space somatotopically. This system would be
particularly suitable for guiding and adapting movements of the AIP (Gallese et al., 1997). Jeannerod and colleagues
reported a patient who, after a bilateral parieto-occipital towards (or away from) everyday objects that surround us
(Graziano and Gross, 1998). infarction, showed a severe and bilateral grasping impairment;
the hand was widely open, without correlation between grip Functional brain imaging studies support the proposed
neurophysiological mechanisms for reaching and grasping. and object size, and the grasp was awkward and inaccurate
(Jeannerod et al., 1994). Binkofski and colleagues studied Matsumura and colleagues studied reaching and grasping
neutral objects. Compared with reaching, grasping was three patients with left hemisphere lesions (two of the
patients having ideomotor apraxia) and two patients with associated with increased activation bilaterally in the PM, the
prefrontal and posterior parietal areas, and in the contralateral right hemisphere lesions involving the anterior lateral bank
of the intraparietal sulcus, possibly the human homologue of cerebellum, thalamus and basal ganglia (globus pallidus and
caudate) (Matsumura et al., 1996). Rizzolatti and colleagues the AIP, who had selective temporal and spatial kinematic
decits in the co-ordination of the nger movements required found that the regions signicantly activated during the
execution of grasping movements were the precentral and for grasping a switch, with minor disturbances of the reaching
phase of the movement. An extended time to achieve maximal mesial motor areas, SPL and cuneus, putamen and cerebellum
(Rizzolatti et al., 1996), whereas Faillenot clearly hand aperture and a prominent disturbance of hand-shaping
was observed in all ve patients (Binkofski et al., 1998). In demonstrated activation of the premotor as well as mesial
frontal cortices in addition to the parietal and primary motor clinical terms, as the authors suggested, this visuomotor
decit would represent a focal decit of the unimodal apraxic and somatosensory cortices during grasping (Faillenot, 1997).
A recent functional MRI study in control subjects during type, as described by Freund (Freund, 1992). The report of
Sirigu and colleagues clearly demonstrated the relationship reaching and grasping a familiar object showed activation
of the contralateral sensorimotor cortex, bilateral premotor between grasping and praxis (Sirigu et al., 1995). Their
patient, with bilateral hypometabolismin the posterior parietal cortex, SMA and bilateral posterior parietal cortices.
Signicant bilateral activation, more marked on the regions, showed a selective praxic decit for hand postures
during the grasping of objects in the context of utilization contralateral side of the lateral bank of the anterior
intraparietal sulcus, was observed during grasping (Binkofski gestures, with apparently normal movement trajectories and
accurate scaling of manual grasp during simple reaching et al., 1998).
movements. Thus, object attributes are likely to be processed
differently according to the task in which the subject is
involved. When a subject is requested to grasp an object but
Selective apraxia-related decits resulting from
not to use it, the brain extracts the structural attributes of the
object (i.e. form, size, orientation) relevant to action to damage to the parietofrontal circuits
Lesions in the SPL involving circuits which subserve generate the appropriate movement. However, during
utilization gestures, in addition to data about object somatosensory transformation for reaching, somatosensory
transformation for posture and transformation of body part characteristics, prior knowledge about the functional
properties of objects needs to be integrated into the grasping location data into information for the control of body part
movements would explain the external conguration and subsystem to produce an accurate manual grasp (Jeannerod
et al., 1995; Sirigu et al., 1995). movement types of praxic errors such as faulty orientation
and abnormal limb conguration. Monkeys with bilateral Lesions in animals and humans involving those areas of
the motor cortex making up the parietofrontal circuits also lesions of area 5/7b/MIP showed misreaching in the dark but
not in the light, further conrming the essential role of area cause distinct types of praxic-like decits, though less
selectively than those observed when there is damage to the 5/7b/MIP for the spatial co-ordination of arm movements in
relation to proprioceptive and efference copy information parietal component of the circuits.
Earlier studies in monkeys with extensive ablations of the (Rushworth et al., 1997a). Heilman and colleagues described
a right-handed patient with an apraxia resulting from a right PMd cortex, some of them also involving the SMA and/or
prefrontal cortex, have shown groping reaching movements superior parietal lesion. Her performance with her left hand
was characterized by minor temporal but gross spatial errors, and impairment of skilled arm movements (Fulton et al.,
1932). On examining a problem box-trained chimpanzee after particularly with her eyes closed; she moved her arm
erroneously in space and oriented the limb abnormally in the paralysis of a premotor cortex ablation had remitted,
Jacobsen noticed that the animal appeared unable to organize relation to the object. She did not have visuomotor ataxia,
and grasping appeared to be preserved (Heilman et al., 1986). the necessary manipulations and had to relearn them, because
it was incapable of setting about the proper movements Selective decits limited to the grasping phase of the
movement, which can mirror some of the internal (Jacobsen, 1934). Similar results were reported in monkeys
with periarcuate lesions (Deuel, 1977). conguration types of praxic errors, have also been described
in animals and humans with damage to parietofrontal circuits Kurata and Hoffman found that muscimol injections in the
872 R. C. Leiguarda and C. D. Marsden
PMd caused directional errors in a visually cued delayed
Frontostriatal and frontoparietal systems:
response task, whereas when muscimol was injected in the
sequencing of movements
PMv the movements were in the correct direction, although
Functional brain imaging studies have shown that different
they were slower and of small amplitude (Kurata and
neural systems are actively engaged in the preparation and
Hoffman, 1994). Gallese and colleagues observed that
generation of a sequential action depending on whether a
inactivation of F
5
caused a decit similar to that caused by
sequence has been prelearned or is a new one, and contingent
inactivation of the AIP: a severe disruption of hand preshaping
on the complexity of the attentional demands of the task
and object grip without reaching decits (Gallese et al.,
(Jenkins et al., 1994; Grafton et al., 1995; Catalan et al.,
1997). However, the ability to grasp was not totally disrupted,
1998).
since the animal was still able to grasp the objects after a
The SMA, primary sensorimotor cortex, basal ganglia
series of corrections that relied on tactile explorations.
(mid-posterior putamen) and cerebellum may be mainly
Kennard and colleagues described a patient with persistent
involved in the execution of automatic, overlearned,
impairment of skilled movement after removal of a glioma
sequential movements, whereas the prefrontal, premotor and
from the right premotor area (Kennard et al., 1934). Luria
posterior parietal cortices and the anterior part of the caudate/
stressed the loss of the kinetic melody, resulting in
putamen would be particularly recruitedin addition to
disintegration of the dynamics of the motor act and of
such areas engaged in the execution of simple movement
complex skilled movements in patients with premotor lesions,
sequenceswhen a complex or newly learned sequence,
which is mainly apparent when the task requires the learning
which requires attention, integration of multimodal informa-
of a new skilled movement (Luria, 1980). Patients with
tion and working memory processes for its appropriate
frontal lobe lesions may exhibit decits in visually steering
selection and monitoring, has to be performed (Grafton et al.,
the arm accurately, particularly during rapid movements
1995; Miyachi et al., 1997; Catalan et al., 1998; Harrington
(catching a thrown ball) because of abnormal temporal
et al., 1998).
sequencing of muscular activation (Freund and Hummelstein,
Scheduling or timing a series of actions has been suggested
1985). As mentioned above, patients with premotor lesions
to be an emergent property of interactions of the left cerebral
exhibit a decit in conditional motor learning (Halsband and
cortex with the basal ganglia (Harrington and Haaland, 1992).
Freund, 1990; Passingham, 1993; Rushworth et al., 1997b).
Cortical systems with reciprocal pathways to the basal ganglia
Therefore, it might be posited that the disintegration of
(e.g. SMA, PM cortex), which receive projections from the
skilled hand movements may be attributed mainly to damage
cerebellum (e.g. PM cortex) or send bilateral projections to
to the PMv (F4 and F5) and dysfunction of those populations
the putamen and caudate, such as the inferior parietal cortex,
of neurons encoding the motor vocabulary in the frontal
are important candidates that may support timing processes
component of the circuit involved in grasping and
(Harrington et al., 1998). Rubia and colleagues have recently
manipulating. On the other hand, lesions in the PMd (F
2
and
suggested a neural network for temporal bridging and timing
F
7
) may cause (i) coordination breakdown of proximal arm
movements made up by the left prefrontal cortex, the SMA
muscles when these muscles are used for the generation of
and the supramarginal gyrus (Rubia et al., 1998). The frontal
reaching movements, (ii) abnormal orientation and trajectory
lobes have been considered to be a crucial structure for
defects, and (iii) decit in conditional motor learning, which
bridging temporal gaps in the action perception cycle and
may underlie the inappropriate selection of actions in relation
for the temporal organization of the motor output (Fuster,
to the context exhibited by apraxic patients (Passingham,
1990). The ndings of Halsband and colleagues in patients
1993).
with unilateral lesions of the frontal lobe have further
Patients with ideomotor apraxia may show abnormal
emphasized the critical roles of both the SMA and the PM
performance of transitive movements directed away from the
cortex in the generation of motor sequences from memory
body (e.g. hammering), whereas self-directed movements
that t into a precise timing plan (Halsband et al., 1993).
(e.g. combing) are relatively well executed. This dissociation
Thus, different neural systems would be engaged depending
might be due to the fact that the target of self-directed
on the type of movement sequence requested to be executed
actions, an important part of the context, is invariably present, during the evaluation of praxis. When the sequence is well
or that associated damage to the circuit subserving the known or automated, or else performed from memory, the
somatotopic representation of peripersonal space causes a SMAbasal ganglia system would be recruited preferentially.
decit in transforming object locations into appropriate However, most of the sequences used to test praxis are new
movements towards them (Graziano and Gross, 1998). In (e.g. sequencing of movement in the movement imitation
contrast, poorer performance of self-directed compared with test for ideomotor apraxia), or the content of an otherwise
externally directed movements may reect the fact that the well learned goal-directed action (e.g. the multiple sequential
former require the participation of another circuit, or that use of objects test for ideational apraxia) has to be represented
gestures directed towards the body demand greater movement explicitly. In any case, the system composed of the prefrontal,
precision than those performed away from the body (Roy premotor and parietal cortices, the striatum and white matter
fascicles would be engaged specically. In addition, it might and Square, 1994).
Limb apraxia 873
be possible that, within this system, there are many different PET studies in humans support neurophysiological ndings
in monkeys. Observation of grasping markedly increased subsystems subserving functionally separate cognitive
computations that are involved in motor sequencing (i.e. cerebral blood ow in the cortex of the STS, the rostral part
of Brocas area and in the rostral part of the left intraparietal timing, motor attention, selection of limb movements and
object-oriented responses), which may be selectively sulcus on the left hemisphere of right-handed subjects (Bonda
et al., 1996; Grafton et al., 1996; Rizzolatti et al., 1996). damaged by the pathological process and so produce different
types of sequencing impairment in apraxic patients Furthermore, when a gesture was observed with the intention
that it should be imitated rather than recognized, the activation (Harrington and Haaland, 1992; Roy and Square, 1994;
Rushworth et al., 1997b, 1998). was observed predominantly in structures usually involved
in the planning of action, such as the dorsolateral prefrontal
cortex and the SMA. If the action had a semantic content
referring to objects, it would be processed mainly by the
The temporoparietalfrontal system: recognition
ventral visual pathway (occipitotemporal cortex, hippo-
campus and PMv cortex) of the left hemisphere, whereas an and imitation of action
Di Pellegrino and colleagues discovered a particular subset unfamiliar action would activate the dorsal visual pathway
(occipitoparietal and PMd cortices) of the right hemisphere of neurons in F
5
which discharge while a monkey observes
meaningful hand movements made by the experimenter, in with the contribution of regions within the ventral pathway
(Decety et al., 1997). particular when interacting with objects; they called them
mirror neurons and speculated that they belong to an Thus, the imitation of meaningful actions seems to be
mediated by implicit knowledge about the form as well as observation/execution matching system involved in
understanding the meaning of motor events (Di Pellegrino the meaning of the gesture, which is processed by regions
involved in the planning and generation of actions plus the et al., 1992). Neurons with properties similar to those of
mirror neurons in F
5
are also found in the posterior superior temporal cortex (Decety et al., 1997). On the other hand,
imitation of meaningless actions would depend on the temporal sulcus (STS) in monkeys (the superior temporal
polysensory region, which might be the monkeys homologue decoding of their spatiotemporal layout in the
occipitoparietalPM cortex pathway (Decety et al., 1997), or of part of the human IPL) (Morel and Bullier, 1990; Perret
et al., 1990a; Milner, 1995; Oram and Perret, 1996). These on the analysis of arbitrary body movements or components
(i.e. hand open, nger extended) by cells in the temporal neurons respond not only to the sight of the monkeys own
hand performing the action, but also to the sight of the cortex and their corresponding parietal and/or premotor
connections (Carey et al., 1997). That imitative movements experimenters hand performing the same action, an
equivalence that may be crucial for recognizing, imitating or may be generated by direct connections between the
occipitotemporal and frontal cortices, without the shaping ones own actions to match those witnessed (Carey
et al., 1997). participation of the occipitoparietal pathway, is suggested by
the lack of correlation between the transport phase of a Two other types of neurons which may contribute to the
recognition and imitation of postures and actions have also movement and end-point errors in apraxic patients when they
imitate meaningful hand positions (Hermsdorfer et al., 1996) been found in the STS by Perrett and co-workers. One type
encodes the visual appearance of particular parts of the body In left brain-damaged patients with left limb apraxia,
the improvement on imitation may be explained by the (i.e. ngers, hands, arms) while static or in motion, and these
neurons combine in such a way that the collection of participation of the right hemisphere, or by the use of the
undamaged temporofrontal component of the putative system components can specify a particular meaningful posture or
action (Perret et al., 1995), whether novel actions or in the left hemisphere if the lesion is more posterior and
dorsally located (Carey et al., 1997). On the other hand, stereotyped social signals. The second type encodes specic
body movements, such as walking and turning (Perret several mechanisms may explain why patients are impaired
when imitating meaningless gestures but perform awlessly et al., 1990b).
Cells responding to handobject interaction might also be when imitating a meaningful one. A perceptive decit due
to a parietal lesion may cause an abnormal mental present in area 7b (Fogassi et al., 1998). Area 7b in the
rostral part of the convexity of the IPL sends its cortical transformation of another persons body part (Bonda et al.,
1995), or the defective imitation can be produced by inability output to the convexity F
5
; area 7b receives projection from
the STS region, and the latter is interconnected with the to store temporarily and/or manipulate spatial relationships
in visuospatial working memory. Both of these mechanisms frontal lobe (Matelli et al., 1985; Seltzer and Pandya, 1989),
thus closing a cortical circuit involved in the perception of may be bypassed when the meaningful gesture has access to
meaning. Alternatively, the decit may be due to damage to handobject interaction. The crucial cognitive role of the
STS7bF
5
network would be the internal representation of those populations of temporal cells encoding arbitrary hand
postures and movements with preservation of those engaged actions which, when evoked by an action made by others,
would be involved in two related functions: action recognition in encoding expressive body movements (or postures) and
object-oriented actions (Carey et al., 1997), or to a lesion and action imitation (Rizzolatti et al., 1998).
874 R. C. Leiguarda and C. D. Marsden
which disrupts the decoding of the spatiotemporal layout in of close interrelation between both premotor cortices during
movements, although subtle abnormalities may be observed in the occipitoparietalPM cortex pathway (Decety et al., 1997).
Imitation decit restricted to hand positions but with normal the limb ipsilateral to a damaged left hemisphere, particularly
when the subject pantomimes transitive movements to verbal nger conguration (Goldenberg and Hagmann, 1997) may
be explained by selective involvement of cell populations in command.
Involvement of the circuits subserving sensorimotor the temporal cortex which encode static hand but not
nger postures (Carey et al., 1997), although alternative transformation for grasping in the PMv cortex may produce
some of the ideomotor type of praxis errors conned to hand interpretations have been advanced (Goldenberg, 1999).
movements. However, we believe that damage to this region
of the premotor cortex would primarily disrupt particular
segments of the action and the specicity for different
Limb apraxias due to dysfunction of the
hand and nger movements and congurations. The motor
parietofrontal circuits: higher-order defects of
vocabulary necessary for the proper selection of nger and
hand movements would be impaired and a limb-kinetic type sensorimotor integration
Disruption of parietofrontal circuits and their subcortical of praxis decit would appear in the hand contralateral to
the more affected hemisphere regardless of the pattern of connections, subserving the transformation of sensory
information into action, would give rise to most of the praxic cerebral dominance. An associated sensory decitas occurs
in most patients with corticobasal degenerationthat would errors observed in ideomotor apraxia. Damage to circuits
devoted to sensorimotor transformation for grasping, reaching in addition interfere with the information necessary for the
nal updating of the nger and hand schemas to the objects and posture, as well as for the transformation of body part
location into the information necessary for the control of physical characteristics, further undermining the process of
manipulation, might be required for the adexterous hand body part movements, would produce incorrect nger and
hand posture and abnormal orientation of the tool/object, typical of limb-kinetic apraxia to nally develop.
The complexity of limb praxis disorders requires a inappropriate conguration of the arm and faulty orientation
of the movement (with respect to both the body and the multidisciplinary approach which should encompass expertise
ranging from clinical and cognitive neurology and neuro- target of the movement in extrapersonal space), as well as
movement trajectory abnormalities. These errors may be psychology to the basic neurosciences. Future studies
exploring normal praxis functions with functional neuro- observed in the limb contralateral to a left or right parietal
lesion, if an associated elemental motor or sensory decit imaging, as well as kinematic analysis of reaching, grasping
and manipulating components of object-oriented actions does not preclude their proper interpretation. However, they
would be particularly reective of ideomotor apraxia, and (particularly when combined with activation studies), in
patients with different types of limb praxis decits due to would then also be observed in the limb ipsilateral to a left
hemisphere lesion, when the patient pantomimes a transitive restricted focal cortical and subcortical lesions, will most
likely allow the specic underlying neural mechanisms to be movement under verbal command. Thus, the praxic quality
of the errors in ideomotor apraxia would be determined by identied and limb praxis disorders to be classied within
the framework of the modular organization of the brain. the context in which the movement is performed and the
cognitive requirements of the task.
Selective praxic decits may be observed when specic
circuits are involved in the parietal or frontal lobes. Damage Acknowledgements
The authors wish to thank Professor Hans Joachim Freund, to the SPL in circuits subserving somatosensory
transformation for reaching, posture and movements would who provided the most helpful comments on the previous
draft of the review, and both reviewers for detailed and produce praxic errors, such as abnormal limb orientation and
conguration, resembling those observed in patients with insightful comments.
apraxia secondary to superior parietal lesions (Heilman et al.,
1986). When the circuits subserving grasping mechanisms
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Tsuchiya K, Ikeda K, Uchihara T, Oda T, Shimada H. Distribution Received August 24, 1999. Revised October 28, 1999.
Accepted November 17, 1999 of cerebral cortical lesions in corticobasal degeneration: a