Review
Ideomotor apraxia: A review
Lewis A. Wheaton a,b
, Mark Hallett a,⁎
a
Human Motor Control Section, Medical Neurology Branch, National Institute of Neurological Disorders and Stroke,
National Institutes of Health, Bethesda, MD, United States
b
Division of Gerontology, Geriatric Research Education and Clinical Center, Veterans Affairs Medical Center, Baltimore, MD, United States
Received 3 January 2007; accepted 3 April 2007
Available online 16 May 2007
Abstract
Ideomotor apraxia (IMA) is a disorder traditionally characterized by deficits in properly performing tool-use pantomimes (e.g., pretending
to use a hammer) and communicative gestures (e.g., waving goodbye). These deficits are typically identified with movements made to verbal
command or imitation. Questions about this disorder relate to its diagnosis, anatomical correlates, physiological mechanisms involved, and
the patients in whom IMA is best characterized. In this review, utilizing information presented at an international workshop, we summarize
the present state of knowledge about IMA. We include insights on how to distinguish IMA from the other motor apraxias and confounding
disorders. We discuss testing for IMA and the need for more rigorous tests that examine more elements, such as imitation, actual use, task
selection, and recognizing proper use. From neurophysiological insights, we propose hypotheses of the necessity of networks in praxis
performance. We also point out that more neurophysiological knowledge in humans might lead to a better understanding of how different
brain structures may aid in the rehabilitation of praxis. While little is known about exactly how rehabilitation may be pursued, biological
evidence warrants the further exploration of this issue.
© 2007 Elsevier B.V. All rights reserved.
Keywords: Ideomotor apraxia; Motor control; Rehabilitation; Parietofrontal; Apraxia; Higher-order motor control
Contents
1. Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2. Clinical definitions of the apraxias . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
3. IMA diagnosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
4. Testing for IMA . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
5. Lesions that produce IMA . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
5.1. Left vs. right hemisphere lesions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
5.2. Basal ganglia lesions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
5.3. Callosal, cortical, and subcortical lesions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
6. Clinical and theoretical models of IMA . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
7. Physiology of parietal, premotor, and subcortical structures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
7.1. Parietal action coding . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
7.2. Premotor action coding . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
7.3. Networks of parietal and premotor areas for praxis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
8. Rehabilitation of IMA patients . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
9. Linking physiology and pathophysiology. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
Journal of the Neurological Sciences 260 (2007) 1–10
www.elsevier.com/locate/jns
⁎ Corresponding author. Human Motor Control Section, Medical Neurology Branch, National Institute of Neurological Disorders and Stroke, National
Institutes of Health, Building 10, Room 5N244, 10 Center Drive, MSC 1428, Bethesda, MD 20892-1428, United States. Tel.: +1 301 4969526.
E-mail address: hallettm@ninds.nih.gov (M. Hallett).
0022-510X/$ - see front matter © 2007 Elsevier B.V. All rights reserved.
doi:10.1016/j.jns.2007.04.014
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
1. Introduction
Ideomotor apraxia (IMA) has been studied since the early
1900s. Early investigations of the disorder focused on patients
who had lesions resulting from a stroke. These patients are
unable to perform communicative gestures and properly pantomime
tool use, and have other cognitive and motor problems.
Tool-use movements are more often impaired than
communicative gestures [1]. Deficits in actual tool use may
also be observed [2], and this makes the disorder practically
relevant. IMA is commonly seen in patients with stroke involving
the left hemisphere, and is also present in conditions
such as corticobasal degeneration (CBD), Parkinson's disease
(PD), Alzheimer's disease (AD), progressive supranuclear
palsy (PSP), and Huntington's disease (HD) [3–6].
In accord with the pioneering proposal of Hugo Liepmann,
Norman Geschwind [7,8] posited that IMA was a result of a
disconnection of anatomically separate cortical regions. While
Liepmann suggested that parietal and premotor areas were
mainly affected, Geschwind proposed a more specific model
based on the disconnection of Wernicke's area and the
convexity of the premotor cortex. The theory of a disconnection
has remained fairly strong over the years. It is known that
lesions of the periventricular white matter, which can create a
disconnection of the parietal and premotor cortices, may cause
apraxia [9]. Gray matter lesions may also result in disconnections,
since the gray matter is the source of white matter tracts.
Clinicoanatomical correlates are most commonly lesions of the
parietal or premotor cortices, or both [10]. However, lesions of
these areas do not always produce apraxia [10]. Apraxia is
present in at least one third of patients with left hemisphere
stroke [11], but the exact percentage is unclear since there is no
standard test for apraxia, and many neurologists do not
routinely test for the deficit. Additionally, there is some
ambiguity in distinguishing IMA from other motor apraxias.
Current research in IMA should begin with a better delineation
of the disorder.
2. Clinical definitions of the apraxias
The term apraxia is used to describe a variety of phenomena
involving different functions of the body (e.g., buccolingual
apraxia, construction apraxia, dressing apraxia, and gait
apraxia), but there are six main, recognized types of apraxia
involving the upper limb (Table 1). The precise definitions of
these apraxias are a focus of considerable debate, probably
because clinical reports of each apraxia type in similar patient
groups are inconsistent or insufficient. However, we define
the core deficits in each of the six apraxia subtypes:
1. Limb-kinetic apraxia involves deficits mainly in fine and
precise finger movements, such as those used in picking
up a small coin or paper clip. Grasping with the full hand
may also be affected. It is a basic motor coordination
deficit, not explainable by more elemental deficits implicating
areas such as the cerebellum or corticospinal tract.
2. Conceptual apraxia relates to the inability to solve tool/
mechanical problems. The distinguishing feature of the
deficit is the loss of tool–object associations, actions
associated with tools, and the mechanical advantage of
using tools. This deficit is more representative of a loss of
knowledge of proper performance than loss of motor
function.
3. Ideational apraxia is commonly confused with conceptual
apraxia. It is characterized as a failure to sequence task
elements correctly. Conceptual problems are not the main
issue. The distinguishing factor is that patients can convey
knowledge of how to perform a sequence task (e.g.,
making a ham sandwich), but they fail to properly order
the elements of the task, such as missing steps or doing
steps out of order.
4. In verbal–motor dissociation apraxia, patients fail to respond
to verbal commands to make movements. Dissociation
apraxia has also been referred to as disassociation
apraxia, but dissociation is the preferred term. (Heilman,
K., personal communication). This disorder may be more
involved with speech processing than motor performance.
5. Tactile apraxia is a selective disturbance of active touch.
Hand skills not related to object exploration and manipulation
are left intact. The disturbance is not specific for
tool use, but affects any use of the hand as a sense organ.
6. IMA, the focus of this review, is the inability to pantomime,
imitate, and, sometimes, use tools properly. The
movements are spatially incorrect, and may be abnormally
slow and deliberate. This deficit may extend into
communicative gestures as well, but is more often seen
in tool-use pantomime. The deficits commonly include
Table 1
The six main types of apraxia that affect the hand and arm
Apraxia Deficit
Ideomotor Deficit in pantomiming tool use and gestures specifically.
Knowledge of tasks is still present.
Limb-kinetic Loss of hand and finger dexterity generally
contralateral to the lesion. Mainly affects “manipulative”
movements.
Ideational Failure to carry out a series of tasks using multiple objects
for an intended purpose. Tools are identifiable, but no
coherent action is made.
Conceptual Loss of tool knowledge and inappropriate use of tools and
objects.
Verbal–motor
dissociation
Inability to respond properly to verbal commands to make
movements.
Tactile Disruption of use of the hand as a sense organ, in which
object exploration and manipulation are impaired.
2 L.A. Wheaton, M. Hallett / Journal of the Neurological Sciences 260 (2007) 1–10
orientation errors (e.g., holding a comb upside down on
top of the head) and spatial and temporal errors (e.g.,
carving a turkey with jerky vertical movements instead of
smooth anterior–posterior movements). Other deficits
include movement errors (e.g., patients make extra and
unnecessary movements or move the wrong joints). Use
of an object or tool in real-life situations may be impaired
as well. Patients may also perform “body part as object”
errors (e.g., when instructed to cut a slice of bread, they
will use the arm as if it were a knife instead of holding a
knife). An important distinction is that patients with IMA
must know what they are told to do. Thus, patients with
Wernicke's aphasia, agnosia, and asymbolia must be excluded
as confounds in any diagnosis. Aphasia, in particular,
must be excluded, as apparent apraxia often coexists
with language impairment. The coexistence occurs for
several reasons. One, brain areas that process language for
communication may overlap with brain areas that process
language to drive movement. Two, frontal areas involved
in language are also involved in complex movement,
perhaps because those brain areas devoted to the hand
communication gesturing of ancestral humans have been
co-opted for verbal communication of modern humans.
3. IMA diagnosis
It is important to have a sense of confounding elements
that may lead to a misdiagnosis of IMA. IMA is seen in
various disorders, including stroke, PD, PSP, and CBD.
While degraded spatial and temporal features of movements
are clearly indicative of IMA, subcortical signs such as
bradykinesia or dystonia may also be present, and these
might prevent a firm diagnosis. For example, pantomiming
“brushing your hair” in a patient with IMA might include
large circular arcs above the head, or incorrect orientation of
the hand for brushing the hair. Such errors cannot be attributed
to more elemental movement disorders, and thus it is
possible to make a bona fide diagnosis of apraxia in a
bradykinetic patient. It must be clear that the deficits occur
only for complex apraxia-specific tasks. If the deficits are
generalized to even simple movements, then it is difficult to
clearly make a case for IMA. It is expected that testing results
for these elemental motor disorders would appear normal in
patients with apraxia. However, a patient with PD, for
example, may have spatial and temporal deficits for all types
of movements. Thus, the problem is not related to lost or
damaged representations of motor programs, but to confounding
motor elements that prevent proper execution of all
movements. Clearly, typical IMA is best described as a
motor problem that cannot be attributed to other movement
or cognitive disorders, [12] as is certainly the case in CBD.
Patients with CBD may have many clinical features that
could contribute to a diagnosis of IMA. Corticobasal
syndrome (CBS), which is defined as a syndrome that has
the movement disorder features of CBD but with more
cognitive and perceptual abnormalities, may be more commonly
related to apraxia [13]. CBD (or CBS) can only be
confirmed upon post-mortem examination of the brain, revealing
the presence of tau+tangles, which correlate with the
clinical difficulties. Post-mortem findings show that the
clinical CBD syndrome is often misdiagnosed as AD, PSP,
Pick's disease, nonspecific degenerative changes, or Creutzfeldt–Jakob
disease, even in patients who have apraxia,
which is sometimes thought to be a hallmark of CBD [14].
Many investigators only study IMA in cases of relatively
focal stroke and avoid the confounds of degenerative cases,
in which the lesions are likely more widespread and present
with complex pathologies, unless adequately evaluated before
testing [3–6,15].
4. Testing for IMA
There is little consensus on the proper way to test for
IMA. As a result, reports may refer to “apraxia” without
details of the testing strategy, which makes interpretation of
the findings difficult. This issue directly relates to the
definition of apraxia. The traditional definition is one of a
disorder of learned, skilled movements. However, what the
“disorder” looks like is debatable. Differences in distinguishing
and testing the nature of the deficit arise from distinctions
between recognition or imitation, single object use tests and
multiple object use tests, pantomime only deficits and reallife
scenario deficits [16]. Additionally, when testing for
IMA is done carefully, a patient may have multiple apraxias,
which may present problems in interpreting the findings.
Many tests have been developed to characterize IMA.
While the tests meet the goal of capturing the most sensitive
deficits, they have become highly selective. This is justifiable,
but not entirely appropriate, as further research shows
that multiple deficits can occur in IMA. Testing should be
done bilaterally, if possible, as apraxia can affect both limbs
equally. In the event of a paretic limb, however, testing may
be done in the nonparetic (usually ipsilesional) limb. Many
studies rely on this standard [3,5,10].
Of the many tests used, two are particularly common. The
Test of Oral and Limb Apraxia (TOLA) is used [4], but is
incomplete because it ignores performance when the patient
sees or uses tools. While the Florida Apraxia Battery is also
used [17,18], it only assesses gestures to verbal command.
The scores of four different apraxia batteries were poorly
correlated, indicating that they all tested different features of
the deficit [19]. Apparently, investigators cannot entirely rely
on the most apparent features, but must assess the broad
spectrum of deficits occurring in patients with apraxia.
Assessing the activities of daily living is thought to be a
good way to test patients, but it is unclear to what extent IMA
affects such activities in each patient [19,20]. Analyzing the
motion of patients as they make specified movements may
be most reliable [21], because it clearly reveals different
characteristics of spatial abnormalities in IMA, based on
lesion location and clinical signs and symptoms [15]. In one
study, testing of pantomime to verbal command, imitation,
3L.A. Wheaton, M. Hallett / Journal of the Neurological Sciences 260 (2007) 1–10
performance upon seeing the tool, and performance with the
tool showed high inter-rater reliability and may have
accounted for other possible cognitive deficits, which
could be useful [22], but the patient population was small.
An ideal assessment of IMA for tool-use movements
should likely include at least the four factors related to IMA:
pantomime to verbal command, imitation, performance upon
seeing the tool, and performance with the tool. For gestures,
testing should include pantomime, imitation, and performance
in “real” situations (e.g., choosing to wave goodbye when
presented with a scene prompting this particular action).
Deficits in these actions are commonly seen in patients with
apraxia. In addition, recognition and discrimination of correct
pantomimes, performance of nonsense gestures, and tool
selection tasks are all valuable. Demonstration of intact basic
motor control should be an essential element of testing.
5. Lesions that produce IMA
5.1. Left vs. right hemisphere lesions
Continued debate concerns the precise cortical areas
involved in apraxia. Early studies of IMA and lesion location
suggested that subcortical damage to white matter tracts was
most critical [7]. However, white matter lesions are not more
common in IMA patients [23]. In fact, lesions in deeper brain
areas (e.g., white matter, thalamus, and basal ganglia) are
more common in nonapraxia groups. However, white matter
damage found in several other studies shows that subcortical
disconnection of the parietal and premotor areas may cause
apraxia [9,10]. In addition, damage to cortical structures,
particularly the angular gyrus or the supramarginal gyrus,
has been observed in cases of apraxia [12]. Generally, in
stroke patients, left hemisphere lesions of the parietal and
premotor areas are implicated in apraxia. Anterior lesions
may produce aphasia (e.g., ventrolateral premotor cortical
lesions extending into Broca's area) or paresis (e.g., SMA
lesions extending to the adjacent motor cortex), which make
the determination of IMA difficult or impossible. As well,
anterior lesions may produce disturbances in postural and
force control, while parietal lesions produce more severe
deficits of cognitive motor behavior, which is more
characteristic of IMA [24]. However, there are patients
with IMA apparently caused by SMA damage [25]. Other
patients have been reported to have IMA from lateral anterior
frontal lesions [10]. While the extent of premotor lesion
effects needs further study, it is clear that left-sided parietal
lesions commonly produce bilateral deficits on pantomiming
tool-use movements [26]. Because apraxia deficits are
clearly caused by lesions in nonprimary motor areas, it is
unlikely that the deficit is limited to execution only. There
must be a relationship to not only planning and execution,
but also the notion of the correct movement to make.
Lesions of the left hemisphere have been largely regarded as
the main cause of apraxia, but the right hemisphere has also been
implicated. In a study comparing left and right hemispheredamaged
patients, patients with left hemisphere impairment
performed worse on pantomime of tool-use, but there was no
difference in deficits of gestures, indicating that both the left and
right hemispheres may store gesture representations [27].
5.2. Basal ganglia lesions
Patients with basal ganglia lesions apparently may also
have apraxia. Generally, the left basal ganglia is involved in
control of spatial and temporal features of learned movements,
sequence learning, and response inhibition [28,29]. A
skilled, cognitively based movement (e.g., praxis) requires
smooth timing of the movement elements for it to be correct
[30,31]. Again, it is essential in any case of IMA that elemental
motor problems do not confound otherwise normal
praxis. Such deficits are commonly seen in patients with
damage to the basal ganglia.
With the avoidance of the confounding elementary motor
deficits, a diagnosis of IMA was made in patients with PD
and PSP [3]. A case study concluded that both IMA and
ideational apraxia were the result of basal ganglia damage in
a patient with CBD [32]. However, CBD has widespread
pathological effects that involve cortical structures. A patient
with basal ganglia and external capsule lesions produced
normal tool-use and communicative gestures on command
and imitation, but had low scores in performing intended
gestures appropriately based on the presented scenes [33].
While this is an expected deficit in apraxia, abnormally
produced pantomimes have been long considered a hallmark
of IMA. IMA is uncommon in HD when damage is limited to
the basal ganglia, but is more likely to occur when the cortex
or its interconnections are damaged [5].
It is still debated whether damage to the basal ganglia
alone can result in IMA. Qualitative evidence suggests that
there are apraxia patients with ischemic lesions of the left
basal ganglia only. However, the types of errors differed
from those in patients with cortical stroke [34]. In PD
patients, dopaminergic medication does not improve the
initial performance of an apraxic motor task (it does assist in
incremental learning of a motor command over time) [35].
The conclusion of this work is that the basal ganglia
themselves may not play a major role in the performance of
praxis movements, but they may play a role in apraxia
recovery. This highlights the importance of rigorous assessment
and identification of specific features critical to the
diagnosis of IMA. The clinical symptoms occurring with
basal ganglia damage should be better evaluated. The mechanisms
that might lead to apraxia in patients with basal
ganglia lesions also need to be studied.
5.3. Callosal, cortical, and subcortical lesions
Other types of lesions have been reported to cause IMA, but
they are not well studied. Callosal lesions were studied in
patients with complete callosotomy byhaving them pantomime
to visually presented objects [36]. The right (dominant) hand
4 L.A. Wheaton, M. Hallett / Journal of the Neurological Sciences 260 (2007) 1–10
performed correctly, but the left hand performed poorly,
indicating that left hemisphere networks relevant for praxis
may have limited control of the left hand. In a case study of a
patient with a lesion of the trunk and splenium of the corpus
callosum, apraxia was present with pantomime of object use,
but not imitation [37]. Such lesions evidently interfere with the
capacity of the left hand to retrieve the required representations
from the left hemisphere to control praxis. However, it is likely
that callosal patients with IMAwill serve as an important study
group to learn more about the information stored within the left
and right hemispheres related to performance of pantomime
and tool use (as will be discussed in the Rehabilitation of IMA
patients section). In addition, cortical and subcortical lesions
can cause ipsilateral IMA, such as in the case of sympathetic
apraxia. This has been shown with a patient with right-sided
hemiplegia and left-sided pantomiming deficits without
comprehension difficulties [38].
6. Clinical and theoretical models of IMA
Consideration of how the deficit manifests itself from
lesions in various locations has been of key interest to many
researchers, because lesions at different cortical and
subcortical processing levels may cause different deficits.
Early models hypothesized that IMA results from damage to
white matter tracts connecting higher level parietal areas,
which formulated ideas of a task, with lower level motor
areas, which executed the task [9]. This is the “disconnection”
hypothesis [8], which emphasizes cortico-cortical
projections as the main culprit. Evidence suggests that the
left parietal cortex (specifically, the inferior parietal lobule)
stores motor representations, or “engrams,” that, if damaged,
would affect not only performance, but also recognition of
pantomimes [39–44]. Damage to these engrams was initially
thought to explain the deficit [45]. Clearly, not all apraxic
patients have recognition deficits and white matter damage,
so both hypotheses (IMA resulting from white matter lesions
or particular parietal cortex lesions) can only be partially
true.
A recent paper rejects the notion that failure of normal
tool-use pantomime, most common in IMA, is representative
of natural movement. Because tool-use pantomime is rarely
done, the deficit may be most easily explained by the
patient's inability to create a new movement (tool-use
pantomime) that represents a familiar (actual tool use)
movement [33]. Thus, the patient would likely be impaired
only on pantomime, while real object use is intact. To
substantiate this, it is pointed out that posterior parietal
lesions may impair the patient's ability to position the hand
to use objects in accordance with knowledge of stored motor
representations, while grasping the objects and recognition
of appropriate hand postures for new tools remains intact
[46,47]. This further elaborates the role of the parietal cortex
and apraxia to additionally involve degraded hand postures
associated with familiar tools, and even global errors on
reproduction of complex hand configurations [48].
It has been thought that damage to different brain areas
may cause different types of apraxia [16], a concept coming
mainly from the theoretical notion of hierarchical processing
involved in apraxia (Fig. 1A). As input is delivered to
prompt a particular movement, this information must be
taken in and processed within a cortical network. Briefly, for
tool-use pantomime, this involves identification of the
movement and the knowledge of appropriate action based
on prior experiences with the tool or object. Implementation
of this knowledge into a motor formula representative of the
intended action follows. Afterwards, the motor command
should be correctly employed. Thus, damage to areas critical
for abstract knowledge, which control appropriate actions in
various situations (parietal cortex), may lead to conceptual or
ideational apraxias. Damage to knowledge of action in the
sensorimotor form (connections between parietal and
premotor cortices), which would affect spatial and temporal
processing, would lead to higher level production deficits,
characteristic of IMA. Damage to purely motor mechanisms
(motor cortex) would largely cause production deficits, such
as limb-kinetic apraxia.
Computational modeling of the anatomical aspects of
motor control has been proposed [49,50]. Modeling of the
bread slicing gesture in patients in a parkinsonian network of
reduced basal ganglia output revealed reduced spatial and
temporal accuracy of the movement, characteristic of the
deficit seen in IMA patients [51]. These findings could
support the role of the basal ganglia in praxis and IMA.
However, research has yet to firmly determine whether the
form of IMA reported in basal ganglia lesion studies is
typical, or what lesion profile could cause the deficit [21].
Modeling parietofrontal networks, including possible subcortical
components, will also contribute to our understanding
of the deficit.
7. Physiology of parietal, premotor, and subcortical
structures
Much of the evidence for the physiological function of the
parietal and premotor cortices comes from work in monkeys.
Extrapolating this information to human behavior is not
completely direct, as movement types and errors in IMA are
largely impossible to replicate in monkeys. However, insight
can be gained from these studies and hypotheses developed
from the findings.
7.1. Parietal action coding
Intensive investigation of the posterior parietal cortex
shows that it is involved in the preparation and execution of
eye movement, reach, grasp, and hand position. Stimulation
studies reveal that the ventral intraparietal area is involved in
many types of complex movements [52]. This work relates to
areas that are considered to be phylogenetically similar to
those regions in humans that mediate praxis. Coding complex
movements within these regions is of interest, even in
5L.A. Wheaton, M. Hallett / Journal of the Neurological Sciences 260 (2007) 1–10
the midst of convincing evidence supporting the generation
of complex movements from motor cortex stimulation alone
[53]. However, these movements are not as complex as
praxis movements. The medial intraparietal area has shown
regions of activity that can be decoded to position a cursor in
the direction of a movement before the movement begins
[54], and this has direct application to the functioning of
neuronal-based prosthetic devices [55]. If parietal activity
can be decoded, the development of robotic prosthetic devices
could be a possible rehabilitation strategy for patients
with apraxia. Such premovement activity is similar to intention
activity in the posterior parietal area [56].
7.2. Premotor action coding
Coding for complex action is also represented in the
premotor cortex [44]. Divisions of the lateral premotor
cortex have a role in movement planning. Specifically, the
dorsal part of the lateral premotor cortex has much in
common with the SMA in that they both project to the spinal
cord and both are involved in motor control [57]. It is
thought that the SMA together with its connection in the
parietal lobe plays an important role in movement onset and
specific sequences of multiple joint movements [58]. The
pre-SMA receives a modest connection from the parietal
lobe. This area controls actions encoded in the lateral
parietofrontal circuits, possibly through motivation or cognition
[59–61]. Cells having connections from the parietal
cortex to the caudal region of the dorsal premotor cortex
(PMd) are more active during a limb movement task [62].
However, the rostral PMd seems to have more of a role in
cognitive processes related to motor control [61].
7.3. Networks of parietal and premotor areas for praxis
Activities in different brain regions do not occur independently,
but are part of networks. Thus, for pantomime of
meaningful praxis movements, a functional network may include
V5, the inferior parietal lobule and inferotemporal
cortex, and the lateral premotor cortex. Involvement of the
basal ganglia is also certainly possible, particularly because
some connections of the parietal lobe to the premotor cortex
pass through the basal ganglia [63–65]. Since the critical brain
areas for apraxia (parietal lobe, basal ganglia, and premotor
cortex) are anatomically distinct, one must consider how
functional activity in separate areas influences activity in other
regions. There is evidence for cortical processing (ventral or
dorsal streams) and subcortical pathways in guiding goalFig.
1. (A) Hypothesized network involved in praxis, utilizing the left parietal, premotor, and motor cortices, with the brain areas that may correspond to that
particular function (in red) (adapted, see [32]). (B and C) EEG coherence analysis of activity related to the preparation and execution of self-paced transitive and
intransitive praxis in normal right-handed subjects, which verifies parts of the network shown in (A). Coherence increases are shown between electrodes over the
left parietal and premotor electrodes (B) and the left premotor and motor electrodes (C). Time (s) is relative to the movement onset (0 s) (see [72]).
6 L.A. Wheaton, M. Hallett / Journal of the Neurological Sciences 260 (2007) 1–10
directed behavior. While movements are made during
visuomotor paradigms, it is conceivable that different brain
networks are functioning, perhaps a temporal–striatal–premotor
pathway initially when defining a motor command and a
parietal–premotor pathway after learning has been established
[66–68]. Subcortical structures are involved in the initial
learning of motor actions compared with actual performance
[69]. This suggests that if a task is over-learned (e.g., communicative
gestures), a parietal–premotor network is active,
whereas, if a novel tool-use pantomime is performed [29], the
relevant pathway might be mediated by subcortical structures.
This view is substantiated clinically by the finding that patients
with CBD and basal ganglia lesions had no deficit in communicative
gestures, but tool-use pantomime and meaningless
gesture pantomime were impaired [70].
With regard to praxis performance, anatomical and physiological
studies have substantiated the hypothesis that
parietal and premotor areas are involved in praxis preparation
and execution [71–73]. When subjects make these
movements in a self-paced paradigm, EEG activity related to
praxis movements is seen in the parietal cortex 3.0 s before
movement onset [73,74]. Moreover, evidence suggests a
coherent left hemisphere parietal–premotor–motor network
engaged in self-paced praxis that is active before and during
movement onset [75]. This evidence is in anatomical accord
with cortical lesion data in apraxia patients, and suggests that
praxis is not defined best by discrete areas of activation but
rather by dynamic relationships across multiple areas. Not
only activation, but also binding of the activity in these
distinct cortical areas is imperative for proper execution of
these motor commands. These studies also support the existing
models of praxis performance (Fig. 1). While there is
some disagreement on the specifics of the models, the core
idea is that the parietal cortex stores the concept of the
movements and the premotor cortex modifies the concept to
a specific motor plan for motor cortex implementation.
Therefore, there must be communication between each of
these structures to successfully generate a plan for the
movement. Existing studies in humans clearly show convincing
anatomical correlates and functional coupling that
match what has been proposed in models and in monkeys.
EEG studies point to the presence of early parietal activity
that eventually spreads to the sensorimotor areas before praxis
movements, which differs from the confined premotor and
sensorimotor activity seen before simple movements [74]. In
addition, fMRI evidence supports premovement posterior
parietal activity extending to the anterior parietal cortex from
planning to execution of praxis [72]. There is a critical need for
more knowledge of the human physiological function of
networks of parietal and premotor areas for praxis. The results
will directly apply to patient care. One such aspect is the
possible role of the mirror neuron framework for the disturbance
of imitative motor behavior in apraxic patients.
Experimental and human studies have shown that parietal–
premotor circuits are instrumental for vision-to-action translation
and for observation–action matching. Whereas the premotor
cortex is generally involved in such tasks, the parietal
cortex is specifically recruited when the motor behavior is
object related [76]. Since damage of these areas is known to
interfere with the pragmatic aspects of goal-oriented movements,
disturbance of this capacity may provide interesting
new approaches to the investigation of apraxia. Understanding
behavioral effects and brain activations during observation and
imitation in apraxic patients can help in understanding this
process and improve therapy. It does appear that focusing
rehabilitation to apraxic deficits can improve function [77].
8. Rehabilitation of IMA patients
IMA has historically been viewed as a deficit only
manifested in clinical settings [78], but recent evidence has
supported the notion that IMA affects daily living [79,80].
Such evidence is important, as it emphasizes the necessity
of rehabilitation in patients with deficits in activities of
daily living. The impact of cognitive disabilities, such as
apraxia, is seen in attempts to rehabilitate stroke patients
[81]. Deficits in IMA must be better evaluated so that the
scope of necessary therapies can be completely defined. In
addition, some subacute patients spontaneously recover
from apraxia. Understanding this recovery process should
be useful in understanding the relevant processes of brain
plasticity. Unfortunately, there has been very little progress
in this area.
While rehabilitation literature is scarce, several biological
principles help to explain how recovery may occur. After left
hemisphere lesions impair basic motor function, homologous
right hemisphere structures begin to compensate over time [82].
Learning (or relearning) the playing of a stringed instrument
leads to an experience-based reorganization of the left parietal
and premotor cortices [83]. Activity related to spatial
processing in a patient with a parietal lesion shifts from the
left to right parietal lobe, suggesting plasticity of higher level
processes as well [84]. Early evidence suggests that this may
also be true for apraxia [85]. The mechanisms of this
hemispheric shift of activity are unknown. One mechanism
for re-establishing motor control in an impaired limb is the
release of intracortical inhibition [86]. The premotor cortex of
the lesioned hemisphere may reorganize to control movement
in the event of cortical damage [87]. The question of whether
these mechanisms can extend to include the parietal and
premotor cortices for praxis should be investigated. If the left
perilesional parietal cortex or the right parietal lobe stores
copies of the engrams used to perform praxis, then it is possible
to restore normal function. However, this speculation is
criticized, as it has been suggested that the right hemisphere
may not store praxis representations [88]. Work in patients with
complete callostomy shows apraxic errors only with the left
hand (right hemisphere control) during pantomime of visually
presented objects but not during actual object manipulation,
suggesting right hemisphere indeed stores representations for
movement concepts but has limited perceptual object representations
[89]. However, it is additionally shown that split-
7L.A. Wheaton, M. Hallett / Journal of the Neurological Sciences 260 (2007) 1–10
brain patients may imitate nonsense head–hand gestures
correctly so long as visual feedback of the imitating hand is
available, suggesting a heavy reliance of vision for proper
gesture performance [90]. It is encouraging though, to consider
that the right hemisphere may be able to utilize some limited
representations that it stores to mediate praxis performance, and
this might be helpful in recovery of function.
9. Linking physiology and pathophysiology
There is insufficient understanding of what lesions will
produce precisely what deficits. Advances are now possible
primarily due to the relatively recent emergence of data
relating specific cortical areas to particular functions in
monkeys [91,92]. It is difficult to properly assess normal
function of the brain based on lesions and the resulting
deficit [93]. This is even more difficult for apraxia, since
there are variable manifestations from apparently similar
lesions [10,94]. Progress should be possible by studying the
physiology and active anatomical areas related to praxis
movements in normal subjects. Investigators will then be
able to form better hypotheses related to brain-damaged
patients. In the clinic, we need an improved apraxia battery
for comparison of normal subjects and patients, which
should lead to clearer clinicoanatomical correlates. The
efforts made so far indicate that the different facets of complex
dysfunctions such as the apraxias may be better
attributed to networks than to circumscribed modules.
Acknowledgments
The meeting which engendered this review, the International
Workshop on Ideomotor Apraxia, held in Bethesda,
Maryland, on September 20–22, 2004, was sponsored by the
Office of Rare Diseases and the National Institute of Neurological
Disorders and Stroke at the National Institutes of
Health, and the Movement Disorder Society. The authors
thank the following persons for their participation and for their
insight during and after the meeting in the writing of this
review: Richard Andersen, Stephan Bohlhalter, Laurel
Buxbaum, Leonardo Cohen, Jose L. Contreras-Vidal, Hans
Joachim Freund, Scott Grafton, Michael Graziano, Kathleen
Haaland, Brenda Hanna-Pladdy, Edward B. Healton, Kenneth
Heilman, Anthony E. Lang, Ramon Leiguarda, Jay P. Mohr,
Hiroshi Shibasaki, Angela Sirigu, Alan Sunderland, Ivan Toni,
and Steven Wise.
We also thank Devera Schoenberg and B.J. Hessie for
skillful editing.
References
[1] Haaland KY, Flaherty D. The different types of limb apraxia errors
made by patients with left vs. right hemisphere damage. Brain Cogn
1984;3:370–84.
[2] Poizner H, Clark MA, Merians AS, Macauley B, Gonzalez Rothi LJ,
Heilman KM. Joint coordination deficits in limb apraxia. Brain
1995;118:227–42.
[3] Leiguarda RC, Pramstaller PP, Merello M, Starkstein S, Lees AJ,
Marsden CD. Apraxia in Parkinson's disease, progressive supranuclear
palsy, multiple system atrophy and neuroleptic-induced parkinsonism.
Brain 1997;120:75–90.
[4] Pharr V, Uttl B, Stark M, Litvan I, Fantie B, Grafman J. Comparison of
apraxia in corticobasal degeneration and progressive supranuclear
palsy. Neurology 2001;56:957–63.
[5] Hamilton JM, Haaland KY, Adair JC, Brandt J. Ideomotor limb apraxia
in Huntington's disease: implications for corticostriate involvement.
Neuropsychologia 2003;41:614–21.
[6] Parakh R, Roy E, Koo E, Black S. Pantomime and imitation of limb
gestures in relation to the severity of Alzheimer's disease. Brain Cogn
2004;55:272–4.
[7] Geschwind N. Disconnexion syndromes in animals and man. I. Brain
1965;88:237–94.
[8] Geschwind N. Disconnexion syndromes in animals and man. II. Brain
1965;88:585–644.
[9] Kertesz A, Ferro JM. Lesion size and location in ideomotor apraxia.
Brain 1984;107:921–33.
[10] Haaland KY, Harrington DL, Knight RT. Neural representations of
skilled movement. Brain 2000;123:2306–13.
[11] Donkervoort M, Dekker J, van den Ende E, Stehmann-Saris JC,
Deelman BG. Prevalence of apraxia among patients with a first left
hemisphere stroke in rehabilitation centres and nursing homes. Clin
Rehabil 2000;14:130–6.
[12] Heilman KM, Gonzalez Rothi LJ. Apraxia. In: Heilman KM,
Valenstein E, editors. Clinical Neurophysiology. 4 ed. New York:
Oxford University Press; 2003. p. 215–35.
[13] Lang AE. Corticobasal degeneration: selected developments. Mov
Disord 2003;18(Suppl 6):S51–6.
[14] Boeve BF, Maraganore DM, Parisi JE, Ahlskog JE, Graff-Radford N,
Caselli, et al. Pathologic heterogeneity in clinically diagnosed corticobasal
degeneration. Neurology 1999;53:795–800.
[15] Leiguarda R, Merello M, Balej J, Starkstein S, Nogues M, Marsden
CD. Disruption of spatial organization and interjoint coordination in
Parkinson's disease, progressive supranuclear palsy, and multiple
system atrophy. Mov Disord 2000;15:627–40.
[16] Buxbaum LJ. Ideomotor apraxia: a call to action. Neurocase 2001;7:
445–58.
[17] Hanna-Pladdy B, Daniels SK, Fieselman MA, Thompson K, Vasterling
JJ, Heilman KM, Foundas AL. Praxis lateralization: errors in right and
left hemisphere stroke. Cortex 2001;37:219–30.
[18] Rothi LJ, Raymer AM, Maher L, Greenwald M, Morris M. Assessment
of naming failures in neurological communication disorders. Clin
Commun Disord 1991;1:7–20.
[19] Butler JA. How comparable are tests of apraxia? Clin Rehabil 2002;16:
389–98.
[20] van Heugten CM, Dekker J, Deelman BG, Stehmann-Saris JC,Kinebanian
A. Rehabilitation of stroke patients with apraxia: the role of additional
cognitive and motor impairments. Disabil Rehabil 2000;22:547–54.
[21] Elble RJ. Motion analysis to the rescue? Mov Disord 2000;15:595–7.
[22] Zwinkels A, Geusgens C, van de Sande P, Van Heugten C. Assessment
of apraxia: inter-rater reliability of a new apraxia test, association
between apraxia and other cognitive deficits and prevalence of apraxia
in a rehabilitation setting. Clin Rehabil 2004;18:819–27.
[23] Basso A, Luzzatti C, Spinnler H. Is ideomotor apraxia the outcome of
damage to well-defined regions of the left hemisphere? Neuropsychological
study of CATcorrelation. J Neurol Neurosurg Psychiatry 1980;43:
118–26.
[24] Freund HJ. Clinical aspects of premotor function. Behav Brain Res
1985;18:187–91.
[25] Watson RT, Fleet WS, Gonzalez-Rothi L, Heilman KM. Apraxia and
the supplementary motor area. Arch Neurol 1986;43:787–92.
[26] Halsband U, Schmitt J, Weyers M, Binkofski F, Grutzner G, Freund
HJ. Recognition and imitation of pantomimed motor acts after
unilateral parietal and premotor lesions: a perspective on apraxia.
Neuropsychologia 2001;39:200–16.
8 L.A. Wheaton, M. Hallett / Journal of the Neurological Sciences 260 (2007) 1–10
[27] Roy EA, Heath M, Westwood D, Schweizer TA, Dixon MJ, Black SE,
et al. Task demands and limb apraxia in stroke. Brain Cogn
2000;44:253–79.
[28] Boyd LA, Winstein CJ. Impact of explicit information on implicit
motor-sequence learning following middle cerebral artery stroke. Phys
Ther 2003;83:976–89.
[29] Seiss E, Praamstra P. The basal ganglia and inhibitory mechanisms in
response selection: evidence from subliminal priming of motor responses
in Parkinson's disease. Brain 2004;127:330–9.
[30] Harrington DL, Haaland KY. Sequencing and timing operations of the
basal ganglia. In: Rosenbaum DA, Collyer CE, editors. Timing of
Behavior: Neural, Psychological and Computational Perspectives.
Cambridge: MIT Press; 1998. p. 35–61.
[31] Harrington DL, Haaland KY, Hermanowicz N. Temporal processing in
the basal ganglia. Neuropsychology 1998;12:3–12.
[32] Chainay H, Humphreys GW. Ideomotor and ideational apraxia in
corticobasal degeneration: a case study. Neurocase 2003;9:177–86.
[33] Bartolo A, Cubelli R, Della Sala S, Drei S. Pantomimes are special
gestures which rely on working memory. Brain Cogn 2003;53:483–94.
[34] Hanna-Pladdy B, Heilman KM, Foundas AL. Cortical and subcortical
contributions to ideomotor apraxia: analysis of task demands and error
types. Brain 2001;124:2513–27.
[35] Hanna-Pladdy B, Heilman KM. The role of dopamine in motor learning.
Thirteenth Annual International Neuropsychological Society Conference,
2002. Toronto, Canada. Cambridge University Press; 2002. p. 204.
[36] Lausberg H, Kita S, Zaidel E, Ptito A. Split-brain patients neglect left
personal space during right-handed gestures. Neuropsychologia
2003;41:1317–29.
[37] Goldenberg G, Laimgruber K, Hermsdorfer J. Imitation of gestures by
disconnected hemispheres. Neuropsychologia 2001;39:1432–43.
[38] Geschwind N. Sympathetic dyspraxia. Trans Am Neurol Assoc
1963;88:219–20.
[39] Kalaska JF, Scott SH, Cisek P, Sergio LE. Cortical control of reaching
movements. Curr Opin Neurobiol 1997;7:849–59.
[40] Kertzman C, Schwarz U, Zeffiro TA, Hallett M. The role of posterior
parietal cortex in visually guided reaching movements in humans. Exp
Brain Res 1997;114:170–83.
[41] Moll J, De Oliveira-Souza R, De Souza-Lima F, Andreiuolo PA.
Activation of left intraparietal sulcus using a fMRI conceptual praxis
paradigm. Arq Neuropsiquiatr 1998;56:808–11.
[42] Moll J, de Oliveira-Souza R, Passman LJ, Cunha FC, Souza-Lima F,
Andreiuolo PA. Functional MRI correlates of real and imagined tooluse
pantomimes. Neurology 2000;54:1331–6.
[43] Rizzolatti G, Fogassi L, Gallese V. Parietal cortex: from sight to action.
Curr Opin Neurobiol 1997;7:562–7.
[44] Rushworth MF, Johansen-Berg H, Gobel SM, Devlin JT. The left
parietal and premotor cortices: motor attention and selection. Neuroimage
2003;20(Suppl 1):S89–S100.
[45] Heilman KM, Rothi LJ, Valenstein E. Two forms of ideomotor apraxia.
Neurology 1982;32:342–6.
[46] Buxbaum LJ, Sirigu A, Schwartz MF, Klatzky R. Cognitive
representations of hand posture in ideomotor apraxia. Neuropsychologia
2003;41:1091–113.
[47] Sirigu A, Cohen L, Duhamel JR, Pillon B, Dubois B, Agid Y. A
selective impairment of hand posture for object utilization in apraxia.
Cortex 1995;31:41–55.
[48] Sunderland A, Sluman SM. Ideomotor apraxia, visuomotor control and the
explicit representation of posture. Neuropsychologia 2000;38:923–34.
[49] Burnod Y, Baraduc P, Battaglia-Mayer A, Guigon E, Koechlin E,
Ferraina S, et al. Parieto-frontal coding of reaching: an integrated
framework. Exp Brain Res 1999;129:325–46.
[50] Contreras-Vidal JL, Kerick SE. Independent component analysis of
dynamic brain responses during visuomotor adaptation. Neuroimage
2004;21:936–45.
[51] Contreras-Vidal JL. Computer modeling in basal ganglia disorders. In:
Litvan I, editor. Atypical Parkinsonian Disorders: Clinical and
Research Aspects. Totowa: Humana Press; 2004. p. 95–108.
[52] Cooke DF, Taylor CS, Moore T, Graziano MS. Complex movements
evoked by microstimulation of the ventral intraparietal area. Proc Natl
Acad Sci U S A 2003;100:6163–8.
[53] Graziano MS, Taylor CS, Moore T, Cooke DF. The cortical control of
movement revisited. Neuron 2002;36:349–62.
[54] Musallam S, Corneil BD, Greger B, Scherberger H, Andersen RA.
Cognitive control signals for neural prosthetics. Science 2004;305:
258–62.
[55] Andersen RA, Burdick JW, Musallam S, Pesaran B, Cham JG.
Cognitive neural prosthetics. Trends Cogn Sci 2004;8:486–93.
[56] Andersen RA, Buneo CA. Intentional maps in posterior parietal cortex.
Annu Rev Neurosci 2002;25:189–220.
[57] Geyer S, Matelli M, Luppino G, Zilles K. Functional neuroanatomy of
the primate isocortical motor system. Anat Embryol (Berl) 2000;202:
443–74.
[58] Tanji J, Shima K, Mushiake H. Multiple cortical motor areas and
temporal sequencing of movements. Brain Res Cogn Brain Res 1996;5:
117–22.
[59] Picard N, S.P. Imaging the premotor areas. Curr Opin Neurobiol 2001;11:
663–72.
[60] Rizzolatti G, Luppino G, Matelli M. The organization of the cortical
motor system: new concepts. Electroencephalogr Clin Neurophysiol
1998;106:283–96.
[61] Picard N, Strick PL. Imaging the premotor areas. Curr Opin Neurobiol
2001;11:663–72.
[62] Boussaoud D. Attention versus intention in the primate premotor cortex.
Neuroimage 2001;14:S40–5.
[63] Petrides M, Pandya DN. Projections to the frontal cortex from the
posterior parietal region in the rhesus monkey. J Comp Neurol 1984;228:
105–16.
[64] Glickstein M. Subcortical projections of the parietal lobes. Adv Neurol
2003;93:43–55.
[65] Geyer S, Matelli M, Luppino G, Zilles K. Functional neuroanatomy of
the primate isocortical motor system. Anat Embryol (Berl) 2000;202:
443–74.
[66] Toni I, Shah NJ, Fink GR, Thoenissen D, Passingham RE, Zilles K.
Multiple movement representations in the human brain: an event-related
fMRI study. J Cogn Neurosci 2002;14: 769–84.
[67] Thoenissen D, Zilles K, Toni I. Differential involvement of parietal and
precentral regions in movement preparation and motor intention.
J Neurosci 2002;22:9024–34.
[68] Toni I, Rowe J, Stephan KE, Passingham RE. Changes of corticostriatal
effective connectivity during visuomotor learning. Cereb Cortex
2002;12:1040–7.
[69] Gerardin E, Sirigu A, Lehericy S, Poline JB, Gaymard B, Marsault C,
et al. Partially overlapping neural networks for real and imagined hand
movements. Cereb Cortex 2000;10:1093–104.
[70] Salter JE, Roy EA, Black SE, Joshi A, Almeida Q. Gestural imitation
and limb apraxia in corticobasal degeneration. Brain Cogn 2004;55:
400–2.
[71] Johnson-Frey SH, Newman-Norlund R, Grafton ST. A distributed left
hemisphere network active during planning of everyday tool use skills.
Cereb Cortex 2004;15:681–95.
[72] Fridman E, Immisch I, Hanakawa T, Bohlhalter S, Waldvogel D,
Kansaku K, et al. The role of the dorsal stream for gesture production.
Neuroimage 2006;29:417–28.
[73] Wheaton LA, Shibasaki H, Hallett M. Temporal activation pattern of
parietal and premotor areas related to praxis movements. Clin
Neurophysiol 2005;116:1201–12.
[74] Wheaton LA, Yakota S, Hallett M. Posterior parietal negativity preceding
self-paced praxis movements. Exp Brain Res 2005;163:535–9.
[75] Wheaton LA, Nolte G, Bohlhalter S, Fridman E, Hallett M. Synchronization
of parietal and premotor areas during preparation and execution
of praxis hand movements. Clin Neurophysiol 2005;116:1382–90.
[76] Buccino G, Vogt S, Ritzl A, Fink GR, Zilles K, Freund HJ, et al. Neural
circuits underlying imitation learning of hand actions: an event-related
fMRI study. Neuron 2004;42:323–34.
9L.A. Wheaton, M. Hallett / Journal of the Neurological Sciences 260 (2007) 1–10
[77] Smania N, Aglioti SM, Girardi F, Tinazzi M, Fiaschi A, Cosentino A,
et al. Rehabilitation of limb apraxia improves daily life activities in
patients with stroke. Neurology 2006;67:2050–2.
[78] Liepmann H. Ein Fall von linksseitiger Agraphie und Apraxie bei
reshtsseitiger Lahmung. J Psychol Neurol 1907;10:214–27.
[79] Hanna-Pladdy B, Heilman KM, Foundas AL. Ecological implications
of ideomotor apraxia: evidence from physical activities of daily living.
Neurology 2003;60:487–90.
[80] Foundas AL, Macauley BL, Raymer AM, Maher LM, Heilman KM,
Gonzalez Rothi LJ. Ecological implications of limb apraxia: evidence
from mealtime behavior. J Int Neuropsychol Soc 1995;1:62–6.
[81] Walker CM, Sunderland A, Sharma J, Walker MF. The impact of
cognitive impairment on upper body dressing difficulties after stroke: a
video analysis of patterns of recovery. J Neurol Neurosurg Psychiatry
2004;75:43–8.
[82] Luft AR, Waller S, Forrester L, Smith GV, Whitall J, Macko RF, et al.
Lesion location alters brain activation in chronically impaired stroke
survivors. Neuroimage 2004;21:924–35.
[83] Kim DE, Shin MJ, Lee KM, Chu K, Woo SH, Kim YR, et al. Musical
training-induced functional reorganization of the adult brain: functional
magnetic resonance imaging and transcranial magnetic stimulation
study on amateur string players. Hum Brain Mapp 2004;23:188.
[84] Zacks JM, Michelon P, Vettel JM, Ojemann JG. Functional reorganization
of spatial transformations after a parietal lesion. Neurology
2004;63:287–92.
[85] Bohlhalter S, Fridman E, Wheaton L, Hattori N, Grafman J, Hallett M.
Hemispheric lateralization of normal and impaired praxis movements:
an event-related functional MRI study. Mov Disord 2005;20:S39.
[86] Murase N, Duque J, Mazzocchio R, Cohen LG. Influence of
interhemispheric interactions on motor function in chronic stroke.
Ann Neurol 2004;55:400–9.
[87] Fridman EA, Hanakawa T, Chung M, Hummel F, Leiguarda RC,
Cohen LG. Reorganization of the human ipsilesional premotor cortex
after stroke. Brain 2004;127:747–58.
[88] Colvin MK, Handy TC, Gazzaniga MS. Hemispheric asymmetries in
the parietal lobes. Adv Neurol 2003;93:321–34.
[89] Lausberg H, Cruz RF, Kita S, Zaidel E, Ptito A. Pantomime to visual
presentation of objects: left hand dyspraxia in patients with complete
callostomy. Btain 2003;126:343–60.
[90] Lausberg H, Cruz RF. Hemispheric specialisation for imitation of
hand-head positions and finger configurations: a controlled study in
patients with complete callosotomy. Neuropsychologia 2004;42:
320–34.
[91] Rizzolatti G, Luppino G. The cortical motor system. Neuron 2001;31:
889–901.
[92] Fogassi L, Gallese V, Buccino G, Craighero L, Fadiga L, Rizzolatti G.
Cortical mechanism for the visual guidance of hand grasping movements
in the monkey: a reversible inactivation study. Brain 2001;124:571–86.
[93] Rorden C, Karnath HO. Using human brain lesions to infer function: a
relic from a past era in the fMRI age? Nat Rev Neurosci 2004;5:813–9.
[94] Goldenberg G. Pantomime of object use: a challenge to cerebral
localization of cognitive function. Neuroimage 2003;20:S101–6.
10 L.A. Wheaton, M. Hallett / Journal of the Neurological Sciences 260 (2007) 1–10