C. von Hofsten & K. Rosander (Eds.)
Progress in Brain Research, Vol. 164
ISSN 0079-6123
Copyright r 2007 Elsevier B.V. All rights reserved
CHAPTER 4
Apraxia: a review
Biljana Petreska1,Ã, Michela Adriani2
, Olaf Blanke2
and Aude G. Billard1
1
Learning Algorithms and Systems Laboratory (LASA), Ecole Polytechnique Fe´de´rale de Lausanne (EPFL),
EPFL-STI-I2S-LASA, Station 9, CH 1015 Lausanne, Switzerland
2
Laboratory of Cognitive Neuroscience (LNCO), Ecole Polytechnique Fe´de´rale de Lausanne (EPFL), EPFL-SV-BMI,
Station 15, CH 1015 Lausanne, Switzerland
Abstract: Praxic functions are frequently altered following brain lesion, giving rise to apraxia — a complex
pattern of impairments that is difficult to assess or interpret. In this chapter, we review the current taxonomies
of apraxia and related cognitive and neuropsychological models. We also address the questions of the
neuroanatomical correlates of apraxia, the relation between apraxia and aphasia and the analysis of apraxic
errors. We provide a possible explanation for the difficulties encountered in investigating apraxia and also
several approaches to overcome them, such as systematic investigation and modeling studies. Finally, we
argue for a multidisciplinary approach. For example, apraxia should be studied in consideration with and
could contribute to other fields such as normal motor control, neuroimaging and neurophysiology.
Keywords: apraxia; brain lesion; neuropsychological models of apraxia; kinematic studies; computational
neuroscience; multidisciplinary approach
Introduction
Apraxia is generally defined as ‘‘a disorder of
skilled movement not caused by weakness, akinesia,
deafferentation, abnormal tone or posture,
movement disorders such as tremor or chorea,
intellectual deterioration, poor comprehension, or
uncooperativeness’’ (Heilman and Rothi, 1993).
Apraxia is thus negatively defined, in terms of what
it is not, as a higher order disorder of movement
that is not due to elementary sensory and/or motor
deficits. This definition implies that there are situations
where the effector is moved with normal
skill (Hermsdo¨ rfer et al., 1996). Puzzling parts of
apraxia are the voluntary-automatic dissociation
and context-dependence. On the one hand, apraxic
patients may spontaneously perform gestures that
they cannot perform on command (Schnider et al.,
1997). This voluntary-automatic dissociation can
be illustrated by an apraxic patient who could use
his left hand to shave and comb himself, but could
not execute a specific motor action such as opening
the hand so as to let go of an object (Lausberg
et al., 1999). In this particular case, focusing on the
target of the movement rather than on the movement
itself increased his chances of a successful
execution. On the other hand, the execution of the
movement depends heavily on the context of testing
(De Renzi et al., 1982). It may be well preserved
in a natural context, with a deficit that appears in
the clinical setting only, where the patient has to
explicitly represent the content of the action outside
of the situational props (Jeannerod and
Decety, 1995; Leiguarda and Marsden, 2000).
Several authors agree that although apraxia is
easy to demonstrate, it has proven difficult to
understand. Research on apraxia is filled with
ÃCorresponding author. Tel.: +41 21 693 54 65;
Fax: +41 21 693 78 50; E-mail: biljana.petreska@a3.epfl.ch
DOI: 10.1016/S0079-6123(07)64004-7 61
confusing terminology, contradictory results and
doubts that need to be resolved (De Renzi et al.,
1982; Goldenberg et al., 1996; Graham et al., 1999;
Koski et al., 2002; Laeng, 2006). Inconsistencies
between similar studies may be explained by differences
in the methodological and statistical approaches
for the apraxia assessment (i.e., types of
gestures used and scoring criteria), chronicity and
aetiology of damage and brain lesion localization
tools (Haaland et al., 2000). Therefore, it still stands
that our understanding of the neural and cognitive
systems underlying human praxis is not well establi-
shed.
The chapter is structured as follows. We first review
existing types of apraxia as well as important
current and historical models of the apraxic deficit.
We then consider the inter- and intra-hemispheric
lesion correlates of apraxia. Two other sections are
dedicated to the relationship between praxis and
language and to the analysis of apraxic errors. We
finally discuss the current state-of-the-art in apraxia,
and argue for a multidisciplinary approach
that encompasses evidence from various fields such
as neuroimaging or neurophysiology.
Types of apraxia
This section reviews the current taxonomies of apraxia.
Some of the frequently observed types of apraxia
have inspired the apraxia models described in
the following section, others still challenge them.
Ideational apraxia was historically defined as a
disturbance in the conceptual organization of actions.
It was first assessed by performing purposive
sequences of actions that require the use of various
objects in the correct order (e.g., preparing a cup of
coffee) (Poeck, 1983). It was later accepted that
ideational apraxia is not necessarily associated to
complex actions, but is a larger deficit that also
concerns the evocation of single actions. In this
view, complex sequences of multiple objects are
simply more suitable to reveal the deficit, possibly
because of the heavier load placed on memory and
attentional resources (De Renzi and Lucchelli,
1988). Nonetheless, the term conceptual apraxia
was introduced to designate content errors in single
actions, excluding sequence errors in multi-staged
actions with tools1
(Ochipa et al., 1992; Heilman et
al., 1997). In theoretical models, ideational and
conceptual apraxia correspond to a disruption of
the conceptual component of the praxis system, i.e.,
action semantics memory, described in more detail
in the ‘‘Models of apraxia’’ section (De Renzi and
Lucchelli, 1988; Graham et al., 1999). Patients with
ideational apraxia are not impaired in the action
execution per se, but demonstrate inappropriate use
of objects and may fail in gesture discrimination
and matching tasks. For example, a patient was
reported to eat with a toothbrush and brush his
teeth with a spoon and a comb. His inability to use
tools could not be explained by a motor production
deficit that would characterize ideomotor apraxia
(defined below). Interestingly, although he was able
to name the tools and point to them on command,
he could not match the tools with the objects, hence
suggesting a loss of knowledge related to the use of
tools.
Ideomotor apraxia is considered to be a disorder
of the production component of the praxis system,
i.e., sensorimotor action programs that are concerned
with the generation and control of motor
activity (Rapcsak et al., 1995; Graham et al.,
1999). It is characterized by errors in the timing,
sequencing and spatial organization of gestural
movements (Leiguarda, 2001). Since the conceptual
part of the praxis system is assumed to be
intact, patients with ideomotor apraxia should not
use objects and tools in a conceptually inappropriate
fashion and should not have difficulty with
the serial organization of an action (De Renzi
et al., 1982). Ideational and ideomotor apraxia
have been assessed by testing the execution of
various types of gestures: transitive and intransitive
(i.e., with or without the use of tools or objects),
meaningless non-representational (e.g.,
hand postures relative to head) and meaningful
representational (e.g., waving good-bye), complex
sequences with multiple objects, repetitive movements,
distal and proximal gestures (e.g., imitation
of finger and hand configurations), reaching in
peri-personal and body-centered space (e.g., targets
in near space or on the patient’s body), novel
movements (i.e., skill acquisition) or imagined
1
Conceptual apraxia is often observed in Alzheimer’s disease.
62
movements. These gestures can also be executed
under different modalities such as: verbal command,
imitation, pantomime and tactile or visual
presentation of objects.
The use of various gestures and different
modalities to assess apraxia has helped to uncover
many interesting functional dissociations that are
listed below. For example, apraxia was shown to
be modality-specific, i.e., the same type of gesture
was differentially impaired according to the
modality of testing (De Renzi et al., 1982). One
dissociation, named conduction apraxia, is the
syndrome of superior performance on verbal command
than on imitation (Ochipa et al., 1994). The
opposite pattern has also been observed: very poor
performance on verbal command that improved
on imitation or when seeing the object (Heilman,
1973; Merians et al., 1997). The extreme occurrence
of conduction apraxia, namely the selective
inability to imitate with normal performance on
verbal command was termed visuo-imitative
apraxia (Merians et al., 1997). In some cases of
visuo-imitative apraxia, defective imitation of
meaningless gestures (e.g., fist under chin) contrasts
with preserved imitation of meaningful
gestures (e.g., hitchhiking) (Goldenberg and
Hagmann, 1997; Salter et al., 2004). A surprising
case of double dissociation from this kind of visuoimitative
apraxia was described in Bartolo et al.
(2001), where the patient showed impairment in
meaningful gesture production (both on imitation
and verbal command) and normal performance in
imitation of meaningless gestures, suggesting that
the patient was able to reproduce only movements
he did not identify or recognize as familiar.
Similarly, the apraxic patients in Buxbaum et al.
(2003) responded abnormally to familiar objects
(e.g., a key, a hammer or a pen) but normally in
recognizing the hand postures appropriate for
novel objects (e.g., parallelepipeds differing in size
and depth). These two studies argue that the
reproduction of a gesture may be constrained by
its degree of familiarity, indicating that current
models of apraxia would need some refinement.
Furthermore, the representation of transitive and
intransitive actions may be dissociable. In Watson
et al. (1986), bilateral apraxia was observed only
for transitive (e.g., hammering) but not intransitive
(e.g., hitchhiking, waving goodbye) movements.2
Whereas transitive gestures are constrained by the
shape, size and function of objects, intransitive
actions are related to socio-cultural contexts
(Cubelli et al., 2000; Heath et al., 2001). The isolated
disturbance of transitive hand movements for
use of, recognition and interaction with an object,
in the presence of preserved intransitive movements,
was named tactile apraxia and usually
appears in the hand contralateral to the lesion
(Binkofski et al., 2001).
As mentioned in the ‘‘Introduction’’, contextual
cues strongly influence the execution of actions.
Some studies have systematically manipulated the
contextual cues in order to assess their relative
importance. For example, patients with impaired
pantomime of motor actions showed no deficit in
the comprehension of the use of tools or in manipulating
the tools (Halsband et al., 2001). Graham
et al. (1999) also observed dramatic facilitation in
the demonstration of tool use when the patient was
given the appropriate or a neutral tool to manip-
ulate.3
Interestingly, the patient could not prevent
himself from performing the action appropriate to
the tool he was holding, rather than the requested
action. In another study however, gesture execution
improved when the object of the action, but not the
tool, was given (Clark et al., 1994). Hence, the
addition of visual and somaesthetic cues may
improve certain aspects of apraxic movements,
since it provides mechanical constraints and supplementary
information that facilitates the selection
of an adequate motor program (Hermsdo¨ rfer et al.,
2006). Nonetheless, there is the case of a patient
that performed much worse when he was actually
manipulating the tool than on verbal command4
(Merians et al., 1999).
Dissociations that concern the nature of the target
were also observed. For example, the left brain
damaged patients in Hermsdo¨ rfer et al. (2003) had
prolonged movement times and reduced maximum
velocities when the movements were directed
2
These patients had lesions in the left supplementary motor
area (SMA).
3
The subject had clinically diagnosed corticobasal degener-
ation.
4
Ibid.
63
toward an allocentric target without visual feedback,
but performed normally when the target was
their own nose. Also, a clear dissociation was found
in Ietswaart et al. (2006) between impaired gesture
imitation and intact motor programming of goaldirected
movements, hence arguing against the
interpretation of impaired imitation as a purely
executional deficit (see ‘‘Models of apraxia’’).
A particular type of apraxia is constructional
apraxia, originally described by Kleist as ‘‘the inability
to do a construction’’ and defined by Benton
as ‘‘the impairment in combinatory or organizing
activity in which details must be clearly perceived
and in which the relationship among the component
parts of the entity must be apprehended’’ (Laeng,
2006). Constructional apraxic patients are unable to
spontaneously draw objects, copy figures and build
blocks or patterns with sticks, following damage
not only to the dominant but also non-dominant
hemisphere. Hence, constructional apraxia appears
to reflect the loss of bilaterally distributed components
for constructive planning and the perceptual
processing of categorical and coordinate spatial
relations (Platz and Mauritz, 1995; Laeng, 2006).
Apraxia can also be observed in mental motor
imagery tasks. Motor imagery is considered as a
means of accessing the mechanisms of action preparation
and imitation, by sharing a common neural
basis (Jeannerod and Decety, 1995). Apraxic
patients were deficient in simulating hand actions
mentally and in imagining the temporal properties
of movements5
(Sirigu et al., 1999). Other apraxic
patients showed a deficit in generating and maintaining
internal models for planning object-related
actions (Buxbaum et al., 2005a). These findings
support the notion that the motor impairments
observed in apraxic patients result from a specific
alteration in their ability to mentally evoke
actions, or to use stored motor representations
for forming mental images of actions.
Apraxia may also be appropriate to reveal the
role of feedback during the execution of a movement.
Some apraxic patients were impaired in
reaching and aiming movements only in the condition
without visual feedback (Ietswaart et al.,
2001, 2006) and performed worse during pointing
with closed eyes (Jacobs et al., 1999; Hermsdo¨ rfer
et al., 2003). Interestingly, the patients in Haaland
et al. (1999) overshot the target when feedback of
the hand was removed and undershot the target
when the feedback of the target was unavailable.
Importantly, these patients continued to rely on
visual feedback during the secondary adjustment
phase of the movement and never achieved normal
end-point accuracy when visual feedback of the
hand position or target location was unavailable.
These findings also suggest that ideomotor limb
apraxia may be associated with the disruption of
the neural representations for the extra-personal
(spatial location) and intra-personal (hand position)
features of movement (Haaland et al., 1999).
The importance of feedback signals was demonstrated
in one of our own apraxic patients
(unpublished data). We reproduced a seminal
study of imitation of meaningless gestures6
by
Goldenberg et al. (2001) on an apraxic patient
with left-parietal ischemic lesion. We observed that
the patient relied heavily on visual and tactile
feedback. He often needed to bring his hand in the
field of vision and corrected the hand posture by
directly comparing it with the displayed stimulus
to imitate. He also used tactile exploration when
searching for the correct spatial position on his
face. He showed many hesitations and extensive
searching which led to highly disturbed kinematic
profiles of the gesture (shown in Fig. 3c, d), but
often correct final postures.
Apraxia can also be defined in relation to the
selectively affected effectors: orofacial apraxia or
buccofacial apraxia, oral apraxia, upper and lower
face apraxia, lid apraxia, limb apraxia, leg apraxia,
trunk apraxia, etc. Oral apraxia, for example, is
defined as the inability to perform mouth actions
such as sucking from a straw or blowing a kiss. It
should not be confounded with apraxia of speech
(also called verbal apraxia), which is a selective
disturbance of the articulation of words (Bizzozero
et al., 2000). Motor planning disorders in children
are denominated developmental dyspraxia (Cermak,
1985). Apraxia can also designate a praxic ability
impaired in an isolated manner such as: gait
5
These patients had posterior parietal lesions.
6
Hand postures relative to the head, an example is shown in
Fig. 3a.
64
apraxia, apraxic agraphia, dressing apraxia, orienting
apraxia and mirror apraxia (i.e., inability to
reach to objects in a mirror (Binkofski et al., 2003)).
When the side of brain lesion and affected hand
are considered, the terms sympathetic and crossed
apraxia are used. Apraxia can sometimes be related
to the specific neural substrate that causes the
disorder, for example following subcortical lesions
in corticobasal degeneration (Pramstaller and
Marsden, 1996; Jacobs et al., 1999; Merians et al.,
1999; Hanna-Pladdy et al., 2001; Leiguarda, 2001)
or following lesions of the corpus callosum (Watson
and Heilman, 1983; Lausberg et al., 1999, 2000;
Goldenberg et al., 2001; Lausberg and Cruz, 2004).
Callosal apraxia for example is particularly appropriate
for disentangling the specific hemispheric
contributions to praxis.
An extensive list of the types of apraxia and
their definitions, including types that were not
mentioned above, can be found in Table 1.
Models of apraxia
Contemporary neuropsychological views of apraxia
arise from Liepmann’s influential work that dates
from more than a hundred years ago. Liepmann
proposed the existence of an idea of the movement,
‘‘movement formulae’’, that contains the ‘‘timespace-form
picture’’ of the action (Rothi et al.,
1991). He believed that in right-handers, these movement
formulae are stored in the left-parietal lobe,
endorsing the view of a left hemispheric dominance
for praxis (Faglioni and Basso, 1985; Leiguarda and
Marsden, 2000). To execute a movement, the spatiotemporal
image of the movement is transformed into
‘‘innervatory patterns’’ that yield ‘‘positioning of the
limbs according to directional ideas’’ (Jacobs et al.,
1999). Liepmann distinguished between three types
of apraxia that correspond to disruptions of specific
components of his model (Faglioni and Basso, 1985;
Goldenberg, 2003). First, a damaged movement formula
(i.e., faulty integration of the elements of an
action) would characterize ‘‘ideational apraxia’’.
Second, failure of the transition from the movement
formula to motor innervation (i.e., inability to translate
a correct idea of the movement into a correct
act) is defined as ‘‘ideomotor apraxia’’. According to
Liepmann, faulty imitation of movements is a purely
executional deficit and proves the separation
between the idea and execution of a movement,
since in imitation the movement formula is defined
by the demonstration (Goldenberg, 1995, 2003;
Goldenberg and Hagmann, 1997). Finally, loss of
purely kinematic (kinaesthetic or innervatory) inherent
memories of an extremity is the ‘‘limb-kinetic’’
variant of apraxia.
Another historically influential model is the
disconnection model of apraxia proposed by
Geschwind (1965). According to this model the verbal
command for the movement is comprehended in
Wernicke’s area and is transferred to the ipsilateral
motor and premotor areas that control the movement
of the right hand (Clark et al., 1994; Leiguarda
and Marsden, 2000). For a left-hand movement, the
information needs to be further transmitted to the
right association cortex via the corpus callosum.
The model postulates that the apraxic disorder
follows from a lesion in the left and right motor
association cortices, or a disruption in their communication
pathways. However this model cannot
explain impaired imitation and impaired object use
since these tasks do not require a verbal command
(Rothi et al., 1991).
Heilman and Rothi (1993) proposed an alternative
representational model of apraxia, according to
which apraxia is a gesture production deficit that
may result from the destruction of the spatiotemporal
representations of learned movements stored
in the left inferior-parietal lobule. They proposed to
distinguish between dysfunction caused by destruction
of the parietal areas (where the spatiotemporal
representations of movements would be encoded),
and the deficit which would result from the disconnection
of these parietal areas from the frontal
motor areas (Heilman et al., 1982). In the first case,
posterior lesions would cause a degraded memory
trace of the movement and patients would not be
able to correctly recognize and discriminate gestures.
In the second case, anterior lesions or disconnections
would only provoke a memory egress
disorder. Therefore patients with a gesture production
deficit with anterior and posterior lesions
should perform differently on tasks of gesture discrimination,
gesture recognition and novel gesture
learning.
65
Table 1. Taxonomy of apraxia
Type of apraxia Definition
Ideational apraxia Initially used to refer to impairment in the conceptual organization of actions, assessed
with sequential use of multiple objects. Later defined as conceptual apraxia.
Conceptual apraxia Impairment in the concept of a single action, characterized by content errors and the
inability to use tools.
Ideomotor apraxia Impairment in the performance of skilled movements, characterized by spatial or
temporal errors in the execution of movements.
Limb-kinetic apraxia Slowness and stiffness of movements with a loss of fine, precise and independent
movement of the fingers.
Constructional apraxia Difficulty in drawing and constructing objects. Impairment in the combinatory or
organizing activity in which details and relationship among the component parts of the
entity must be clearly perceived.
Developmental dyspraxia Disorders affecting the initiation, organization and performance of actions in children.
Modality-specific apraxias Localized within one sensory system.
Pantomime agnosia Normal performance in gesture production tests both on imitation and on verbal
command, but poor performance in gesture discrimination and comprehension. Patients
with pantomime agnosia can imitate pantomimes they cannot recognize.
Conduction apraxia Superior performance on pantomime to verbal command than on pantomime imitation.
Visuo-imitative apraxia Normal performance on verbal command with selectively impaired imitation of gestures.
Also used to designate the defective imitation of meaningless gestures combined with
preserved imitation of meaningful gestures.
Optical (or visuomotor) apraxia Disruptions to actions calling upon underlying visual support.
Tactile apraxia Disturbance of transitive hand movements for use of, recognition and interaction with
an object, in the presence of preserved intransitive movements.
Effector-specific apraxias
Upper/lower face apraxia Impairment in performing actions with parts of the face.
Oral apraxia Inability to perform skilled movements with the lips, cheeks and tongue.
Orofacial (or buccofacial) apraxia Difficulties with performing intentional movements with facial structures including the
cheeks, lips, tongue and eyebrows.
Lid apraxia Difficulty with opening the eyelids.
Ocular apraxia Impairment in performing saccadic eye movements on command.
Limb apraxia Used to refer to ideomotor apraxia of the limbs frequently including the hands and
fingers.
Trunk (or axial) apraxia Difficulty with generating body postures.
Leg apraxia Difficulty with performing intentional movements with the lower limbs.
Task-specific apraxias
Gait apraxia Impaired ability to execute the highly practised, co-ordinated movements of the lower
legs required for walking.
Gaze apraxia Difficulty in directing gaze.
Apraxia of speech (or verbal apraxia) Disturbances of word articulation.
Apraxic agraphia A condition in which motor writing is impaired but limb praxis and non-motor writing
(typing, anagram letters) are preserved.
Dressing apraxia Inability to perform the relatively complex task of dressing.
Dyssynchronous apraxia Failure to combine simultaneous preprogrammed movements.
Orienting apraxia Difficulty in orienting one’s body with reference to other objects.
Mirror apraxia A deficit in reaching to objects presented in a mirror.
Lesion-specific apraxias
Callosal apraxia Apraxia caused by damage to the anterior corpus callosum that usually affects the left
limb.
Sympathetic apraxia Apraxia of the left limb due to damage to the anterior left hemisphere (the right hand
being partially or fully paralyzed).
Crossed apraxia The unexpected pattern of apraxia of the right limb following damage to the right-
hemisphere.
66
Roy and Square (1985) proposed a cognitive
model of limb praxis that involves two systems,
i.e., a conceptual system and a production system
(illustrated in Fig. 1). The ‘‘conceptual system’’
provides an abstract representation of the action
and comprises three kinds of knowledge: (1)
knowledge of the functions of tools and objects,
(2) knowledge of actions independent of tools and
objects and (3) knowledge about the organization
of single actions into sequences. The ‘‘production
system’’ incorporates a sensorimotor representation
of the action and mechanisms for movement
control. Empirical support for the division of the
praxis system into a conceptual and a production
component is provided by a patient who could
comprehend and discriminate transitive gestures
she was unable to perform (Rapcsak et al., 1995).
This model predicts three patterns of impairment
(Heath et al., 2001). First, a deficit in pantomime
but not in imitation would reflect damage to the
selection and/or evocation of actions from longterm
memory. Second, a deficit in imitation alone
would indicate a disruption of the visual gestural
analysis or translation of visual information into
movement. Finally, concurrent impairment in
pantomime and imitation is thought to reflect a
disturbance at the latter, executive stage of gesture
production and was the most frequent deficit
pattern observed in Roy et al. (2000) and Parakh
et al. (2004).
None of these models predict a number of
modality-specific dissociations observed in neurologically
impaired patients, such as preserved gesture
execution on verbal command that is impaired
in the visual modality when imitating (Ochipa et al.,
1994; Goldenberg and Hagmann, 1997). To
account for these dissociations, Rothi et al. (1991)
proposed a cognitive neuropsychological model of
limb praxis, which reflects more appropriately the
complexity of human praxis (illustrated in Fig. 2a).
This multi-modular model has input that is selective
according to the modality, a specific ‘‘action semantics
system’’ dissociable from other semantics
systems, an ‘‘action reception lexicon’’ that communicates
with an ‘‘action production lexicon’’ and
a separate ‘‘nonlexical route’’ for the imitation of
novel and meaningless gestures7
(Rothi et al., 1997).
Although this model is widely used to explain
data from multiple neurological studies, it has
difficulties concerning several aspects. First, it does
not consider the existence of a selective tactile
route to transitive actions (Graham et al., 1999).
For example, the model fails to explain data from
a patient profoundly impaired in gesturing in the
verbal and visual modalities, but not with the tool
in hand (Buxbaum et al., 2000). Second, imitation
of meaningless gestures is assumed to test the
integrity of a direct route from visual perception to
motor control. However, Goldenberg et al. (1996)
have shown that this route is far from direct and
involves complex intermediate processing steps.
For example, apraxic patients that are impaired in
reproducing gestures on their own bodies are also
impaired in replicating the gestures on a life-sized
manikin (Goldenberg, 1995). Hence, general
conceptual knowledge about the human body
and the spatial configuration of body parts seems
necessary for performing an imitation task
(Goldenberg, 1995; Goldenberg et al., 1996;
Conceptual System
Abstract knowledge of Action:
Knowledge of Object Function
Knowledge of Action
Knowledge of Serial Order
Production System
Knowledge of Action in Sensorimotor Form:
Attention at Key Points
Action Programs
Mechanisms for Movement Control
Environment
Muscle Collectives
Fig. 1. Roy and Square’s cognitive model of limb praxis.
Adapted with permission from Roy and Square (1985).
7
The vocabulary was borrowed from the literature of language
processing.
67
Auditory Analysis
Auditory/Verbal
Input
Visual Object
Input
Visual Gestural
Input
Phonological Input
Lexicon
Visual Analysis Visual Analysis
Object Recognition
System
Action Input
Lexicon
Action Semantics
Action Output
Lexicon
Innervatory Patterns
Visual Analysis
Action Input
Lexicon
Action Semantics
Action Output
Lexicon
Gestural Buffer
Visuo-Motor
Conversion
Mechanism
(a)
(b)
(c)
Spatiomotor transformations
from retinotopic to 'intrinsic'
body-centered coding
Dynamic model of body
coded in 'intrinsic' spatial
coordinates (body schema)
Stored portion of
gesture
representation
Knowledge of tools'
characteristic
movements
Motor Output
Visual Analysis
Object Recognition
System
Fig. 2. A cognitive neuropsychological model of limb praxis. The three components on the right are interchangeable with the empty
box in the complete model on the left. Under (a) Rothi et al.’s original model of limb praxis. Under (b) the previous model revised by
Cubelli et al. and under (c) the model extended by Buxbaum et al. For a detailed description see the text. Adapted respectively with
permission from Rothi et al. (1997), Cubelli et al. (2000) and Buxbaum et al. (2000).
68
Goldenberg and Hagmann, 1997). The belief that
imitation is a rather simple and straightforward
visuomotor process is misleading as one would
have to resolve the ‘‘body correspondence prob-
lem’’8
to transpose movements from bodies with
different sizes and different owners, which are in
addition represented in different perspectives
(Goldenberg, 1995).
To account for the last observation, Cubelli et al.
(2000) have revised Rothi et al.’s cognitive neuropsychological
model of limb praxis (illustrated in
Fig. 2b). They have added ‘‘a visuomotor conversion
mechanism’’ devoted to transcoding the visual input
into appropriate motor programs. They have also
suppressed the direct link between the ‘‘input’’ and
‘‘output action lexicon’’, leaving only an indirect link
through the ‘‘action semantics system’’, as no empirical
evidence was found of a patient able to reproduce
familiar gestures with obscure meaning, but
not unfamiliar gestures (see Fig. 2a, b). Finally, they
have also added a ‘‘gestural buffer’’ aimed at holding
a short-term representation of the whole action. The
model predicts five different clinical pictures (for
definitions of the different apraxic disorders please
refer to Table 1): (1) a deficit of the ‘‘action input
lexicon’’: pantomime agnosia (i.e., a difficulty in the
discrimination and comprehension of gestures), (2) a
deficit of the ‘‘action semantics system’’: conceptual
apraxia without ideomotor apraxia, (3) a deficit of
the ‘‘action output lexicon’’: conceptual apraxia with
spared gesture-meaning associations, (4) a deficit of
the ‘‘visuomotor conversion mechanism’’: conduction
apraxia (not observed in their study) and (5) a
deficit of the ‘‘gestural buffer’’: both ideomotor and
ideational apraxia (i.e., impairment in all execution
tasks with preserved ability to perform judgment
and categorization tasks).
Buxbaum et al. (2000) further extended Rothi
et al.’s cognitive neuropsychological model of limb
praxis, based on their observation of a patient who
performed particularly poorly on tasks that required
a spatial transformation of the body. According to
their model (illustrated in Fig. 2c), a unitary set of
representations named ‘‘body schema’’ calculates
and updates the dynamic positions of the body parts
relative to one another. Importantly, this dynamic
body-centered representation of actions is a common
processing stage between the ‘‘lexical’’ and ‘‘nonlexical
route’’ and hence subserves both meaningful
and meaningless actions. Note that at the level of the
‘‘lexical route’’, there is an additional interaction
with the stored representations of learned actions.
Existing models of apraxia still fail to account for
additional empirical evidence such as, for example,
the differential performance in imitation of hand
postures and imitation of finger configurations
shown in Goldenberg and Hagmann (1997) and
Goldenberg and Karnath (2006). Furthermore, in a
study of ideomotor apraxia, Buxbaum et al. (2005b)
provided data which is compatible with the influential
‘‘mirror neuron hypothesis’’. Apraxia models
cannot easily be reconciled with this hypothesis
which, based upon neurophysiological observations
from the monkey brain, postulates a ‘‘mirror neuron
system’’ underlying both action recognition and
action execution (Rizzolatti and Craighero, 2004).
Mirror neurons are a special class of visuomotor
neurons, initially discovered in area F5 of the monkey
premotor cortex (see Fig. 4), which discharge
both when the monkey does a particular action and
when it observes another individual doing a similar
action (Gallese et al., 1996; Rizzolatti and Luppino,
2001; Rizzolatti et al., 2002). Hence, the ‘‘mirror
neuron system’’ is believed to map observed actions
onto the same neural substrate used to execute these
actions. As the same representations appear to subserve
both action recognition and action production
tasks, it would not be surprising if the
perception of a movement is constrained by its executional
knowledge. Related to apraxia, the ‘‘mirror
neuron hypothesis’’ questions the separation of
the ‘‘input’’ and ‘‘output lexicon’’ (Koski et al.,
2002).
Contributions of the left- and right-brain
hemispheres
Although most apraxia studies show a left-brain
hemisphere dominance for praxis, the studies
8
Here we give a shortened version of the informal statement
of the body correspondence problem. Given an observed behavior
of the model, i.e., a sequence (or hierarchy) of subgoals,
find and execute a sequence of actions using one’s own (possibly
dissimilar) embodiment which leads through the corresponding
subgoals (Nehaniv and Dautenhahn, 2002).
69
arguing for a significant involvement of the right
hemisphere are numerous. Left-brain damage
usually affects both hands, whereas right-brain
damage affects only the left hand, suggesting that
the left hemisphere is not only fully competent for
processing movement concepts but also contributes
to the generation of movements in the right hemisphere.
Apraxic deficits following left hemisphere
lesions are also more frequent (De Renzi et al.,
1980; Weiss et al., 2001); however, in some rare
cases, severe apraxia was observed following right
hemisphere lesions (Marchetti and Sala, 1997;
Raymer et al., 1999). The concept of crossed
apraxia was introduced to describe patients with
this opposite pattern of limb apraxia that cannot
be explained by handedness. Callosal lesions are
most suitable for investigating the issues of hemispheric
specialization of praxis. For example,
split-brain patients were apraxic with their left
hands, also suggesting a left hemisphere dominance
for processing skilled movement (Watson
and Heilman, 1983; Lausberg et al., 1999, 2003),
but both hemispheres appeared to contain concepts
for skill acquisition (Lausberg et al., 1999)
and object use (Lausberg et al., 2003).
In kinematic studies (described in more detail in
‘‘The analysis of apraxic errors’’), only left-brain
damaged patients were impaired in imitation of
meaningless movements (Hermsdo¨ rfer et al., 1996;
Weiss et al., 2001), as well as in pointing movements
(Hermsdo¨ rfer et al., 2003); whereas right-brain
damaged patients had deficits in slow-paced tapping
and initiation of aiming movements (Haaland
and Harrington, 1996). Hence, the left hemisphere
was associated with movement trajectory control
(Haaland et al., 2004), sequencing and ballistic
movements (Hermsdo¨ rfer et al., 2003) and the right
hemisphere was related to on-line control of the
movement (Hermsdo¨ rfer et al., 2003) and closedloop
processing (Haaland and Harrington, 1996).
A left–right dichotomy was also observed for
imitation and matching of hand and finger configurations
(Goldenberg, 1999). Left-brain damaged
patients had more difficulties with imitation than
matching and vice versa. In addition, the left hemisphere
seemed fully competent for processing hand
postures, but needed the right hemisphere’s contribution
for processing finger postures (Goldenberg
et al., 2001; Sala et al., 2006a). It was concluded that
the left hemisphere mediates conceptual knowledge
about the structure of the human body and that the
right hemisphere is specialized for visually analyzing
the gesture (Goldenberg, 2001; Goldenberg et al.,
2001).
Finally, several studies observed similar impairment
scores following left- and right-brain lesions,
arguing for a bi-hemispheric representation of
skilled movement (Haaland and Flaherty, 1984;
Kertesz and Ferro, 1984; Roy et al., 1992, 2000;
Heath et al., 2001). The less frequent, nevertheless
well-detected incidence of limb apraxia following
right-brain lesion, was attributed to the sensitivity
and precision of the assessment methodology.
In addition, right-hemisphere lesions often led to
severe face apraxia (Bizzozero et al., 2000; Sala
et al., 2006b). Hence, a model of widespread praxis,
distributed across both hemispheres, may be more
appropriate than the unique left-lateralized center
previously hypothesized. Moreover, it seems that
the degree of left-hemisphere dominance varies
within subjects and with the type of movement
(Haaland et al., 2004), raising the issue of overlap
between the contributions of the right and left
hemispheres to specialized praxic functions.
Intra-hemispheric lesion location: a distributed
representation of praxis?
Several studies have failed to find a consistent
association between the locus of the lesion within
a hemisphere and the severity of apraxia (Basso
et al., 1980; Kertesz and Ferro, 1984; Alexander
et al., 1992; Schnider et al., 1997; Hermsdo¨ rfer et al.,
2003). Moreover, areas involved in apraxia can also
be damaged in non-apraxic patients (Haaland et al.,
1999; Buxbaum et al., 2003). However, apraxic
deficits are most frequent following parietal and
frontal lesions, but were also observed in patients
with temporal, occipital and subcortical damages
(De Renzi and Lucchelli, 1988; Goldenberg, 1995;
Hermsdo¨ rfer et al., 1996; Bizzozero et al., 2000).
More specifically, ideomotor apraxia and motor
imagery deficits were observed following lesions in
the left inferior parietal and the left dorsolateral
frontal lobes (Haaland et al., 2000; Buxbaum et al.,
70
2005a). For example, several studies suggested that
Brodmann areas 39 and 40 (i.e., angular and supramarginal
gyri of the inferior-parietal lobule) are
critical in visuo-imitative apraxia (Goldenberg and
Hagmann, 1997; Goldenberg, 2001) and ideomotor
limb apraxia (Haaland et al., 1999; Buxbaum et al.,
2003). In addition, the superior-parietal lobe
appeared crucial in integrating external visual and
intra-personal somaesthisic information (Heilman
et al., 1986; Haaland et al., 1999). Goldenberg and
Karnath (2006), subtracted the lesion overlay of
unimpaired from impaired patients and associated
disturbed imitation of hand postures with lesions in
the inferior-parietal lobe and temporo–parieto–
occipital junction, whereas disturbed imitation of
finger postures could be related to lesions in the
inferior frontal gyrus. Interestingly, parts of the
middle and inferior frontal gyri, in the vicinity of
Brodmann areas 6, 8 and 46, were involved in all of
the ideomotor apraxics in Haaland et al. (1999).
Furthermore, premotor lesions (including lesions to
the supplementary motor area) particularly affected
bimanual actions in Halsband et al. (2001) and
transitive actions in Watson et al. (1986).
It has been difficult to disentangle between the
specific contributions of the parietal and the frontal
cortices, as lesions in these areas lead to similar
deficits (Haaland et al., 1999, 2000). For example,
target and spatial errors were related to posterior
lesions only (Haaland et al., 2000; Halsband et al.,
2001; Weiss et al., 2001; Goldenberg and Karnath,
2006), but internal hand configuration errors were
present in patients with anterior and posterior
lesions (Haaland et al., 2000; Goldenberg and
Karnath, 2006). Importantly, only patients with
posterior lesions, and not anterior lesions, had
difficulties in discriminating between correctly
and incorrectly performed actions and in recognizing
pantomimes or appropriate hand postures
(Halsband et al., 2001; Buxbaum et al., 2005b).
Apraxia can also develop following subcortical
lesions (Pramstaller and Marsden, 1996; Graham
et al., 1999; Jacobs et al., 1999; Merians et al., 1999;
Hanna-Pladdy et al., 2001). In this case, it is not
clear whether the apraxia originates from lesions in
the basal ganglia, which are extensively connected
to the superior-parietal lobe and premotor and
supplementary motor areas (Jacobs et al., 1999;
Merians et al., 1999), or from the surrounding
white matter (i.e., fronto-parietal connections)
(Pramstaller and Marsden, 1996).
Failure to find clear correlations between specific
lesion loci and different apraxic deficits argues
for a widespread cortical and subcortical representation
of praxis, distributed across specialized
neural systems working in concert (Leiguarda and
Marsden, 2000; Hermsdo¨ rfer et al., 2003). However,
we believe that a selective damage to one of
these systems may produce a particular pattern of
errors tightly related to a subtype of apraxia.
Praxis and language?
Apraxia is most often seen in association with aphasia
(i.e., loss of the ability to speak or understand
speech), which renders the assessment of apraxia
very difficult. Indeed, one has to provide evidence
that the patient has understood the commands so
that the motor deficit cannot be attributed to aphasia
(De Renzi et al., 1980). Historically, gestural
disturbance in aphasics was considered to be a manifestation
of damaged abstract knowledge. This idea
of a common impaired symbolic function underlying
aphasia and apraxia was supported for a long
time (Kertesz and Hooper, 1982). However, several
large-scale studies failed to find correlations between
subtypes of apraxia and aphasia (Goodglass and
Kaplan, 1963; Lehmkuhl et al., 1983; Buxbaum
et al., 2005b). Moreover, clear evidence of a double
dissociation between apraxia and aphasia was presented
in Papagno et al. (1993). For example, some
patients were able to verbalize a desired movement
but could not perform it (Goodglass and Kaplan,
1963), whereas other patients were able to pantomime
actions they were unable to name (Rothi et al.,
1991). Hence, it seems that many aspects of language
and praxis are subserved by independent, possibly
contiguous neuronal processes, but concomitant
deficits may also appear because of shared neuroanatomical
substrates (Kertesz and Hooper, 1982).
Nevertheless, the question of how language is related
to praxis is a fascinating one and needs further
study, as it can give some insight into the existence
of a supramodal representation of knowledge, or
alternatively shed light onto the communication
71
mechanisms between the praxic- and languagespecific
representations of knowledge.9
The analysis of apraxic errors
There are extensive quantitative analyses of the severity
of apraxic errors in single case studies and in
large samples of brain-damaged patients. Qualitative
analyses however are less numerous and nonstandardized,
but nonetheless essential for precisely
understanding the nature of apraxia. Performances
are usually classified in a limited number of response
categories such as:10
temporal errors, spatial
errors, content errors, substitutive errors, augmentative
errors, fragmentary errors, associative errors
(i.e., the correct movement is replaced by another
movement that shares one feature), parapraxic errors
(i.e., correct execution of a wrong movement),
wrong body part errors (e.g., patients that execute a
correct movement with the head instead of the
hand), body part as tool errors (i.e., a body part is
used to represent the imagined tool) and perseveration
errors (Lehmkuhl et al., 1983; Poeck, 1983;
De Renzi and Lucchelli, 1988; Platz and Mauritz,
1995; Lausberg et al., 1999, 2003; Halsband et al.,
2001; Weiss et al., 2001). Perseveration and body
parts as tool errors should be accorded some special
interest in future studies, as they are prominent in
apraxia and their occurrence is far from being elucidated
(Poeck, 1983; Raymer et al., 1997; Lausberg
et al., 2003). For example, even though normal
subjects also commit body part as tool errors,11
only subjects with brain lesion cannot correct their
error after re-instruction (Raymer et al., 1997).
A significant step forward in the analysis of apraxic
errors was the use of quantitative 3D
kinematic motion analysis. These techniques allowed
to show many abnormalities in the kinematic
features of apraxic movements such as:
deficits in spatial accuracy, irregular velocity profiles,
reduced maximum velocities, reduced movement
amplitudes, de-coupling of the relationship
between instantaneous wrist velocity and trajectory
curvature, improper linearity of the movement,
wrong orientation of the movement in space and/or
deficient joint coordination (Poizner et al., 1990,
1995, 1997; Clark et al., 1994; Platz and Mauritz,
1995; Rapcsak et al., 1995; Merians et al., 1997,
1999; Haaland et al., 1999; Binkofski et al., 2001;
Hermsdo¨ rfer et al., 2006). An example of an apraxic
movement with abnormal kinematics is shown
in Fig. 3. Based on kinematic studies it could be
concluded that ideomotor limb apraxia impaired
the response implementation but not the preprogramming
of the movement (Haaland et al., 1999)
and decoupled the spatial and temporal representations
of the movement (Poizner et al., 1990,
1995). Importantly, the kinematic abnormalities
observed were often spatial and not temporal, the
longer movement times in the apraxic group could
be interpreted as an artifact of the longer distance
traveled (Haaland et al., 1999; Hermsdo¨ rfer et al.,
2006). However, several authors have advised
against systematically interpreting the irregular
kinematics as an indicator for deficient motor programming
or deficient motor implementation
(Platz and Mauritz, 1995; Haaland et al., 1999).
For example, no correlation could be found between
the kinematic abnormalities and apraxic
errors in Hermsdo¨ rfer et al. (1996). Indeed, movements
with degraded kinematics frequently reached
a correct final position, while, on the contrary,
kinematically normal movements often led to
apraxic errors. The abnormal kinematic profile of
the gesture probably arose from several corrective
and compensatory strategies that the patient used
to cope with the apraxic deficit (Goldenberg et al.,
1996; Hermsdo¨ rfer et al., 1996). For example, hesitant
and on-line controlled movements generated
multi-peaked velocity profiles in our study (see
Fig. 3d). Hence, according to the authors, the basic
deficit underlying apraxia may concern the mental
representation of the target position. Consistently
with this hypothesis, it was found that apraxic
9
Some authors have posited that an actionÀrecognition
mechanism might be at the basis of language development
(Rizzolatti and Arbib, 1998).
10
This list is not extensive. Terminologies can vary a lot
across different authors.
11
There is a hierarchical organization in the performance of
actions with increasing difficulty. Children first acquire the
ability to actually use objects, then to demonstrate the action
with similar substitute objects, then with dissimilar substitute
objects, then to use body parts as substitutes, and finally to
perform pantomimes with holding imagined objects. This note
was taken from Lausberg et al. (2003).
72
patients relied more than normal subjects on
on-line visual information in aiming movements
(Ietswaart et al., 2006).
Discussion
We have shown in the preceding sections that
apraxia has proven very difficult to assess and
understand. Here we will try to provide some
hypotheses on why these difficulties might arise
and we propose several ways to overcome these.
The complex nature of apraxia
Apraxia designates the impairment of the human
praxis system following brain lesion and has to
deal with the high complexity and wide range of
human praxic functions. Therefore studies of
Patient Matched normal subject
0
2
4
6
8
10
12
Time(s)
0 1 2 3 4 5 6 7 8
30
40
50
60
70
80
90
100
110
120
Shoulderflexionextension(degrees)
Time (s)
patient
matched normal subject
0 2 4 6 8
0
0.5
1
1.5
2
Time (s)
HandVelocity(m/s2) patient
matched normal subject
(a)
(b)
(c)
(d)
Fig. 3. An example of the abnormal kinematics of an apraxic movement. A patient with left ischemic lesions was tested in a study of
imitation of meaningless gestures. The stimulus to imitate for this movement is shown under (a) and represents a hand posture relative
to the head. Under (b), the movement times of the patient are longer than those of a matched normal subject (including replacement of
the hand in the initial condition). Under (c), the trajectory of the shoulder flexion-extension joint angle of the patient (shown in solid
line) contains several irregularities, which are the result from multiple hesitations and changes of directions, whereas the matched
normal subject shoulder flexion-extension trajectory (dashed line) is smooth. The speed profile of the patient (solid line) is shown under
(d) and contains multiple peaks with reduced maximum velocities that contrast with the simple bell-shaped velocity profile of the
matched normal subject (dashed line).
73
apraxia have separately tackled the faulty execution
of many types of gestures (e.g., transitive and
intransitive, meaningful and meaningless, peripersonal
and body-centered, etc.) of various endeffectors
(e.g., mouth, face, leg, limb) in different
types of modalities (e.g., visual, auditive, tactile
presentation and imitation). The high dimensionality
of varying parameters has led to a lack of
systematicity in the apraxia assessment and terminologies
used. This has also rendered the coherent
interpretation of the disorder rather arduous.
It follows that there is a great need to discriminate
between different types of actions, as they
appear to be differentially impaired in apraxia and
hence may involve distinct underlying mechanisms
(see ‘‘Types of apraxia’’). Indeed, it is very likely
that the mechanisms of imitation and execution of
movements vary according to the type of action
that is imitated or executed (Schnider et al., 1997;
Goldenberg, 1999; Goldenberg and Karnath,
2006). This suggests that different categories of
actions require the use of separate systems at some
stage of processing, but the level of separation
between the representations underlying actions of
different types, or even different actions of the
same type, is not at all clear yet.
We will principally argue that it is important to
better understand what a particular gesture or
execution modality implies in terms of brain
resources and brain processes when compared to
another gesture/execution modality. For example,
a transitive action, i.e., an action that involves an
object, is very different from an intransitive action
in the sense that it provides supplementary tactile
input as a result from the interaction with the
object. This tactile sensory input then needs to be
integrated to the representation of the action that
relies also on other types of sensory inputs such as
visual and proprioceptive. Moreover, executing a
transitive action in a pantomime condition is also
different from executing it with the object in hand,
since the action has to be retrieved without the
help of tactile input produced by the object.
Indeed the movement is somehow modified, for
example movement amplitudes in normal subjects
were larger in the pantomime condition when
compared to actual sawing (Hermsdo¨ rfer et al.,
2006).
The distinction between meaningful and meaningless
gestures would also need some clarification.
The reproduction of a recognized meaningful gesture
on the one hand, appears entirely based on the
internal representation of the gesture. Indeed, the
knowledge of a learned skilled act is preferably
retrieved from motor memory rather than being
constructed de novo (Halsband et al., 2001). On the
other hand, the reproduction of a meaningless gesture
involves a close visual tracking of the imitatee’s
body configuration and was modeled by a ‘‘visuomotor
conversion mechanism’’ or a ‘‘body schema’’
(see Fig. 2b, c). To summarize, a meaningful gesture
seems to be, to a certain extent, assimilated to a
goal that guides the action from memory, whereas a
meaningless gesture is defined as a particular configuration
of the body in space and time, with no
external referents (Goldenberg, 2001). Hence, imitation
of meaningless gestures might be used to test
the comprehension and replication of changing relationships
between the multiple parts and subdivisions
of the refined and complex mechanical device,
which is the human body (Goldenberg, 2001).
Furthermore, a preserved imitation of meaningless
gestures is crucial for the apraxic patient as it might
be useful for relearning motor skills. The double
dissociation observed between imitation of meaningless
and meaningful gestures argues for completely
separate processing systems, and is still not
accounted for by any of the existing apraxia models
previously described. However, meaningless actions
involve novel motor sequences that must be analyzed
and constructed from the existing movements
(Koski et al., 2002) and both meaningless and
meaningful gestures appear to engage the body
schema, i.e., a dynamic model for coding the body
(Buxbaum et al., 2000). Hence, meaningless and
meaningful actions may also share some overlapping
conceptual representations.
These examples show that there are some common
and some distinct processes involved in the
different types of movements and modalities used
for testing apraxia. Identifying the overlap of these
processes would provide a clearer framework for
interpreting the patient’s performance and would
simplify the analysis of the lesion correlates. The
choice of the testing condition is crucial, as well as
identifying the processes inherent to the chosen
74
condition. However this is a difficult task, since
correlations can be found between some very
different and even dissociated types of move-
ments.12
For example, kinematic measures of
pointing movements were correlated to gesture
imitation, suggesting that the kinematic deficits
observed during pointing movements are generalized
to more global aiming movements, including
movements for imitating hand gestures
(Hermsdo¨ rfer et al., 2003). Accordingly, gesture
imitation is believed to depend upon some of the
same cognitive mechanisms as reaching and grasping
(Haaland et al., 2000), however the level and
extent of interplay is not clear. To make the
picture even more complex, the underlying representations
may be componential, for example with
separate hand posture representations for transitive
gestures (Buxbaum et al., 2005b). This leads us
to two questions that urge to be answered: (1)
What are the basic motor primitives from which
all movements are constructed? and (2) Which are
the motor components that are related to specific
movements?
Beyond the complex nature of apraxia
One way to cope with the complex nature of
apraxia is to be even more precise and systematic
in assessing the apraxic disorder. Ideally, the full
range of praxic functions, related to different
effectors, including mouth, face and foot should be
tested in a complete set of modalities (Koski et al.,
2002). Moreover, we find it unfortunate that qualitative
measures of the errors, such as kinematic
measures of the movement trajectory (refer to
‘‘The analysis of apraxic errors’’), are frequently
missing or given in a purely statistical fashion (e.g.,
25% of errors in Condition A). As such, these
measures do not suffice to understand why the
patient succeeds at the execution of some actions,
but not other similar actions. For example, in one
study the patient was able to evoke some actions
(using a razor and a comb) fairly consistently, yet
others (hammering and writing) were never
produced (Graham et al., 1999). In another study,
the same gestures were not always congruently
disturbed across the different modes of execution,
namely on imitation and on verbal command
(Jacobs et al., 1999). We believe that it is this
inability to distinguish between different types of
errors related to different types of gestures that has
prevented us so far from discovering the precise
neuroanatomical correlates of apraxia, on top of
the difficulty to accurately identify the brain lesion.
Hence, the typology and analysis of apraxic
errors need to be improved. We encourage extensive
categorization of the errors and their characterization
via kinematic methods. In addition, the
errors should be reported in relation to the exact
movement and not only specific condition tested.
We also suggest that studies that assess apraxia
should more often integrate tasks of motor learning,
as patients with apraxia may also be deficient
in learning new motor tasks (Heilman et al., 1975;
Rothi and Heilman, 1984; Platz and Mauritz,
1995; Lausberg et al., 1999). The main motivation
in understanding apraxia is to help the apraxic
patients in their everyday lives through the development
of efficient rehabilitation methods and
training programs.13
Assessing the exact expression
of the apraxic deficit, and especially the
patient’s motor learning abilities, would help to
choose an appropriate therapy for the patient.
Efficiently targeting the movements and praxis
components specifically affected in each patient
would accelerate the process of improving his or
her praxic faculties. For the moment, apraxia in
relation to motor learning is an under-investigated
line of research.
Furthermore, we believe that modeling research
may prove very helpful to gain some insight into
the details and potential implementation of the
processes underlying human praxis. When a
roboticist searches for an algorithm for his robot
to manipulate objects, he or she has to provide
with all the different input signals and implement
in practice all the necessary computations and
12
Surprisingly, single finger tapping was a better predictor of
the severity of apraxia than goal-directed grasping and aiming
(Ietswaart et al., 2006). Single finger tapping is almost never
used to assess apraxia.
13
According to Platz and Mauritz (1995), only patients with
ideomotor apraxia and not ideational and constructional apraxia
could benefit from a task-specific sensorimotor training.
75
processing resources. For example, the differences
and similarities between reaching to body-centered
versus peripersonal cues would become evident
through the development of corresponding
algorithms, as they would be explicitly computed.
According to Schaal and Schweighofer (2005),
computational models of motor control in humans
and robots often provide solid foundations that
can help us to ground the vast amount of neuroscientific
data that is collected today. Thus,
biologically inspired modeling studies such as
Sauser and Billard (2006) and Hersch and Billard
(2006) seem to be very promising approaches in
the understanding of the nature of gestures and
in emphasizing the differences and similarities of
their underlying processes.
Although neuropsychological models are essential
for the understanding of apraxia, they do not
address the question of the precise neural representation
of the action and how this representation
can be accessed. In a neurocomputational model,
one has to take into account the computational
principles of movement that reproduce the behavioral
and kinematic results of the patient, as
well as propose a biologically plausible implementation
of the black-box components of apraxia
models. In this view, we have a developed a
simple neurocomputational model described in
Petreska and Billard (2006), that accounts for
the callosal apraxic deficit observed in a seminal
experimental study of imitation of meaningless
gestures (Goldenberg et al., 2001). Our model combines
two computational methods for unsupervised
learning applied to a series of artificial neural networks.
The biologically inspired and distributed
representations of sensory inputs self-organize according
to Kohonen’s algorithm (Kohonen, 2001)
and associate with antihebbian learning (Gerstner
and Kistler, 2002). The appropriate transformations
between sensory inputs needed to reproduce
certain gestures are thus learned within a biologically
plausible framework. It is also possible to impair
the networks in a way that accounts for the
performance of Goldenberg et al.’s apraxic patient
in all of the conditions of the study. The model also
suggests potential neuroanatomical substrates for
this task. We believe that the development of neurocomputational
models is a good way to probe our
understanding of apraxia and is compatible with
the view of integrating knowledge from different
lines of research, a point that we will defend in the
following section.
Toward a multidisciplinary approach
We believe that apraxia can be best dismantled by
adopting a multidisciplinary approach. Future
models of apraxia will need to encompass knowledge
and data from studies of normal human motor
control, human brain imaging and monkey brain
neurophysiology. Fortunately, several authors have
already attempted to combine different sources of
evidence: by considering apraxia in the neurophysiological
framework (e.g., Leiguarda and Marsden,
2000) or by validating a model of apraxia using
neuroimaging methods (e.g., Hermsdo¨ rfer et al.,
2001; Peigneux et al., 2004; Chaminade et al., 2005;
Mu¨ hlau et al., 2005).
Normal human motor control has been extensively
studied via behavioral, psychophysical, kinematic
or computational methods for decades,
giving rise to several principles of movement, such
as: spatial control of arm movements (Morasso,
1981), maps of convergent force fields (Bizzi et al.,
1991), uncontrolled manifold concepts (Scholz
and Scho¨ ner, 1999), t-coupling in the perceptual
guidance of movements (Lee et al., 1999) and
inverse and forward internal models (Wolpert and
Ghahramani, 2000). Studies of motor control have
also inspired several models for reaching like: minimum
jerk trajectory control (Flash and Hogan,
1985), vector-integration-to-endpoint model (Bullock
and Grossberg, 1988), minimum torque change
model (Uno et al., 1989) and stochastic optimal
feedback control (Todorov and Jordan, 2002)
(for a review refer to Desmurget et al. (1998)). Proposed
models for grasping (e.g., schema design
(Oztop and Arbib, 2002)) are reviewed in Jeannerod
et al. (1995) and models for sensorimotor learning
(such as the modular selection and identification
for control model (Haruno et al., 2001)) in Wolpert
et al. (2001). In addition, it was also shown that the
amplitude and direction of pointing movements
may be independently processed (Vindras et al.,
2005) or that the kinematics and dynamics for
76
reaching may be separately learned (Krakauer
et al., 1999). Investigation of apraxia can only
benefit from taking into account the rich knowledge
of the computational processes of movement used
by the brain; and obviously, apraxia models would
need to be compatible with the current general
theories of movement control.
Progress in describing the contribution of specific
brain regions to human praxis through the study of
brain-damaged patients has been limited by the variability
in the size, location and structures affected
by the lesion (Koski et al., 2002). Human brain imaging
studies, particularly positron emission tomography
(PET) and functional magnetic resonance
(fMRI) overcome this difficulty to a certain extent
and have an essential role in resolving the neuroanatomical
correlates of human functions. Despite the
evident difficulties and limitations to study movements
with neuroimaging, numerous studies have
addressed the question of the representation of human
praxis, making significant contributions to the
understanding of the neural substrates underlying
visuomotor control (for a review see Culham et al.
(2006)). In order to give an idea of the number of
praxis functions that have been addressed with brain
imaging technologies, we will mention some of
them: observation of meaningful and meaningless
actions with the intent to recognize or imitate
(Decety et al., 1997), hand imitation (Krams et al.,
1998), visually guided reaching (Kertzman et al.,
1997; Desmurget et al., 1999; Grefkes et al., 2004),
object manipulation and tool-use (Binkofski et al.,
1999; Johnson-Frey et al., 2005), real and/or imagined
pantomimes (Moll et al., 2000; Choi et al.,
2001; Rumiati et al., 2004) and sequential organization
of actions (Ruby et al., 2002). The areas specialized
for the perception of body parts and
postures have been consistently identified14
(Peigneux et al., 2000; Downing et al., 2001). Most
importantly, several brain imaging studies have been
conducted in relation to apraxia (Hermsdo¨ rfer et al.,
2001; Peigneux et al., 2004; Chaminade et al., 2005;
Mu¨ hlau et al., 2005) with the intent to test the neuroanatomical
hypothesis of the neuropsychological
models previously described.
Neurophysiological studies allow the investigation
of brain processes at the neuronal level and are
essential to the understanding of the principles of
neural computation. Certainly the monkey brain
differs from the human brain, however this discrepancy
can be overcome to some extent through
the search of homologies (Rizzolatti et al., 2002;
Arbib and Bota, 2003; Orban et al., 2004; Sereno
and Tootell, 2005). Sensorimotor processes such as
reaching and grasping for example, have been
extensively studied: several parallel parietofrontal
circuits were identified, each subserving a particular
sensorimotor transformation (Kalaska et al., 1997;
Wise et al., 1997; Matelli and Luppino, 2001;
Battaglia-Mayer et al., 2003). Without going into
the details of the representations used in each of
these functionally distinct parietal and frontal areas
(illustrated in Fig. 4), we will mention those that
seem relevant for understanding apraxia. For example,
LIP-FEF neurons discharge in relation with
eye movements and are sensitive to the direction
and amplitude of eye saccades (Platt and Glimcher,
1998), VIP-F4 neurons construct a representation
of the ‘‘peripersonal space’’ confined to the head
(Duhamel et al., 1998), MIP-F2 neurons have a
crucial role in the planning, execution and monitoring
of reaching movements (Eskandar et Assad,
1999; Simon et al., 2002; Raos et al., 2004) and
finally AIP-F5 neurons mediate motor responses
selective for hand manipulation and grasping movements
(Cohen and Andersen, 2002). Furthermore,
multiple space representations appear to coexist in
the brain that integrate multisensory inputs (e.g.,
visual, somatosensory, auditory and vestibular inputs)
(Graziano and Gross, 1998). For example,
neurons in area 5 appear to combine visual and
somatosensory signals in order to monitor the configuration
of the limbs (Graziano et al., 2000) and
the receptive fields of VIP neurons respond congruently
(i.e., with matching receptive fields) to tactile
and visual stimulation (Duhamel et al., 1998).
It is very interesting that the modality-specific
activities are spatially aligned: the visual receptive
field corresponding to the arm or the face may shift
along with that body part when it is passively
14
Interestingly, these occipital and visually specialized areas
are not only modulated by the visual presentation of body
configurations, but also when the person executes a limb movement
(Astafiev et al., 2004), indicating a bi-directional flow of
the information.
77
moved (Graziano et al., 1997). In addition, neurophysiological
data can give us insight into how the
arm posture modulates the activity of somatosensory
neurons (Helms Tillery et al., 1996) and how it
affects the neurons that compute the trajectory of
the hand (Scott et al., 1997). It should be noted that
several sensorimotor transformations are needed in
order to grasp an object, the motor command being
in hand coordinates and the object’s location in
gaze coordinates. To compute these transformations,
the brain appears to use multiple bodycentered
frames of references (Graziano and Gross,
1998): the frames of references underlying VIP area
neurons appear to be organized along a continuum
from eye to head coordinates (Duhamel et al., 1997;
Avillac et al., 2005) and direct transformations
from head to body-centered representations are
possible in the posterior-parietal cortex (Buneo
et al., 2002; Buneo and Andersen, 2006) with an
error estimate of the target position computed in a
common eye reference frame (Batista et al., 2002;
Cohen and Andersen, 2002). Finally, it was also
shown that tools may be integrated into the ‘‘body
schema’’ at the neuronal level (Iriki et al., 1996;
Maravita et al., 2003).
To conclude, we strongly believe that this multidisciplinary
approach should be bidirectional.
Not only apraxia can be interpreted in the neuropsychological
and neurophysiological frameworks,
but these research domains would also benefit
from taking into consideration observations from
apraxia. For example, one could learn enormously
on how the normal human praxis system functions
by looking at how it is affected by apraxia.
Acknowledgments
This work is supported in part by the Swiss
National Science Foundation, through grant 620-
066127 of the SFN Professorships Program, by the
Sport and Rehabilitation Engineering Program at
EPFL and by the Robotcub Project.
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