Neuropsychologia 39 (2001) 200–216
Recognition and imitation of pantomimed motor acts after
unilateral parietal and premotor lesions: a perspective on apraxia
U. Halsband a,b,
*, J. Schmitt b
, M. Weyers b
, F. Binkofski b
, G. Gru¨tzner d
,
H.-J. Freund c
a
Department of Neuropsychology, Albert-Ludwig-Uni6ersity of Freiburg, Niemensstraße 10, D-79089 Freiburg, Germany
b
Department of Neurology, Heinrich-Heine-Uni6ersity of Du¨sseldorf, Du¨sseldorf, Germany
c
Reha Krefeld-Rk-GmbH, Krefeld, Germany
d
Department of Radiology, Heinrich-Heine-Uni6ersity of Du¨sseldorf, Du¨sseldorf, Germany
Received 13 July 1997; received in revised form 23 March 2000; accepted 17 May 2000
Abstract
We compared gesture comprehension and imitation in patients with lesions in the left parietal lobe (LPAR, n=5) and premotor
cortex/supplementary motor area (LPMA, n=8) in patients with damage to the right parietal lobe (RPAR, n=6) and right
premotor/supplementary motor area (RPMA, n=6) and in 16 non-brain damaged control subjects. Three patients with left
parietal lobe damage had aphasia. Subjects were shown 136 meaningful pantomimed motor acts on a videoscreen and were asked
to identify the movements and to imitate the motor acts from memory with their ipsilesional and contralesional hand or with both
hands simultaneously. Motor tasks included gestures without object use (e.g. to salute, to wave) pantomimed imitation of gestures
on one’s own body (e.g. to comb one’s hair) and pantomimed imitation of motor acts which imply tool use to an object in
extrapersonal space (e.g. to hammer a nail). Videotaped test performance was analysed by two independent raters; errors were
classified as spatial errors, body part as object, parapraxic performance and non-identifiable movements. In addition, action
discrimination was tested by evaluating whether a complex motor sequence was correctly performed. Results indicate that LPAR
patients were most severely disturbed when imitation performance was assessed. Interestingly, LPAR patients were worse when
imitating gestures on their own bodies than imitating movements with reference to an external object use with most pronounced
deficits in the spatial domain. In contrast to imitation, comprehension was not or only slightly disturbed and no clear correlation
was found between the severity of imitation deficits and gesture comprehension. Moreover, although the three patients with
aphasia imitated the movements more poorly than non-aphasic LPAR patients, the severity of comprehension errors did not
differ. Whereas unimanual imitating performance and gesture comprehension of PMA patients did not differ significantly from
control subjects, bimanual tasks were severely disturbed, in particular when executing different movements simultaneously with
the right and left hands. © 2000 Elsevier Science Ltd. All rights reserved.
Keywords: Parietal cortex; Premotor areas; Comprehension of gestures; Movement imitation; Clinical neuropsychology
www.elsevier.com/locate/neuropsychologia
1. Introduction
Since Liepmann’s [44,45] first description, one of the
pertinent issues in apraxia research is the question
whether not only the production but also the recognition
and understanding of motor acts is disturbed.
According to Liepmann [45,46] model apraxic symptoms
can either appear consequent to disturbances of
the mental representation of movements, or of the
actual carrying out of movements, or of the translation
of the mental representation into movement production.
It was suggested that apraxic disturbances may be
traced back to an impairment of representation of the
form or the meaning of the particular action [4]. The
interaction between cognitive representation and production
has been the focus of critical discussions
[25,26,40,42,57,58]. Jeannerod and Decety [42] came to
the conclusion that the motor impairments observed in
apraxic patients result from a specific alteration in their
ability to mentally evoke actions, or to use stored
* Corresponding author.
E-mail address: halsband@psychologie.uni-freiburg.de (U. Hals-
band).
0000-0000/00/$ - see front matter © 2000 Elsevier Science Ltd. All rights reserved.
PII: S0028-3932(00)00088-9
U. Halsband et al. / Neuropsychologia 39 (2001) 200–216 201
motor representations for forming mental images of
actions.
In a series of experiments Heilman et al. [32–35] and
Rothi et al. [61,62] examined pantomime discrimination
and comprehension in patients with ideomotor apraxia.
Heilman et al. [32] investigated whether patients with
posterior dominant lesions that include the parietal lobe
differ from patients with anterior lesions in their ability
to discriminate between correctly and incorrectly performed
motor acts. Twenty subjects were classified into
four groups, according to the locus of the lesion (anterior
versus posterior) and whether or not they were
suffering from ideomotor apraxia. Results indicate that
apraxic patients with posterior lesions have more
difficulties discriminating between correctly and incorrectly
performed acts than apraxics with anterior lesions.
However, the authors were unable to identify the
exact localisation of the lesions and some of their
patients did not even have a CT scan. Rothi et al. [61]
reported that apraxic patients with posterior lesions
had difficulties in comprehending the meaning of pantomimes
using a non-verbal paradigm. In contrast,
Heilman [34] described three patients who could not
perform meaningful actions on verbal command, but
who were unimpaired in picking out the correct act
from several alternatives performed by the experimenter.
These findings [34] are consistent with the
results by Roy and Square [63], who postulated a
dissociation between conceptual and production components.
The findings are further supported by Rapcsak
et al. [57] who described a patient with bilateral damage
to the posterior parietal lobe. The female patient was
unable to pantomime simple movements with either the
left or the right hand. She also showed deficits in the
usage of real tools, albeit with some improvement over
her performance on imitation. However, the patient
showed no problems in the interpretation and discrimination
of presented pantomimes of actions. The authors
interpreted the results as empirical proof of a
dichotomy between the mental comprehension of an
action and its motor realisation.
Here we addressed the question whether motor impairments
observed in apraxic patients are associated
with difficulties in the recognition and understanding of
motor acts. For this purpose, the comprehension and
imitation of gestures was thoroughly examined by a
video test set comprising 136 representational movements
that had to be identified and imitated. It was
argued that in the case of a common disturbance of
comprehension and generation of motor behaviour, the
disorder would affect an integrative sensorimotor transformation
process. Alternatively, a selective impairment
of movement production would argue for a primary
motor disorder. Such a view is supported by the results
of kinematic movement analysis, showing ‘low level’
executional errors of various movement components
[9,36,55,56].
It was further examined whether the occurrence of
recognition and production deficits depends on the
types of movements examined and the site and the side
of the lesion. For this purpose, the ability to recognise
and to imitate different categories of pantomimed unimanual
and bimanual motor acts was examined in
patients with parietal damage and in normal control
subjects. For comparison, patients with premotor damage
or a lesion of the precentral motor strip were tested
in order to evaluate the specificity of the parietal disturbances.
This question was also of interest because parietal
and premotor areas are densely interconnected.
It is important to emphasize that in the present study
our apraxic patients with parietal damage presented
with relatively dorsally located lesions barely involving
the supramarginal gyrus in the inferior parietal lobe
and temporal lobe structures. There is evidence of a
differential involvement of the anterior and posterior
parts of the parietal cortex in motor preparation and
execution. Brain lesion studies of apraxic patients [1–3]
and imaging studies [12,39] indicate that the inferior
parietal cortex near the supramarginal gyrus may be
more important than the superior parietal cortex in the
correct selection of movements. Using positron emission
tomography and measurement of regional cerebral
blood flow (rCBF) as an index of cerebral activity,
Deiber et al. [12] found that the posterior parietal
cortex is more critically involved in the correct selection
of movement on the basis of spatial attention, whereas
the anterior parietal cortex was more activated in the
use of visual information for motor preparation. Thus,
we assume that our findings would be different if
patients with ventrally located lesions were examined.
2. Subjects
All subjects gave their informed consent to participate
in this study. The study was based on 11 patients
with lesions in the parietal cortex (mean age 62 years,
range: 55–71 years), 14 patients with lesions in dorsolateral
premotor cortex or supplementary motor area
(mean age 53 years, range: 22–76 years) and 16 healthy
control subjects (mean age 57 years, range: 28–73
years). In addition, three patients with lesions of the
precentral gyrus (PC) (mean age 51 years, range: 47–54
years) were examined. All patients were investigated
during in-patient treatment at the Department of Neurology,
Heinrich-Heine University of Du¨sseldorf. Control
subjects were recruited from the neighbours of UH
and MW and from the healthy spouses of the patients.
All subjects gave informed consent before entering the
study.
Five of the parietal lesions were in the left (LPAR)
and six in the right hemisphere (RPAR); three patients
with left parietal lobe damage had aphasia. There were
U. Halsband et al. / Neuropsychologia 39 (2001) 200–216202
eight patients with damage to the left premotor/supplementary
motor area (LPMA) and six with damage
to the right premotor/supplementary motor area
(RPMA); two precentral (PC) lesions were in the left
hemisphere (LPC), and one in the right hemisphere
(RPC). As in previous work [17,27], dorsolateral premotor
lesions were allocated to the region anterior to
the precentral sulcus, corresponding to area 6aa of
Vogt’s cytoarchitectonic map. This historical delineation
of the premotor areas in the human was chosen
for the following reasons: (i) the homologies of
the human PMd and monkey’s postarcuate (=precentral)
premotor areas are still unclear [2,19,73]; (ii)
the distinction of the anterior (area 6a) and posterior
(area 4) lesions is virtually impossible; and (iii) so far,
activation studies have also not clarified the issue [38].
All subjects were right-handed and naive as to the
objectives of the study. Handedness was established
by means of the TU8 LUC [68] questionnaire. The
handedness score was based on hand preference
shown in 20 everyday situations, such as writing,
teeth-brushing or catching a ball.
The average duration of the examination was 6 h
and included a neuropsychological screening procedure
(see below). The patients were tested on 2 consecutive
days. On the first day, patients underwent a
neuropsychological evaluation; on day 2, the experimental
sessions on gesture comprehension and imitation
were performed. In addition, a third testing day
was needed for those patients who scored below average
on the Reitan Indiana Aphasia Screening Test.
These patients were examined on the full battery of
the standardised German aphasia test, Aachener
Aphasie Test (AAT); the additional test duration for
the aphasic patients was 2–3 h. In order to avoid
fatigue, all testing sessions were limited to 1 h periods,
followed by 15 min of relaxation.
3. Methods
3.1. Neuropsychological screening procedure
Two formal intelligence tests were administered to
all patients: (1) a verbal German intelligence scale
(Mehrfach-Wortschatz Test B, MWT-B); and (2) a
non-verbal IQ-test, the Raven Test (Standard Progressive
Matrices). In addition, Trail Making Parts A and
B, two tests for visual neglect (Albert’s Test and Line
Bisection) and a formal memory and attention test
battery (Syndrom-Kurztest zur Erfassung von
Aufmerksamkeits- und Geda¨chtnissto¨rungen, SKT)
were used. Only patients who scored with an IQ \
89 in at least one of the IQ tests and who did not
show evidence of neglect disturbances or other apparent
deficits in attention, mnestic performance or cognitive
flexibility were included in this study [27].
All patients with left-sided brain damage were also
subjected to the German version of the Reitan Indiana
Aphasia Screening Test (translation by Jim
Maxwell and Hendrik Niemann). Language functions
were formally assessed with the full battery of the
Aachener Aphasie Test (AAT) only in those three
patients who scored below average on the Aphasia
Screening Test. Thereafter, types of aphasic disturbances
were classified according to the results obtained
by the AAT [37].
3.2. Neurological disturbances as re6ealed by clinical
examination
All patients underwent a thorough clinical examination.
The major clinical findings are summarised in
Fig. 1.
Ideomotor apraxia was examined by our extensive
test battery. Tactile apraxia was diagnosed on the basis
of the misconceived explorative finger and hand
movements during object handling, manipulation and
active touch [52]. Other movements of the hands and
fingers, force and tapping were normal. In addition,
disturbances of interlimb coordination frequently observed
in patients with premotor lesions were examined,
as described by Freund and Hummelsheim [17].
Subjects were asked to perform alternating windmill
and cycling movements in both directions.
4. Action production: imitation of pantomimed motor
acts
4.1. Classification of meaningful mo6ements
Meaningful movements may be grouped into two
broad categories, those directed to manipulate objects,
which have been called transitive movements and those
gestures meant to express ideas or feelings, which have
been called intransitive movements [15]. According to
Hecaen [30] and Hecaen and Rondot [31] intransitive
movements should be further subdivided into symbolic
gestures (e.g. to salute, to make the sign of the cross)
and should be kept separate from expressive gestures
(e.g. to threaten somebody) as they would reflect different
psychological purposes subserved by discrete neuronal
mechanisms. However, in our opinion the
legitimacy of this distinction appears to be questionable
if it applies to gestures produced out of context, as the
performance is not sustained by the emotional mechanisms
implicated in the real situation. In accordance
with De Renzi [15], in the present study the category
intransitive gestures thus consists of both symbolic and
expressive gestures alike. In contrast, transitive movements
were subdivided into two main categories: (i)
U. Halsband et al. / Neuropsychologia 39 (2001) 200–216 203
pantomimed movements centred around the body (egocentric
space); and (ii) movements made in extrapersonal
space. This was done because there is evidence
that movements in relation to one’s own body-scheme
can be more affected than movements made in extrapersonal
space [11,23,51].
Fig. 1. Prominent clinical signs and outline of the lesions for the axial plane showing their largest extent. (A) Brain diagrams for each patient,
on the top right the major sulci are shown. Arrows point to the central sulcus in each drawing. (B) Shows a summary of the extent and the etiology
of the lesion and major clinical deficits for each patient. PCS, precentral sulcus; CS, central sulcus; PoCS, postcentral sulcus.
U. Halsband et al. / Neuropsychologia 39 (2001) 200–216204
Fig. 1. (Continued)
U. Halsband et al. / Neuropsychologia 39 (2001) 200–216 205
Fig. 1. (Continued)
Patients were asked to imitate meaningful actions as
shown on a video screen. Actions included unimanual
and bimanual motor tasks. In all conditions, performance
was separately scored for the lesional and contralesional
hand. In the unimanual motor tasks, the order
of hand conditions was randomised across trials. Performance
on all production tests was videotaped and was
later scored independently by two examiners. It was
assumed that a high inter-rater reliability provides a valid
assessment of the subjects’ motor performance.
The two raters were shown the same videotape and
asked to make, for each movement imitation, a judge-
U. Halsband et al. / Neuropsychologia 39 (2001) 200–216206
ment whether the action was correctly performed or
not. If movement production was judged to be inadequate,
the raters were asked to classify the types of
errors as follows:
1. Spatial errors, including directional errors, were
defined as an inconsistency between the movement
path and the purpose of the action (e.g. if a pantomimed
performance of ‘drinking coffee out of a
coffee mug’ clearly showed that the object was
initially moved away from the subject’s mouth instead
of approaching it) and/or a spatial misplacement at
the target position (e.g. instead of toothbrushing
pantomimed action appeared at the patient’s cheek);
2. Body part as object (e.g. eating soup with a finger and
not with a spoon);
3. Parapraxic errors were defined as a correctly executed
movement which, however, was not appropriate for
the target action (e.g. instead of cutting one’s nails the
pantomimed act was identified as brushing one’s
nails);
4. Non-identifiable and/or incomplete movements (e.g.
the hand was lifted without aiming at a specific
target).
The change-weighted correlation coefficient s was
applied for measuring reliability among raters. The
following rating measures were documented: PAR, s=
0.89; p(Z) B0.01; PMA, s=0.92; p(Z) B0.01; Ml,
s=0.95; p(Z) B0.01; CO, s=0.98; p(Z) B0.01.
4.2. Unimanual motor tasks
4.2.1. Imitation of symbolic gestures
Ten symbolic and conventional gestures were successively
presented on a video-screen. Items included waving,
saluting and threatening. Each presentation lasted
for 8 s. Immediately after each presentation, a coloured
rainbow-pattern appeared on the screen and subjects
were asked to imitate the action.
4.2.2. Imitation of pantomimed motor acts in relation
to a person’s own body
The actor on the videoscreen performed ten pantomimed
movements in relation to his own body.
Movements included hygienic routines, such as combing
one’s hair, toothbrushing, nail-clipping and shaving.
Fig. 1. (Continued)
U. Halsband et al. / Neuropsychologia 39 (2001) 200–216 207
4.3. Pantomiming the use of an object in extrapersonal
space
Subjects were asked to imitate ten pantomimed actions
with respect to the location of an imagined recipient
of a tool’s action in extrapersonal space.
Performance included hammering, stamping and pouring
fluid into a glass.
4.4. Bimanual motor tasks
Subjects were requested to imitate 20 meaningful
movements using both hands simultaneously. Half of
the actions presented consisted of two homogeneous
components, whereby both hands performed an identical
movement to an imagined object, such as wringing
or piano-playing with symmetrical finger movements.
The other ten actions consisted of heterogeneous movement
patterns. In this condition, subjects were requested
to use their left and right hand simultaneously
and to perform two different pantomimed motor acts
to an imagined object. For instance, when subjects
pantomimed the action ‘slicing bread’ they were instructed
to use the left hand for advancing the imagined
loaf, while simultaneously turning an imagined handle
with the other hand. Another example is ‘cooking a
pudding’. In this task, subjects were asked to pantomime
pouring pudding powder into the boiling milk
with their left hand, while simultaneously stirring it
with the other hand.
4.5. Tool use
Subjects were asked to demonstrate the use of ten
common household tools (e.g. screw-driver, pneumatic
pump) presented as static pictures on a video-screen.
Each item was presented for 8 s and appeared without
context-specific cues on an identical neutral background
(examiner’s desk). As before, a coloured rainbow-pattern
appeared on the screen immediately after
each presentation. Subjects were asked to pantomime
the movements associated with the appropriate tool
functioning using his ipsilateral or contralateral hand.
Tool use was further evaluated with the tools provided
as real items on the examiner’s table. For this
purpose, an additional set of ten common tools and the
objects of the tools action were provided (e.g. a pair of
scissors and paper). Only one tool and the relevant
object were presented at a time. Subjects were asked to
demonstrate the tool’s action.
4.6. Completion of serial motor acts
Subjects were instructed to complete a series of motor
acts. For this purpose, a series of ten complex
motor sequences was presented on the video-screen.
For instance, it was shown how to pack various items
into a suitcase before a journey. A series of items
placed on the actor’s table was put, one after each
other, into the suitcase. The film stopped after the last
item was inside the case. The patient was asked to
demonstrate which movement(s) would appear next in
the sequence. The minimum requirement for an answer
to be scored correctly was pantomiming the movement
necessary for closing the lid of the case. However, most
subjects spontaneously continued the sequence task by
adding the movements how to lock the case and to
carry it out of the room.
5. Recognition and evaluation of motor acts
5.1. Recognition of meaningful pantomimed motor acts
5.1.1. Symbolic gestures
Subjects were shown ten symbolic gestures on a
video-screen; each presentation lasted for 8 s. Subjects
were asked to describe the meaning of the gestures and
to indicate the context in which they appear (e.g. taking
an oath at court, putting one’s hands-up at school).
5.1.2. Recognition of pantomimed motor acts in
relation to one’s own body
Subjects were asked to identify and to describe ten
meaningful pantomimed movements with respect to
their own body, such as hair brushing, using a lipstick
and nail colouring.
5.1.3. Recognition of pantomimed performance of the
use of an object in extrapersonal space
Subjects were asked to identify and to describe the
meaning of ten pantomimed actions with respect to an
imagined recipient of a tool’s action in extrapersonal
space, such as writing, using a screw-driver or cutting a
piece of paper.
5.2. Knowledge rele6ant to the serial organisation of
action
5.2.1. E6aluation of motor sequences
Action evaluation was tested by asking the subjects
to judge whether complex motor sequences presented
on a video-screen were flawlessly or incorrectly performed.
Movement sequences were presented within the
usual context and with the aid of the appropriate
objects and tools. For instance, the tasks preparing
fried eggs or extracting the juice from an orange were
videotaped in a kitchen with the use of the appropriate
household equipment.
A total number of 20 different sequences was presented.
A total of 50% of the serial motor acts were
correctly performed; the other tasks were characterised
U. Halsband et al. / Neuropsychologia 39 (2001) 200–216208
by either sequence errors (n=5) or conceptually inappropriate
tool use (e.g. to hammer a cork-screw into the
cork). Subjects were asked to judge whether a given
sequence was correctly or incorrectly performed. If they
scored a performance as incorrect, they were asked to
name and identify the sequence and performance
errors.
5.2.2. Completion of serial action tasks
Knowledge of the serial position of motor acts was
examined by asking the subjects to describe which
movement comes next in an unfinished series of movements.
Subjects were shown ten correctly performed but
incomplete motor sequences, such as lighting a cigarette
or using an electric coffee machine. They were asked to
describe which movement is lacking to complete the
motor act.
5.2.3. Conceptual knowledge of tool function
Subjects were asked to describe verbally the function
of ten common household tools (e.g. hammer, canopener)
presented on a video-screen. Each tool appeared
as a static item without context-specific cues on
a neutral background and remained visible for 10 s.
Knowledge of tool function was further evaluated by
presenting the subjects with an additional set of ten
common tools. This time, tools were presented as real
items on the examiner’s table. Subjects were asked to
visually inspect each tool and to describe the conceptual
knowledge of actions required for appropriate tool
use (e.g. in order to pound a nail one has to put the
handle of the hammer in one’s palm and to swing the
hammer repeatedly through the air).
6. Results
6.1. Mapping of brain lesions
Mapping of brain lesions was carried out by an
investigator who was completely unaware of the neuropsychological
results. Structural lesions were outlined
on CT or T1-weighted MR scans obtained around the
time of the examination (CT scanner: General Electric
CGR CE 1000; MR scanner: Siemens Magnetom 1.5 T,
spin echo MR sequence, 600 ms repetition time, 15 ms
echo time, two excitations, 6.0 mm slice thickness).
Brain lesions were defined as parenchymal defects with
gray scale values clearly different from those of the
normal tissue. All CT and MR sections were obtained
parallel to the canthomeatal line, thereby allowing
anatomical mapping on corresponding templates
derived from the atlas of Matsui and Hirano [49]. For
this purpose, each CT or MR brain section containing
the lesion was proportionally magnified in order to fit
with the maximum anteroposterior and transverse dimensions
of the brain atlas [69].
Fig. 1 shows the individual main clinical findings
along with brain lesion outlines and a summary of the
extent and the etiology of the lesion.
6.2. Action production: imitation of pantomimed motor
acts
6.2.1. Unimanual motor performance
For each movement category, the performance of the
ipsilesional and contralesional hand was evaluated. Fig.
2 gives a comparison of the subjects’ ability to imitate
symbolic gestures (A), to pantomime actions towards
one’s own body (B) and motor acts imitating tool use in
extrapersonal space (C).
Two factor ANOVA was performed, in which patients
were compared with controls on production versus
comprehension (see below) tasks. In patients with
left or right parietal lobe lesions the impairment on
production was significantly higher to any impairment
in recognition (PB0.01).
Results indicate that ipsilateral and contralateral
hand performance of the patients with left parietal
lesions was worst followed by patients with right parietal
lobe damage (PB0.01). Among the various types
of movements examined, pantomiming performance of
meaningful symbolic gestures was the least affected
category. Interestingly, patients with damage to the left
parietal lobe were worse when imitating gestures aimed
towards their own bodies as compared to symbolic
gestures (PB0.01) and movements with reference to an
external object (PB0.01). The fact that our control
subjects as well as our patients with premotor or M1
lesions (see below) had no more difficulties in mastering
the pantomimed movements made in extrapersonal
space as compared to movements centred around the
body makes it unlikely that the second task was more
difficult.
Imitating performance of our patients with PMA
lesions did not differ significantly from the controls or
from patients with PC lesions in any of the movement
categories examined (Fig. 2). Furthermore, the performance
of our patients with PMA lesions did not differ
from patients with supplementary motor (SMA) damage;
due to the small sample size of the dorsolateral and
medial premotor areas, the two groups were pooled
together.
Inadequate movement production was classified according
to the type of error made by the patients. The
results are based on the total score obtained for unimanual
pantomiming performance, whereby all three
movement categories were pooled together. Fig. 3
shows the mean error rate for the various lesion groups.
It can be seen that the most frequent types of errors
that occurred in patients with lesions to the left parietal
lobe were spatial errors which expressed themselves as a
spatial misplacement at the target position and/or an
U. Halsband et al. / Neuropsychologia 39 (2001) 200–216 209
Fig. 2. Distribution of errors (in %) in pantomimed imitations using the ipsilesional (top) or contralesional hand (bottom). For the patient group,
the percentage of errors refers to the use of the ipsilesional (top) or contralesional (bottom) hand as compared to the dominant hand of the normal
volunteers. (A) Symbolic and meaningful gestures; (B) actions towards one’s own body and (C) imagined tool use in extrapersonal space. PAR,
parietal lobe; PMA, premotor areas; PC, precentral gyrus; CO, controls. Vertical lines give the S.D.
inconsistency between the movement path and the purpose
of the action (Fig. 3).
None of our patients had any difficulties in spontaneously
supplying the missing link in an incomplete
sequence. Their performance was as follows (% correct):
LPAR, 97; RPAR, 90; LPMA, 98; RPMA, 95, PC, 100;
CO, 99.
6.2.2. Bimanual motor tasks
Although patients with PMA lesions were not impaired
in pantomiming unimanual movements, they
showed most pronounced deficits in imitating bimanual
movements. Results indicate most pronounced deficits in
the bimanual heterogeneous condition when executing
different movements simultaneously with the right and
left hands in patients with damage to the PMA (Mann–
Whitney U-test, PB0.01). For instance, when asked to
pantomime the movement ‘pouring pudding powder into
the boiling milk with one hand while simultaneously
stirring it with the other hand’, subjects could correctly
perform both movements separately, but were unable to
carry out both movements simultaneously. Their execution
of movement could be characterised as that mostly
only one hand at a time was active (stirring with the right
hand or pouring with the left). Sometimes stirring was
carried out using both hands at the same time, followed
by a bimanual pouring movement.
Patients with PMA lesions were further subdivided
into subjects with preferential damage to the dorsolateral
premotor areas and subjects with damage to the medial
wall motor areas (supplementary motor area, cingulate
motor areas). Results indicate that patients with lesions
to the lateral premotor areas were less severely impaired
in performing bimanual heterogeneous movements
than patients with preferential damage to the
medial wall motor areas (Mann–Whitney U-test for very
small samples, PB0.01) (Fig. 4). Results are based on
the percentage of errors made by subjects with left or
right sided damage to the lateral or medial wall motor
areas.
6.2.3. Action recognition and e6aluation
Only minor disturbances in comprehending the meaning
of a pantomimed action were found among patients
with parietal lesions; patients with PMA, SMA or PC
damage were not impaired on these tasks. Fig. 5 gives
a comparison of the subjects’ ability in identifying
symbolic gestures (A), pantomimed actions towards
one’s own body (B) and motor acts of an imagined tool’s
action in extrapersonal space (C).
A two factor ANOVA was performed to test whether
comprehension deficits were significant in patients with
unilateral parietal lesions as compared to control subjects.
Results indicate a significant impairment for the
U. Halsband et al. / Neuropsychologia 39 (2001) 200–216210
Fig. 3. Classification of errors in motor performance pantomimed on imitation. For this purpose, the three movement categories (see Fig. 2) were
pooled together. PAR, parietal lobe; PMA, premotor areas; PC, precentral gyrus; CO controls; bp, body part as objects (see text). Vertical lines,
S.D.
patients with left-sided damage (PB0.05), the results of
patients with a right-sided parietal lesion did not differ
significantly from the control subjects.
Most interestingly, a heterogeneous picture of disturbances
of recognition and production was found in the
individual patients. It can be seen from Fig. 6 that some
of the apraxic patients showed no deficits at all in the
discrimination of actions at the mental level, although
their production was severely disturbed. In spite of the
preponderance of production errors, almost half of the
patients also showed some comprehension errors (Fig.
6).
The severity of comprehension errors did not differ
between aphasic and non-aphasic patients with parietal
lobe damage, although the aphasic subjects performed
the movements more poorly (Fig. 7).
None of our patients had difficulties in judging
whether a given sequence was correctly or inadequately
performed. They had no problems in naming and identifying
sequence or performance errors. Their performance
was as follows (% correct): LPAR, 97; RPAR,
96; LPMA, 98, RPMA, 97; PC and CO, 100. They also
had no difficulties in identifying the missing link in an
incomplete sequence. Their performance was as follows
(% correct): LPAR, 97; RPAR, 92; PMA, PC and CO,
100.
6.2.4. Knowledge of tool use
None of the patients in this study showed any problems
in the comprehension of the use of a tool or in its
actual use. None of our subjects made any errors when
knowledge of tool function was evaluated by presenting
the subjects with a set of real tools. They identified all
tools correctly (100%). When asked to use the tools,
their performance was as follows (% correct): LPAR,
98; RPAR, 100; LPMA, 97; RPMA, PC and CO, 100.
The percentage of correct responses in identifying the
function of common household tools presented as a
static picture on a video screen was as follows: LPAR,
100, RPAR 98; PMA, PC and CO, 100. However, when
asked to pantomime the use of the tool shown on the
videoscreen, thus producing the relevant action without
the tool being present, patients with parietal lesions
were significantly impaired; the percentage of correct
responses was as follows: LPAR, 66 (P\0.01); RPAR,
88 (P\00.5); LPMA, 94; RPMA, 95; PC and CO, 98.
Fig. 4. Percentage of errors in pantomiming bimanual homogeneous
and heterogeneous (see text) movements. For this purpose, lesions of
the dorsolateral premotor areas (PMd) and the medial wall motor
areas (MWA: SMA and cingulate motor areas) were analysed separately.
PAR, parietal lobe; PC, precentral gyrus; CO, controls; vertical
lines, S.D.
U. Halsband et al. / Neuropsychologia 39 (2001) 200–216 211
Fig. 5. Distribution of correct responses (in %) in the recognition of (A) symbolic and meaningful gestures; (B) movements towards one’s own
body and (C) imagined tool use in extrapersonal space. PAR, parietal lobe; PMA, premotor areas; PC, precentral gyrus; CO, controls; L, left-sided
lesion; R, right-sided lesion. Vertical lines give the S.D.
7. Discussion
7.1. Parietal cortex
The basic finding of this study was that the comprehension
of the symbolic and representational content of
motor acts is not or only slightly disturbed in apraxic
patients with parietal lobe lesions. The dissociation
between the most pronounced disturbances in the production
of movements and relatively preserved comprehension
of the symbolic meaning is not in support of
the hypothesis that apraxic disturbances are rooted in a
common disturbance of representation of the form or
the meaning of the particular action. Rather, the
apraxic disturbance in our parietal patient group appears
primarily as a motor production disorder, thus
supporting a dissociation between conceptual and production
components [57,63].
The results reflected a heterogeneous picture of disturbances
of recognition and production in the individual
patients. Some of the severely apraxic patients
showed no deficit in the discrimination of actions at the
mental level, although their production was severely
disturbed. There was no correlation between the number
of errors in gesture production and gesture comprehension.
However, the present findings indicate an
overall impairment for the patients with left-sided parietal
damage in the recognition and understanding of
motor acts.
The lack of a consistent gesture comprehension
deficit is possibly due to its sampling bias. Our parietal
patients presented with relatively dorsally located lesions
barely involving temporal lobe structures. There is
evidence from single cell recordings in monkeys [54]
and from brain imaging studies in man [47,60] that
action recognition may be mediated by temporal lobe
structures
It is therefore not surprising that, in the present
study, not only the comprehension of language, but
also that of expressive motor behaviour was rather well
preserved. We assume that the data would be different
when the patients were not selected for parietal or
premotor lesions because the ventral stream functions,
such as understanding of symbolic content, appear to
be relatively intact.
The present study makes a further point. The severity
of comprehension errors in our aphasic patients did not
differ from our non-aphasic apraxics with parietal lobe
damage. These findings make it unlikely that the involvement
of aphasia in apraxia could be interpreted as
a language-dependent disturbance in the recognition
and understanding of motor acts. Corina et al. [10]
reported left hemisphere specialisation of American
sign and spoken language in deaf and hearing individuals.
Their results suggest that left hemisphere specialisation
derives from the linguistic nature of the movement:
no evidence of hemispheric asymmetry was found for
production of either symbolic or arbitrary gestures.
The only consistent focal deficit found in the understanding
of pantomimed motor acts was that gestures
related to one’s own body were differentially affected
with regard to severity as compared to production
errors. Interestingly, a most pronounced production
impairment was observed after left parietal lobe lesions,
when subjects were asked to imitate gestures on their
own bodies rather than imitating movements with reference
to an external object. These findings may suggest
that the basic deficit in these subjects concerns the
ability to code and comprehend movements in relation
to their body-scheme [11,23,51]. According to Goldenberg
[23], faulty apprehension of spatial relationships
between body parts manifests itself not only in imitation
on oneself but also on a wooden mannikin. His
findings can be adduced as evidence for an overall
disturbance of representation of the human bodyscheme
independent of whether actions relate to the
own body or to an external model. In the present
investigation, we cannot distinguish between errors in
spatial guidance of movement, errors in missing the
target and spatial errors made from memory. It may be
U. Halsband et al. / Neuropsychologia 39 (2001) 200–216212
argued that the difference between the relatively preserved
extrapersonal space gestures and the body directed
space movements might also be accounted for by
the fact that posterior inferior parietal and intraparietal
sulcus may play a greater role in extrapersonally guided
movements.
The types of production errors classified into four
categories (spatial, body part as object, parapraxic,
non-identifiable) indicate that patients with parietal
lobe lesions presented with most pronounced deficits in
spatial parameters. This is in agreement with previous
findings that movement production impairments in patients
with ideomotor apraxia are characterised predominantly
by spatiotemporal errors [9,36,55,61,62].
The majority of the apraxic disturbances following
parietal lesions appeared in the spatial domain, such as
deviating trajectories with correct directions and/or incorrect
spatial positioning of the hand or finger on the
goal-point of the executable movement. Clark et al. [9]
reported errors in spatial exactness and a spatial-temporal
disintegration in highly atomised movements in
apraxic patients (slicing bread). These disturbances
were also seen when movements were not carried out
under verbal commands. Apraxic patients showed
deficits in the plane of motion, the shape of the trajectory
and in the coupling of hand speed and trajectory
shape under various contextual cue conditions. In conjunction
with the data presented here these results
illustrate the wide range from elementary to complex
motor dysfunctions.
Taken together, these findings support Heilman’s [32]
model of apraxia, which suggests that apraxia results
from destruction of spatiotemporal representations of
learned movements rather than from a disconnection
between the receptive language areas in the left hemisphere
and the motor cortices [21,22]. In order to
perform a skilled learned act, one must place particular
body parts in certain spatial positions in a specific order
at specific times. This implies that the nervous system
stores knowledge of motor skills. When this knowledge
is called into use, it is retrieved from motor memory
rather than being constructed de novo [19,26]. According
to Heilman’s [32] model spatiotemporal representations
of learned, skilled movements are stored in the
parietal cortex which is thought to instruct the premotor
cortex for the necessary movements.
A surprising feature of apraxic deficits is their context
dependence so that movements, which cannot be
made in accordance with verbal command or imitation,
can be flawlessly produced in another context [14,15].
The findings suggest a context-specific interaction between
cognitive representation and production. Jeannerod
and Decety [42] came to the conclusion that
motor impairments observed in apraxic patients may
result from a specific alteration in their ability to mentally
evoke actions, or to use stored motor representations
for forming mental images of actions. Thus, the
deficit arises when the patient shifts from a strategy
where object-orientated actions are processed automatically,
to when the content of these actions has to be
explicitly represented.
Most of our parietal patients did show elementary
and/or complex somatosensory disturbances, such as a
stereognosis or graphanaesthesia. Such disturbances
were not in focus of the present article but were
analysed in an earlier study [52]. That study showed
that damage of parietal sensory association cortex or its
underlying white matter does not only produce elementary
and perceptual/cognitive somatosensory deficits,
but also an impairment of active touch and of the
manipulative capacity of the hand required for object
exploration. This combined deficit of object recognition
and manipulation reveals the intricate interdependence
between the sensory and motor processes and represents
a unimodal somato-sensory or somato-motor dysfunction
(tactile or manipulative apraxia [19,52]). The
Fig. 6. Distribution of errors (in %) made by individual subjects with parietal lesions in the recognition and production of pantomimed motor acts.
Patients are ordered according to production error rate.
U. Halsband et al. / Neuropsychologia 39 (2001) 200–216 213
Fig. 7. Distribution of errors (in %) in the recognition and production of pantomimed movements in aphasic and non-aphasic patients.
apraxic visuomotor or speech behaviour seen in patients
with damage to the parieto-occipital or temporal
areas are other examples of apraxic disturbances bound
to a particular modality. The ideational and ideomotor
apraxias seen after lesions of the left inferior posterior
parietal lobule are supramodal and affect both sides of
the body.
7.2. Premotor areas
Our main finding was that patients with PMA damage
are unimpaired in unimanual motor performance
and in gesture comprehension. Motor impairments after
PMA damage were restricted to the bimanual condition
when executing different movements
simultaneously with the right and left hands (heterogeneous
condition). The most pronounced deficits were
seen in patients with damage of the medial wall motor
areas (supplementary motor area, cingulate motor areas).
Their execution of movement could be characterised
as that mostly only one hand at a time was active
(e.g. stirring with the right hand followed by pouring
with the left hand). Sometimes stirring was carried out
using both hands at the same time, followed by bilateral
pouring movements. In contrast, the performance
of homogeneous movements was normal.
Deficits of simultaneous, but independent movements
of both hands have been observed in monkey experiments
[6,7,43,70–72] and in patients with mesio-frontal
lesions [8,26,28,44,72] Brinkman [5] observed in monkeys
with SMA lesions that the two hands started to
behave in a similar manner instead of sharing the task
between them. Following callosotomy this deficit disappeared.
Wiesendanger et al. [70,71] trained monkeys on
a bimanual pull-and-grasp task, whereby the subjects
were required to open with their left hand a drawer
with a baited food-well and simultaneously to reach
with their right index finger into the food-well in order
to retrieve the reward. Thereafter, a unilateral SMA
lesion was placed in three monkeys, and after several
weeks of recovery, a second SMA lesion was placed on
the other side. In all three monkeys, changes of movement
parameters were observed in the limb contralateral
to the lesion, such as delays in movement initiation,
increased variability in the timing structure and increased
movement times. However, the principle of
motor equivalence, characteristic for invariant goal
achievement, was rather well preserved. The above
motor impairments were transient and recovered within
a month. The authors concluded that although the
SMA participates in bimanual coordination, it appears
to be less involved in the co-ordination of well-practised
bimanual skills.
The significance of PMA for the integration of bilateral
motor behaviour has already been emphasized by
Nielsen [50]. In contrast to patients with parietal lobe
damage, most of the deficits seen after PMA lesions
affect the performance of both arms [17,18,26–28].
Freund and Hummelsheim [17] found that patients with
dorsolateral PMA damage showed a reciprocal coordination
disorder between the two sides. This deficit
became most apparent when the patient was asked to
produce alternating windmill movements with their
arms or paddling movements with their legs in the
backward direction. On the basis of a combined lesion
and activation study, we have recently provided evidence
that the medial wall areas and here in particular,
the cingulate motor areas play a pivotal role for bimanual
interaction [67].
Martin et al. [48] reported an activation in the left
premotor area when subjects named tools. But the
results of this investigation show that lesions of the
dorsolateral premotor cortex or the medial wall areas
do not cause an impairment in demonstrating object
U. Halsband et al. / Neuropsychologia 39 (2001) 200–216214
use to computer presented pictures. Earlier, we have
shown that lesions of the premotor cortex in monkeys
[29] and man [25–27] cause severe impairments on
tasks in which the subject had to learn arbitrary associations
between sensory stimuli and a set of motor
responses. Patients and monkeys with premotor lesions
are impaired when they must recall a movement from
memory on the basis of a visual cue. But here, a crucial
factor seems to be that in all these experiments it was
visual cues from an arbitrary context that must prompt
the recall of specific actions. Passingham [52] has shown
that monkeys with premotor lesions can recall actions if
they are prompted by the identity of the object they
must manipulate. This interpretation might also be
applied to the present findings: Our patients with premotor
damage were unimpaired in demonstrating object
use to computer presented pictures. Furthermore,
clinical observations of these patients do not reveal any
deficits in selecting the appropriate action during their
daily ward activities. But the same patients have serious
difficulties in test situations where an arbitrary sensory
cue is used for directing the movement.
Motor imagery is known to activate medial wall and
dorsolateral premotor areas [39,66]. It has recently been
shown that the observations of actions also activates
the premotor circuitry. Evidence for such an observation/execution
matching system in primates [20,59] was
first presented by Rizzolatti et al. [59] and Gallese et al.
[20] when they registered neurones in the ventral premotor
cortex (area F5) that discharged when the monkey
performed an action but also when the animal
observed an action made by the experimenter or by
another monkey. The authors argued that these ‘mirror
neurones’ reflect the representation of the observed
behaviour. It was concluded that these neurones play a
crucial role in the understanding of motor events. According
to Jeannerod [41] and Jeannerod and Decety
[42], the neurones responsible for the motor image
formation are the same the subject will later activate
during planning and preparation of the action thus
providing action-schemas. These experimental results
were complemented by fMR and magnetic stimulation
studies confirming the existence of an observation/execution
matching system [13,24,60] in the human. The
localization of this system in F5, the likely homologue
of Boca’s area in the monkey, led to the assumption
that it plays a pivotal role for the understanding of
gestures and other expressive motor behaviour.
This concept was recently extended by data showing
more distributed and somatotopically organised premotor
activations during action observation (Buccino et al.
[7]). Whenever these actions were object-related parietal
cortex was additionally activated. These data emphasize
that action observation is processed in dorsal stream
areas in order to automatically generate an internal
replica of that action. The dissociation between the
effects of parietal lesions that interfere with the imitation
of action sequences but leave their recognition
intact is in accordance with the processing of action-related,
pragmatic information along the dorsal and of
semantic decoding of observed actions along the ventral
stream.
Acknowledgements
The work was supported by a grant from the
Deutsche Forschungsgemeinschaft to U.H. (Ha-1262/2-
1 and Ha-1262/2-3).
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