Cerebral Cortex December 2007;17:2769--2776
doi:10.1093/cercor/bhm004
Advance Access publication March 5, 2007
Pantomime of Tool Use Depends on
Integrity of Left Inferior Frontal Cortex
Georg Goldenberg1, Joachim Hermsdörfer2, Ralf Glindemann1,
Chris Rorden3 and Hans-Otto Karnath4
Neuropsychological Department and 2Research Group
Clinical Neuropsychology, Bogenhausen Hospital, D 81925
Munich, Germany, 3Department of Communication Sciences
and Disorders, University of South Carolina, Columbia, SC
29208, USA and 4Section Neuropsychology, Center for
Neurology, Hertie-Institute for Clinical Brain Research,
University of Tübingen, D 72076 Tübingen, Germany
1
Pantomime of tool use is a frequently used test for apraxia. For
basic cognitive neuroscience, pantomime of tool use is of interest
because it constitutes a link between instrumental and communicative manual actions. We used lesion subtraction analysis to
determine the locations specifically associated with defective
pantomime of tool use in patients with left-brain damage and
aphasia. Subtraction of lesions of patients with normal pantomime
from those with defective pantomime yielded a maximum difference in the inferior frontal gyrus and adjacent portions of the insula
and precentral gyrus. This result remained essentially the same
when possible confounding influences of impaired language
comprehension and of lesion size were controlled by selecting
patients equated on these measures and when only patients with
preserved imitation of gestures were considered. By contrast,
parietal lesions did not have a specific impact on pantomime. We
speculate that the vulnerability of pantomime to lesions of left
inferior frontal cortex is due to the high demands on selection of
a very restrained range of features out of the many features that
may come to mind when imagining the actual use of the tool.
Keywords: apraxia, frontal lobe, pantomime, parietal lobe, tool use
Introduction
For testing pantomime of tool use, subjects are requested to
shape their hand as if it would hold a tool and perform the
movements they would make when actually applying that tool.
Pantomime of tool use is a traditional test in clinical neurology
and neuropsychology (Liepmann 1908; Goodglass and Kaplan
1963; Geschwind 1975; Barbieri and De Renzi 1988; Roy and
Hall 1992; Heilman and Rothi 1993; Goldenberg et al. 2003),
which has recently moved into the focus of cognitive neuroscience (Moll et al. 2000; Choi et al. 2001; Rumiati et al. 2004;
Ohgami et al. 2004; Johnson-Frey et al. 2005; Fridman et al. 2006;
Lewis 2006; Hermsdörfer et al. forthcoming). Clinicians are
interested in pantomime because it is a sensitive test for apraxia
resulting from left-brain damage (LBD). Other manifestations of
apraxia are defective imitation of gestures and defective use of
tools and objects. For basic cognitive neuroscience, pantomime
of tool use is of interest because it constitutes a link between
instrumental and communicative manual actions. Pantomimes
are derived from the instrumental actions of actual use. They
are, however, communicative gestures in that they symbolize
the tool and the action rather than exerting any direct impact
upon external objects. The pantomime of tooth brushing does
not clean your teeth. Exploration of the neural basis of
pantomime promises insights into how our brain controls the
dual functions of our hands as instrumental and communicative
devices. The question whether these functions share neural
substrates is of particular interest in the light of speculations
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that human language has evolved from gestural communication
that in turn evolved from manipulation of external objects
(Rizzolatti and Arbib 1998).
A number of functional imaging studies have investigated
both the laterality and the intrahemispheric location of activations during pantomime of tool use (Moll et al. 2000; Choi et al.
2001; Rumiati et al. 2004; Ohgami et al. 2004; Johnson-Frey et al.
2005; Fridman et al. 2006; Lewis 2006; Hermsdörfer et al.
forthcoming). Lesion studies of patients with defective pantomime have established that in right-handed patients, it is bound
to LBD and virtually always associated with aphasia (Liepmann
1908; Goodglass and Kaplan 1963; Geschwind 1975; Barbieri
and De Renzi 1988; Roy and Hall 1992; Heilman and Rothi 1993;
Goldenberg et al. 2003). Several clinical studies have mapped
the intrahemispheric location of lesions that result in apraxia,
but these studies have not attempted to specify brain regions
required for pantomime. Some studies tested imitation of
pantomime and of meaningless gestures (Kolb and Milner
1981; Basso et al. 1985, 1987; Haaland et al. 2000), whereas
others used compound scores of imitation and pantomime to
command. Patients who failed production of pantomime to
command were asked to imitate the same gesture and were
given full credit when imitation succeeded (Heilman et al. 1982;
Kertesz and Ferro 1984; Alexander et al. 1992), or an average
score was computed from pantomime and imitation of meaningless gestures (Buxbaum et al. 2005). There is, however, robust
evidence that pantomime of tool use and imitation of gestures
can independently be affected by LBD (Barbieri and De Renzi
1988; Goldenberg and Hagmann 1997; Rothi et al. 1997). This
independence points to different cerebral substrates within the
left hemisphere. Combined scoring is thus likely to obscure the
location of brain regions specifically devoted to the production
of pantomime on command. The aim of the present study was to
elucidate the location of left-brain lesions impairing pantomime
independently from their effect on imitation of gestures.
Methods
Participants
Forty-four patients admitted to the ward or the day care clinics of the
Neuropsychological Department of Bogenhausen Hospital were included. Right-handed patients who had aphasia caused by a first leftsided cerebrovascular accident at least 3 weeks before were examined.
Patients were excluded when no magnetic resonance imaging (MRI)
could be obtained or when the MRI revealed bilateral or diffuse lesions.
All patients had a complete Aachen aphasia test (AAT) (Huber et al.
1983) within 14 days from the experimental tests. The patients or their
relatives gave their informed consent for participation in the study,
which was performed in accordance with the ethical standards laid
down in the 1964 Declaration of Helsinki. Demographic and clinical data
are provided in Table 1.
Table 1
Demographic and clinical data of all patients
Female/male
Age
Ischemia/bleeding
Lesion sizea
Weeks since lesion
Hand used: R/L
Classification of aphasia
Token testb
Repetitionb
Written languageb
Namingb
Comprehensionb
Imitation finger postures
Imitation hand postures
Pantomime of tool use
Pantomime defective
Pantomime normal
12/17
54.8 (14.6)
27/2
18.2 (8.2)
19.1 (23.6)
10/19
17 global; 3 Broca; 2 Wernicke;
5 amnesic; 2 other
26.7 (24.5)
26.0 (23.2)
24.9 (20.4)
20.4 (18.8)
29.8 (19.3)
13.6 (4.4)
14.7 (4.6)
27.8 (10.8)
5/10
53.0 (10.4)
13/2
11.6 (6.3)*
20.2 (23.1)
7/8
2 global; 1 Broca; 4 Wernicke;
4 amnesic; 4 other*
46.0 (25.8)*
46.9 (26.4)*
48.6 (22.0)**
48.6 (21.0)***
53.0 (27.1)*
16.7 (3.4)*
15.1 (4.8)
48.2 (3.1)***
Note: Values in parentheses are SDs.
a
Percentage of left hemisphere volume.
b
Subtests of AAT, results expressed in percentile of aphasic sample.
*P \ 0.05;
**P \ 0.01;
***P \ 0.001 (t-test).
Pantomime of Tool Use
Patients were asked to mime the use of 20 common tools or objects. The
examiner named the action and the object and simultaneously showed
a photograph of the object. This photograph was hidden from view
before subjects started miming.
Patients were asked to respond with the ipsilesional left hand when
restricted motility of the right hand interfered with the exactitude of
the pantomime. For evaluation, the examiner marked the presence or
absence of predefined features of the pantomime on an examination
sheet. For each item, 1 feature characterized grip and finger configuration, whereas the remaining 1--3 features concerned position and
movement of the whole hand (e.g., screwing in of an electric bulb:
spherical grip and rotation of the hand; cutting with scissors: bended
fingers with opposition of thumb, opening and closing of hand or
fingers, hand oriented perpendicular to table, and movement of whole
hand parallel to table—see Supplementary Material for complete scoring
sheet). Summed up across all 20 items, there were 55 features.
This task is a slightly adapted version of the task used by Goldenberg
et al. (2003). Interrater agreement for scoring had been found very
satisfactorily with the previous version for the number of correct
features per item (kappa = 0.61, P < 0.0001) as well as for the total score
summed up across all items (r = 0.94, P < 0.0001). Normative data for the
new version were obtained from 49 healthy controls (25 female, 24
male; mean age 49, standard deviation [SD] 11.4). Pantomime was
considered as defective when the score was below the fifth percentile of
this control group (45/55—see Supplementary Material for distribution
of control scores).
Imitation of Meaningless Gestures
Meaningless gestures were preferred for testing imitation because
imitation of meaningful gestures, like, for example, the pantomimes of
tool use, can be achieved by comprehension of the gesture’s meaning
and subsequent reproduction of a gesture with the same meaning out of
long-term memory. By contrast, imitation of meaningless gestures
compels to genuine imitation of the gesture’s shape (Goldenberg and
Hagmann 1997; Tessari and Rumiati 2004). Two variants of meaningless
gestures were tested: 10 hand postures required the patients to copy
different positions of the hand relative to the head and face while the
configuration of the fingers remained invariant. For imitation of 10 finger
postures, patients were asked to replicate different configurations of the
fingers. The position of the whole hand relative to the body was not
considered for scoring (see Supplementary Material for scoring sheet
with illustration of all postures).
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Goldenberg et al.
All patients imitated with their left arm and hand while the examiner
demonstrated the gestures ‘‘like a mirror’’ with his right hand: The
patients were allowed to start imitation as soon as the demonstration
was terminated. For correct imitation on first trial, 2 points was credited.
Otherwise, the demonstration was repeated and 1 point was given for
a successful second trial. Scoring considered only the final position of
the relevant body part and did not take into account hesitation,
searching movements, or self-corrections during the course of the
movement. In a previous study using the same test, interrater agreement
of scoring 92% for hand and 99% for finger gestures (Goldenberg and
Strauss 2002) was seen.
For determination of cutoff scores, we used previously published data
obtained by administration of the same test to 60 healthy controls (23
female, 37 male, mean age 54.4, SD 14.0; Goldenberg 1996). Imitation
was classified as disturbed when either hand or finger postures were
below the fifth percentile of the control group (18/20 for hand, 17/20
for fingers—see Supplementary Material for distribution of control
scores).
Lesion Analysis
MRI scans were obtained at the Bogenhausen Hospital’s radiological
service on a 1.0-T MR system (Magnetom Expert, Siemens, Erlangen,
Germany). The T2 sequence used for analysis of lesion location was
acquired with 19 axial slices (thickness 5 mm; interslice gap 1.5 mm),
a field of view of 201 3 230 mm2, matrix 224 3 512, a repetition time of
3600 ms, and an echo time of 96 ms. The minimum time between stroke
and imaging was 3 weeks; the average period for the 44 patients was
16.4 weeks (SD 17.0 weeks).
Mapping of lesions was carried out by one experimenter (H.-O.K.)
without knowledge of test results and clinical features of the patients.
Lesions were mapped using MRIcro software (Rorden and Brett 2000;
http://www.sph.sc.edu/comd/rorden/) on slices of a T1-weighted
template MRI scan from the Montreal Neurological Institute (http://
www.bic.mni.mcgill.ca/cgi/icbm_view). This template is approximately
oriented to match Talairach space (Talairach and Tournoux 1988) and is
distributed with MRIcro. The template scan provides various anatomical
landmarks for precisely plotting size and localization of the lesion.
Lesions were mapped onto the slices that correspond to z coordinates
–40, –32, –24, –16, –8, 0, 8, 16, 24, 32, 40, and 50 mm in Talairach
coordinates by using the identical or the closest matching transversal
slices of each individual.
To identify the structures that are commonly damaged in patients
with defective pantomime, we subtracted the superimposed lesions of
patients scoring within the control range from those scoring below the
cutoff score. Because there were less unimpaired than impaired
patients, we used proportional values for the MRIcro subtraction
analysis, which consequently yielded a percentage overlay plot (for
details concerning the subtraction technique, see Rorden and Karnath
2004). Automatic 3-dimensional rendering of the lesion data was carried
out using MRIcro.
Results
In the entire group of 44 patients, pantomime of tool use was
defective in 29 patients and within the normal range in 15
(Table 1). The accuracy of grip and finger configuration was
tightly related to the accuracy of hand position and movement
in patients with defective pantomime (r = 0.76, P < 0.0005), but
not in those who scored within the normal range (r = 0.33).
Table 1 compares demographic and clinical data as well as
lesion size between patients with defective and normal pantomime. Differences were evaluated by chi square- or t-test. There
were no differences of age, gender, time since lesion, etiology,
or hand used. Patients with defective pantomime had significantly larger lesions, and greater severity of aphasia was
reflected in lower scores on all AAT subtests. The distribution
of aphasia types differed. The proportion of global aphasia was
higher (P < 0.01) and that of Wernicke aphasia was lower (P <
0.05) in patients with defective pantomime than in those with
normal pantomime. Finally, imitation of finger but not of hand
postures was poorer in patients with defective pantomime.
Lesion Subtraction: Defective versus Normal Pantomime
Figure 1 shows the subtraction of lesions of patients with
normal pantomime from those with defective pantomime. The
highest difference of lesion density between patients with
defective and those with normal pantomime was found in the
opercular part of the inferior frontal gyrus (IFG), adjacent
portions of the insula and of the precentral gyrus, and white
matter below the precentral gyrus.
The remaining groups did not significantly differ on any
demographic or clinical measure (t-test or Fisher’s exact test, all
P > 0.2) except pantomime, but it is remarkable that there was
no patient with global or Broca aphasia and normal pantomime
and no patient with Wernicke aphasia and defective pantomime. Figure 2b shows the result of lesion subtraction. The
maximum differences between lesions associated with defective versus normal pantomime were located in the IFG, the
insula, putamen, superior temporal gyrus, the pre- and postcentral gyri, and white matter underlying the central gyri.
Discussion
Lesion Subtraction with Control for Lesion Size and
Language Comprehension
Table 1 shows that patients with defective and with normal
pantomime differed not only in their ability to mime tool use but
also in lesion size, severity of aphasia, and imitation of finger
postures. In a second step of analysis, we controlled for possible
influences of lesion size and language disturbance on lesion
location by exclusion of patients with extreme values on these
variables. We choose the AAT subtest language comprehension
as the primary target for equating severity of aphasia because
insufficient comprehension of verbal instructions is more likely
to have an influence on the nonverbal task of producing
pantomimes than the linguistic abilities assessed by the other
AAT subtests. There were 5 patients with defective pantomime
whose scores on language comprehension were lower than the
minimum score of patients with normal pantomime and 4
patients with normal pantomime whose comprehension scores
were higher than the maximum score of patients with defective
pantomime. These patients were discarded from the following
analysis. Furthermore, we excluded the 5 patients with defective pantomime who had the largest lesions and the 3 with
normal pantomime who had the smallest lesions. As 1 patient
with normal pantomime fulfilled both criteria, the total number
of excluded patients was 6 for normal and 10 for defective
pantomime. Demographic and clinical data of the remaining 28
patients are displayed in Table 2.
Comparison of lesion size and language comprehension
between the remaining patients with defective versus normal
pantomime revealed no significant differences (t-test; lesion
size: P = 0.10; comprehension: P = 0.51). Of the other clinical
and demographic variables, only differences of naming and of
imitation of finger postures came close to conventional significance levels (both P = 0.07). All other comparisons yielded
significance levels of P > 0.2.
Figure 2a shows the result of subtraction of patients with
normal pantomime from those with impaired pantomime.
Impaired pantomime was associated with higher density of
lesion overlap in the IFG, insula, and pre- and postcentral gyri.
Lesions Causing Defective Pantomime in Patients with
Preserved Imitation
To exclude any potential influences of impaired imitation on
the pattern of lesion location associated with defective pantomime and to highlight only locations exclusively related to
pantomime, we conducted a third subtraction analysis considering only patients with normal imitation. Of 11 patients who
imitated both hand and finger postures within the normal range,
6 showed defective and 5 normal pantomime. Demographic and
clinical data of these patients are displayed in Table 3.
We analyzed the location of lesions causing defective pantomime of tool use in 3 steps with increasingly stringent control
for possible confounding variables. Analysis of unselected
patients provided a large sample size but did not control for
the possible influences of confounding variables. Tightening of
selection criteria led to a decrease of sample size, which carries
a risk of overrating anatomical variation in individual patients.
However, consistent findings across the different comparisons
pointed to reliable results: All 3 analyses agreed that pantomime
of tool use depends on integrity of the IFG and adjacent
portions of the insula and the precentral gyrus.
The area of lesion overlap further extended into the underlying white matter. Thus, it is possible that damage of projections to or from cortical areas contributed to pantomime
disturbance (Liepmann 1905; Geschwind 1975; Catani and
ffytche 2005). Future studies using diffusion tensor tractography and magnetic resonance perfusion techniques will be necessary to clarify the possible role of fiber tract lesions for
pantomime of tool use.
Our analysis demonstrates regions that are damaged more
frequently in patients with defective pantomime than in
patients who likewise have brain damage but do not show the
disorder (Rorden and Karnath 2004). As any analysis based on
group comparisons, it does not exclude the possibility of
defective pantomime in single patients with lesions in other
regions. Nevertheless, our finding that frontal but not parietal
regions are crucial for intact pantomime is difficult to reconcile
with the proposal that the parietal lobe stores representations
of tool-related hand shapes and movements, which are needed
for actual tool use as well as for the demonstration of tool use by
pantomime (Heilman et al. 1982; Buxbaum et al. 2005). Our
failure to find an influence of parietal lesions on pantomime is
unlikely to be due to a general underrepresentation of such
lesions in our patient sample. In a companion study (Goldenberg and Karnath 2006), we examined the same group of
patients in order to determine the location of lesions impairing
the imitation of hand and finger postures. That analysis revealed
a predominance of inferior parietal lesions in patients with
defective imitation of hand postures. The conclusion that left
parietal lesions affect imitation of gestures but not pantomime is
corroborated by single case reports of patients with left parietal
lesions who had severe difficulties with imitation of meaningless
gestures but could produce pantomimes perfectly (Mehler
1987; Goldenberg and Hagmann 1997; Peigneux et al. 2000).
The absence of a prominent effect of parietal lesions on
pantomime appears at odds with recent functional imaging
studies, which consistently showed left parietal activation when
neurologically healthy individuals mime the use of tools (Moll
et al. 2000; Choi et al. 2001; Rumiati et al. 2004; Ohgami et al.
Cerebral Cortex December 2007, V 17 N 12 2771
Figure 1. (a) Overlay lesion plots of all patients with disturbed pantomime (n 5 29) and normal pantomime (n 5 15) investigated in the present study. The number of overlapping
lesions is illustrated by different colors coding increasing frequencies from violet (n 5 1) to red (n 5 maximum number of subjects in the respective group). (b) Overlay plot of the
subtracted superimposed lesions of the group of patients with disturbed pantomime minus the group with normal pantomime. The percentage of overlapping lesions of the patients
with disturbed pantomime after subtraction of the group with normal pantomime is illustrated by 5 different colors coding increasing frequencies from dark red (difference 5
1--20%) to bright yellow (difference 5 81--100%). Each color represents 20% increments. The different colors from dark blue (difference 5 1% to 20%) to light blue (difference
5 81% to 100%) indicate regions damaged more frequently in the group of patients with normal pantomime than in the group with disturbed pantomime. Talairach coordinates
(Talairach and Tournoux 1988) of the transverse sections are given. Ins, insula; PrCG, precentral gyrus; and Wh.mat., white matter.
2004; Johnson-Frey et al. 2005; Fridman et al. 2006; Hermsdörfer
et al. forthcoming). For these studies, subjects were lying in
a scanner without visual feedback from their manual action and
the space surrounding it. Furthermore, to avoid head movements, they were not allowed to move the arm at the shoulder
and consequently had to perform all gestures within the space
between chest and waist. These restrictions afford a transposi2772 Pantomime of Tool Use
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Goldenberg et al.
tion of movement trajectories into a reference frame centered
on the supine trunk of the own body, whereas in clinical testing
and in gestural communication, actions are directed toward
other body parts—for example, the mouth and face in tooth
brushing or drinking—or are constructed with reference to the
basic coordinates of external space, which are indicated by
horizontal and vertical surfaces of surrounding objects. Parietal
activation could be related to such additional demands on
body-centered spatial transformations (Bonda et al. 1995;
Alivisatos and Petrides 1997; Felician et al. 2004; Goldenberg
and Karnath 2006). A further difference that possibly influences
the weight given to the contributions of different brain regions
Table 2
Demographic and clinical data of patient groups equated for lesion size and language
comprehension
Female/male
Age
Ischemia/bleeding
Lesion sizea
Weeks since lesion
Hand used: R/L
Classification of aphasia
Token testb
Repetitionb
Written languageb
Namingb
Comprehensionb
Imitation finger postures
Imitation hand postures
Pantomime of tool use
Pantomime defective
Pantomime normal
10/9
53.4 (15.4)
17/2
15.4 (7.3)
14.1 (23.6)
7/12
9 global; 3 Broca; 1 Wernicke;
5 amnesic; 1 other
32.5 (26.6)
30.3 (24.7)
30.1 (21.9)
24.8 (21.1)
34.2 (19.6)
14.1 (4.8)
15.2 (2.0)
30.1 (10.3)
5/4
53.8 (12.1)
7/2
12.3 (2.3)
22.4 (27.7)
6/3
2 global; 0 Broca; 3 Wernicke;
3 amnesic; 1 other
38.6 (24.0)
43.8 (26.4)
40.3 (20.3)
42.7 (22.6)
39.7 (22.5)
17.4 (2.9)
14.8 (4.0)
46.9 (2.5)***
Note: Values in parentheses are SDs.
Percentage of left hemisphere volume.
b
Subtests of AAT, results expressed in percentile of aphasic sample.
***P \ 0.001.
a
concerns the timing of pantomimes. In the functional imaging
studies, the time for 1 pantomime ranged from 2 to 6 s. In
contrast, evaluation of video-recorded tests showed that aphasic
patients frequently needed more than 10 s for completion of
a pantomime. It may be speculated that the fast pace of testing
in functional magnetic resonance imaging (fMRI) studies highlighted the activity of regions whose contributions can be
replaced by compensatory mechanisms when pantomimes are
produced without time limits.
However, both our research and the functional imaging
studies convergently suggest a prominent role of the left IFG
and adjacent portion of the insula and the precentral gyrus for
pantomime. With the exception of 2 early studies (Moll et al.
2000; Choi et al. 2001), all subsequent fMRI studies of
pantomime in normal subjects documented activations of left
premotor and frontal opercular regions largely overlapping with
the regions whose integrity we found to be essential for correct
pantomime (Rumiati et al. 2004; Ohgami et al. 2004; JohnsonFrey et al. 2005; Fridman et al. 2006; Hermsdörfer et al.
forthcoming). Our lesion study demonstrates that activity
within these areas is not only correlated with but also necessary
for pantomime of tool use.
Ventral premotor cortex and the opercular portion of IFG
have been proposed to be the repository of a ‘‘vocabulary’’ of
motor actions (Binkowski et al. 2000; Rizzolatti and Luppino
2001), which serves for translating information about object
properties and action goals into combinations of motor programs
Figure 2. (a) Overlay plot of the subtracted superimposed lesions of subsamples of patients with disturbed pantomime (n 5 19) minus a group with normal pantomime (n 5 9)
who were equated for lesion size and language comprehension. (b) Overlay plot of the subtracted superimposed lesions of subsamples of patients with disturbed pantomime (n 5 6)
minus a group with normal pantomime (n 5 5) who all showed normal imitation. The percentage of overlapping lesions of the patients with disturbed pantomime after subtraction
of the group with normal pantomime is illustrated by different colors coding increasing frequencies as described in Figure 1. Talairach coordinates (Talairach and Tournoux 1988) of
the transverse sections are given. Ins, insula; Pu, putamen; PrCG, precentral gyrus; PoCG, postcentral gyrus; and Wh.mat., white matter.
Cerebral Cortex December 2007, V 17 N 12 2773
Table 3
Demographic and clinical data of patients with normal imitation
Female/male
Age
Ischemia/bleeding
Lesion sizea
Weeks since lesion
Hand used: R/L
Classification of aphasia
Token testb
Repetitionb
Written languageb
Namingb
Comprehensionb
Imitation finger postures
Imitation hand postures
Pantomime of tool use
Pantomime defective
Pantomime normal
3/3
45.8 (15.4)
6/0
14.5 (9.2)
24.2 (37.5)
3/3
3 global; 1 Broca; 0 Wernicke;
2 amnesic; 0 other
50.3 (24.7)
38.8 (20.5)
48.3 (27.4)
38.7 (29.9)
54.5 (19.1)
18.0 (1.3)
19.3 (0.8)
36.2 (7.9)
4/1
53.4 (4.2)
5/0
9.5 (2.5)
23.2 (36.6)
2/3
0 global; 0 Broca; 2 Wernicke;
2 amnesic; 1 other
46.6 (35.8)
49.2 (29.4)
60.0 (16.2)
46.6 (9.2)
60.2 (22.2)
19.0 (1.4)
19.4 (0.5)
49.6 (3.2)**
Note: Values in parentheses are SDs.
Percentage of left hemisphere volume.
Subtests of AAT, results expressed in percentile of aphasic sample.
**P \ 0.01.
a
b
specifying the type of grip and the directions and sequences
of manual actions. It would be tempting to ascribe the deficiency of pantomime following lesions in this location to a
loss of this vocabulary. However, as such a vocabulary develops primarily for enabling actual use of tools and objects,
its destruction should affect actual tool use at least as much
as miming. In contrast, many patients with defective pantomime improve dramatically when allowed to manipulate the
tools (Liepmann 1908; De Renzi et al. 1982; Goldenberg and
Hagmann 1998; Goldenberg et al. 2004). Apparently, pantomime requires cognitive and neural functions that are not
needed for actual tool use.
Both actual use and pantomime are based on knowledge
about objects and their function. In actual tool use, this prior
knowledge influences selection of motor programs that control
the interactions between manual movements and object’s
properties. For example, when grasping a glass, scaling of grip
width to the width of the glass is achieved by first opening the
hand in proportion to, but wider than, the visually perceived
width of the glass and then closing it around the glass. Opening
and closing are precisely synchronized with the transport
movement of the whole hand (Jeannerod 1988), and the
strength of the final grip is finely adapted to surface friction
and estimated weight of the glass (Johansson and Westling
1984). In pantomime, knowledge about objects and their
functions is transformed into motor actions that demonstrate
the distinctive features of the object and its use. Thus, when
miming to grasp a glass, normal subjects open their hand to the
approximate width of the pretended glass at the start of the
transport movement and stop the transport at its pretended
location without further changing the aperture of their grip
(Goodale et al. 1994; Laimgruber et al. 2005). The width of the
aperture demonstrates the width of the glass, and stopping the
transport of the hand suffices for indicating the grasp. Pantomime neglects features of object use that are important for
manipulation but have little value for discriminating the object,
whereas it specifies features that in actual use are determined
by the manipulated object. For example, consider the case of
ironing: the distance of the hand to the table is determined by
the height of the iron, but when ironing is mimed, a distance
must be chosen without external support. If this distance falls
2774 Pantomime of Tool Use
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Goldenberg et al.
outside the usual range of iron heights, the pantomime will
become unrecognizable. The need to demonstrate features of
the action that are hardly attended to in actual use makes
pantomime a nonroutine task even when tested for tools that
are frequently used in daily living. A further difficulty for
selection of appropriate manual actions is posed by the restriction to manual actions which also occur in actual tool use.
For example, it is not permitted to indicate the size and shape of
the iron by drawing its outline in the air before demonstrating
the manner of use.
We propose that IFG injury disturbs the selection of
distinctive features of the object and its use, leading to impaired
pantomime. Functional imaging studies have consistently
shown activation of the left IFG in tasks demanding active
retrieval of information from semantic memory as, for example,
generation of words belonging to a particular semantic category
(Cabeza and Nyberg 2000; Thompson-Schill 2003; Cappa and
Perani 2006). With increasing demands on selection between
competing alternatives, IFG activity in normal subjects increases
and performance of patients with IFG lesions deteriorates
(Thompson-Schill et al. 1998; Kan et al. 2006). Pantomime of
tool use can be conceived as one instance of active retrieval
from semantic memory. From the repository of knowledge
about objects and their functions, those features have to be
selected that permit recognition of both the object and the
manner it is used and that can be demonstrated by manual
actions, which are also part of its actual use. On this view, the
vulnerability of pantomime to lesions of the left IFG is due to the
high demands on selection of a very restrained range of features
out of many closely related features that may come to mind
when imagining the actual use of the tool.
Our companion study on localization of lesions interfering
with imitation revealed that defective imitation of finger
postures was associated with lesions similar to those we found
responsible for defective pantomime, namely, the IFG as well as
the insula and underlying subcortical extension into the putamen and caudate nucleus (Goldenberg and Karnath 2006).
Interestingly, the fMRI studies that did not find IFG activation by
pantomime (see above) both used sequences of single finger
movements as the control condition (Moll et al. 2000; Choi et al.
2001). Possibly the similarity of IFG activation by finger movements and by pantomime obscured the contribution of IFG to
pantomime. In the present analysis, we found that imitation of
finger postures was worse in patients with defective pantomime
than in those with intact pantomime, whereas there was no
such difference with respect to imitation of hand postures (see
Tables 1 and 2). The importance of lesions to left IFG, insula, and
precentral gyrus for defective pantomime remained obvious
when we analyzed only patients who had imitated both hand
and finger postures normally. Nonetheless, the closely related
lesion sites responsible for defective pantomime and for defective imitation of finger postures may indicate a similarity of
functional mechanisms underlying impairment in both tasks.
Finger configurations are composed of a limited set of uniform
elements that differ only in their serial position. The resulting
similarity between different finger configurations makes them
vulnerable to interference and renders selection of the currently correct one difficult. This leads to the speculation that
the common difficulty that renders both pantomime of tool use
and imitation of finger configurations susceptible to lesions of
IFG and neighboring regions concerns selection between
closely related and hence competing alternatives.
Taken together, the findings of the present and the companion study indicate that pantomime of tool use, imitation of hand
postures, and imitation of finger postures rely on different
neural and cognitive mechanisms. Traditionally, their disturbances are subsumed under the common label of ‘‘ideomotor
apraxia,’’ and sum scores from various combinations of these
different tasks are proposed for the clinical examination of
apraxia (Heilman et al. 1982; Kertesz and Ferro 1984; Alexander
et al. 1992; Buxbaum et al. 2005). Our findings add to the
growing evidence that such combinations prohibit insights into
the specific neural and cognitive mechanisms underlying
competency for different domains of manual actions (De Renzi
et al. 1982; Barbieri and De Renzi 1988; Rumiati et al. 2005; Della
Sala et al. 2006).
Supplementary Material
Supplementary material can be found at: http://www.cercor.oxfordjournals.org/.
Notes
This work was supported by the Deutsche Forschungsgemeinschaft
(968/2-1 to G.G. and SFB 550-A4 to H.-O.K.) and the Medical Faculty of
the University of Tübingen. Conflict of Interest: None declared.
Address correspondence to Georg Goldenberg, MD, Neuropsychological Department, Bogenhausen Hospital, Englschalkingerstrasse
77, D 81925 München, Germany. Email: [email protected].
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