doi:10.1093/brain/awu203
Brain 2014: 137; 2796–2810
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BRAIN
A JOURNAL OF NEUROLOGY
Neural bases of imitation and pantomime in acute
stroke patients: distinct streams for praxis
Markus Hoeren,1,2,3 Dorothee Kümmerer,1,2 Tobias Bormann,1,2 Lena Beume,1,2
Vera M. Ludwig,1,2 Magnus-Sebastian Vry,2,4 Irina Mader,2,5 Michel Rijntjes,1,2
Christoph P. Kaller1,2,3 and Cornelius Weiller1,2,3
1
2
3
4
5
Department of Neurology, University Medical Centre Freiburg, Germany
Freiburg Brain Imaging Centre, University of Freiburg, Germany
BrainLinks-BrainTools Cluster of Excellence, University of Freiburg, Germany
Department of Psychiatry, University Medical Centre Freiburg, Germany
Department of Neuroradiology, University Medical Centre Freiburg, Germany
Correspondence to: Dr Markus Hoeren, MD,
Department of Neurology,
University Medical Centre Freiburg,
Breisacher Strasse 64,
79106 Freiburg,
Germany
E-mail: [email protected]
Apraxia is a cognitive disorder of skilled movements that characteristically affects the ability to imitate meaningless gestures, or
to pantomime the use of tools. Despite substantial research, the neural underpinnings of imitation and pantomime have
remained debated. An influential model states that higher motor functions are supported by different processing streams. A
dorso-dorsal stream may mediate movements based on physical object properties, like reaching or grasping, whereas skilled tool
use or pantomime rely on action representations stored within a ventro-dorsal stream. However, given variable results of past
studies, the role of the two streams for imitation of meaningless gestures has remained uncertain, and the importance of the
ventro-dorsal stream for pantomime of tool use has been questioned. To clarify the involvement of ventral and dorsal streams in
imitation and pantomime, we performed voxel-based lesion–symptom mapping in a sample of 96 consecutive left-hemisphere
stroke patients (mean age SD, 63.4 14.8 years, 56 male). Patients were examined in the acute phase after ischaemic stroke
(after a mean of 5.3, maximum 10 days) to avoid interference of brain reorganization with a reliable lesion–symptom mapping
as best as possible. Patients were asked to imitate 20 meaningless hand and finger postures, and to pantomime the use of 14
common tools depicted as line drawings. Following the distinction between movement engrams and action semantics, pantomime errors were characterized as either movement or content errors, respectively. Whereas movement errors referred to
incorrect spatio-temporal features of overall recognizable movements, content errors reflected an inability to associate tools
with their prototypical actions. Both imitation and pantomime deficits were associated with lesions within the lateral occipitotemporal cortex, posterior inferior parietal lobule, posterior intraparietal sulcus and superior parietal lobule. However, the areas
specifically related to the dorso-dorsal stream, i.e. posterior intraparietal sulcus and superior parietal lobule, were more strongly
associated with imitation. Conversely, in contrast to imitation, pantomime deficits were associated with ventro-dorsal regions
such as the supramarginal gyrus, as well as brain structures counted to the ventral stream, such as the extreme capsule. Ventral
stream involvement was especially clear for content errors which were related to anterior temporal damage. However, movement
Received April 12, 2014. Revised June 10, 2014. Accepted June 16, 2014. Advance Access publication July 24, 2014
ß The Author (2014). Published by Oxford University Press on behalf of the Guarantors of Brain. All rights reserved.
For Permissions, please email: [email protected]
Imitation and pantomime in acute stroke
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errors were not consistently associated with a specific lesion location. In summary, our results indicate that imitation mainly
relies on the dorso-dorsal stream for visuo-motor conversion and on-line movement control. Conversely, pantomime additionally
requires ventro-dorsal and ventral streams for access to stored action engrams and retrieval of tool-action relationships.
Keywords: apraxia; imitation; pantomime; ventral stream; voxel-based lesion–symptom mapping
Abbreviations: IPL = inferior parietal lobule; IPS = intraparietal sulcus; LOTC = lateral occipito-temporal cortex; SPL = superior parietal lobule; VLSM = voxel-based lesion–symptom mapping
Introduction
Deficits in the ability to pantomime the use of tools or imitate
meaningless gestures are key features of apraxia, a cognitive disorder of skilled movements not explained by lower-level impairments such as paresis or ataxia (Rothi et al., 1991; Cubelli et al.,
2000; Leiguarda and Marsden, 2000; Goldenberg, 2009).
However, despite more than a century of research, the exact localizations of brain lesions leading to different forms of apraxic
deficits are still debated.
A recent model proposes that higher motor functions are supported by distinct dorso-dorsal and ventro-dorsal processing
streams (Buxbaum and Kalénine, 2010; Binkofski and Buxbaum,
2012). Anatomically, first based on data from macaques (Rizzolatti
and Matelli, 2003) and later corroborated by data from humans
(for review see Binkofski and Buxbaum, 2012), the dorso-dorsal
stream is thought to consist of projections from visual areas like
area V6 to regions within the intraparietal sulcus and superior
parietal lobule, and from there to the dorsal premotor cortex.
Conversely, the ventro-dorsal stream originates from area MT/
V5 + and traverses through inferior parietal lobule (IPL) to the
ventral premotor cortex. Functionally, the dorso-dorsal stream is
suggested to maintain on-line sensorimotor representations of the
postural alignment of different body parts, and to convert physical
object properties such as location or size into appropriate motor
commands for reaching. Optic ataxia, characterized by misreaching (Karnath and Perenin, 2005), is considered the hallmark deficit
ensuing damage to the dorso-dorsal stream. The ventro-dorsal
stream, on the other hand, is thought to contain long-term representations of skilled actions. Disruptions may lead to impairments in pantomime of tool use and actual tool use (Binkofski
and Buxbaum, 2012).
In contrast to object-associated actions, however, the involvement of the two streams in imitation of meaningless gestures
(henceforth: imitation) remains a matter of debate, as different
studies found an involvement of either dorso-dorsal and ventrodorsal areas (Hermsdörfer et al., 2001; Heiser et al., 2003;
Peigneux et al., 2004; Chaminade et al., 2005; Iacoboni, 2005;
Molnar-Szakacs et al., 2005; Mühlau et al., 2005; Goldenberg and
Karnath, 2006; Tessari et al., 2007; Molenberghs et al., 2010;
Buxbaum et al., 2014). Furthermore, behavioural and anatomical
dissociations between meaningless hand- or finger postures cast
doubt on the assumption of one single pathway for imitation
(Goldenberg, 1996, 1999; Goldenberg and Karnath, 2006).
In addition, the association of pantomime deficits with the inferior parietal lobule, a core region of the ventro-dorsal stream has
been questioned (Goldenberg, 2009, 2013), as lesion studies instead indicated a prominent role of the inferior frontal gyrus
(Goldenberg et al., 2007) or the posterior temporal lobe and
extrastriate cortex (Buxbaum et al., 2014) for pantomime.
Moreover, the involvement of the different streams in conceptual
aspects of pantomime and other tool-associated actions has remained unclear (Heilman et al., 1997). Some authors proposed
that incorrect object-action associations, such as combing one’s
hair with a toothbrush, result from damage to action representations stored in ventro-dorsal areas (Buxbaum, 2001; Buxbaum and
Kalénine, 2010; Binkofski and Buxbaum, 2012); others, however,
claimed that the ventral stream, originally proposed to mediate the
perceptual identification of objects (Goodale and Milner, 1992), is
crucial for the selection of actions while the dorsal stream is only
needed for the implementation of these actions (Milner and
Goodale, 2008). The latter view may be concordant with the
growing recognition of functionally distinct ventral and dorsal networks for different aspects of cognitive domains like language
(Saur et al., 2008; Kümmerer et al., 2013), action recognition
and imagination (Vry et al., 2012; Hoeren et al., 2013), or attention (Umarova et al., 2010). These reports have led to the concept
of a functionally more broadly defined ventral stream (Weiller
et al., 2009, 2011; Rijntjes et al., 2012) that anatomically, may
also comprise superior and middle temporal regions, ventrolateral
prefrontal cortex (Saur et al., 2008; Rauschecker and Scott, 2009),
as well as other areas connected by the extreme capsule or the
uncinate fascicle (Rijntjes et al., 2012 for review).
Several methodological challenges may have contributed to this
unresolved debate. In functional neuroimaging studies, the identification of areas critical to a neuropsychological function may be hampered by frequent coactivation of areas not essential to the task
(Rorden and Karnath, 2004). In lesions studies with subacute or
chronic patients (Goldenberg and Karnath, 2006; Goldenberg
et al., 2007; Manuel et al., 2013; Buxbaum et al., 2014), a shift
of functions to other areas (Raineteau and Schwab, 2001; Saur
et al., 2006) and spatial deformations within the affected hemisphere may impede precise lesion–symptom mapping (Rorden and
Karnath, 2004). Moreover, advanced voxel-based methods for lesion
analysis have only been developed in recent years, and require relatively large numbers of patients as well as sophisticated methods for
lesion delineation (Rorden et al., 2007). Possibly for those reasons,
only few studies investigating apraxic syndromes have used voxelbased statistics (Goldenberg, 2009; Manuel et al., 2013; Mengotti
et al., 2013), resorting to descriptive comparisons such as lesion
subtraction (Buxbaum et al., 2005; Goldenberg and Karnath,
2006; Goldenberg et al., 2007; Tessari et al., 2007).
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To overcome these limitations, we conducted a prospective
study with 102 acute left hemisphere stroke patients. To our
knowledge, this is the first study to investigate pantomime and
imitation using voxel-based lesion–symptom mapping (VLSM) in
acute stroke patients. Patients were tested as early as possible, i.e.
within a mean interval of 5.3 days (maximum 10) after stroke to
evade effects of brain reorganization. Lesions were carefully
mapped on diffusion-weighted magnetic resonance images obtained within the first 9 days post-stroke to avoid anatomical alterations as much as possible. Patients underwent testing for
imitation of hand and finger postures, as well as a picture-based
test for pantomime of tool use. Reflecting the concept of separate
neural correlates for motor engrams and action semantics (Rothi
et al., 1991), pantomime errors were grouped into the two categories of movement errors and content errors (Heilman et al.,
1997). As imitation of meaningless gestures relies on intact postural representations of the different body parts and requires the
conversion of visual input into motor commands without access to
stored action engrams, we hypothesized that imitation would
mainly rely on the dorso-dorsal stream, thus possibly extending
the concept of the dorso-dorsal stream to account not only for
optic ataxia, but also for imitation deficits. Conversely, we postulated that pantomime, while also requiring dorso-dorsal functions
(Buxbaum et al., 2000), additionally involves motor engrams
stored in ventro-dorsal areas, as well as, possibly, semantic knowledge processed in the ventral stream. In particular, we postulated
an association of ventro-dorsal damage with movement errors
indicating a disruption of the motor engram (Binkofski and
Buxbaum, 2012), whereas content errors, reflecting the inability
to correctly associate tools with their prototypical actions, may be
associated with areas and their connections in the ventral stream
(Milner and Goodale, 2008).
Materials and methods
Patients
Patients were consecutively recruited from the Stroke Unit of the
Department of Neurology at the University Medical Centre of
Freiburg, Germany. During a screening-period of 2.5 years (February
2011 to October 2013) we identified 364 patients with embolic left
hemisphere stroke. From this cohort, 260 patients were excluded due
to the following reasons: (i) age 490 years (n = 8); (ii) reduced general health status (n = 24); (iii) previous infarcts (n = 71); (iv) pre-existing structural brain changes (e.g. severe brain atrophy, extensive white
matter changes, previous brain injury) (n = 58); (vi) major cognitive
impairment (n = 15); (vii) haemodynamic alterations (e.g. carotid occlusion with insufficient collateralization) (n = 1); and (viii) other reasons, e.g. contraindications for MRI, compliance issues, or technical
problems (n = 83). The remaining 104 patients received neuropsychological testing. Of these, we had to exclude two patients due to excessive sleepiness during the examination, and six patients were
excluded from further analyses due to object agnosia (see below).
Extra- and intracranial ultrasound examinations and available magnetic
resonance or CT angiograms were reviewed to ensure sufficient cerebral blood flow at the time of behavioural testing in all cases. In total,
here we report data of 96 included patients. Taking into account their
M. Hoeren et al.
overall health status, patients were tested as soon as possible after
admission, mean standard deviation (SD) 5.3 1.9 days poststroke (min 2, max 10 days). Of the 96 patients included, all underwent imitation testing and 95 completed testing for pantomime of tool
use. Full written consent was obtained from all patients and control
subjects. In cases of severe aphasia, detailed information was given to
the patient’s relatives or the legal guardian. The study was approved
by local ethics authorities.
Behavioural testing
Testing procedures
All patients were tested by one of three specially trained occupational
therapists with extensive experience in working with stroke patients.
For scoring, performances of 86/96 patients were videotaped and
evaluated separately by two raters (M.H. and V.M.L.). V.M.L. was
blind to location and extent of the stroke. The items which had
been scored differently by the two raters were reviewed jointly by
both raters and a consensus rating was established that was used
for subsequent analyses. The remaining 10 patients who either
declined being recorded on video or could not be filmed due to technical reasons were scored directly by the examining occupational therapist. All examiners were familiarized with the scoring system before
starting the study.
Imitation of meaningless gestures
For imitation of meaningless hand and finger postures, an adaptation
of a previously published test was used (Goldenberg and Strauss,
2002; Goldenberg and Karnath, 2006). The test could be performed
with minimal or even without verbal instructions, and comprised two
subtests, one with 10 positions of the hand relative to the head with
invariant finger position (ImiHand) and one with 10 finger postures
(ImiFinger). The gestures were presented by the examiner with the
contralateral hand compared to the patient, i.e. ‘like a mirror’.
Patients always used the left hand for imitation of meaningless gestures. According to Goldenberg’s original instructions, the examiner
finishes his demonstration before the patient starts imitating
(Goldenberg, 2001; Goldenberg and Strauss, 2002). To reduce working memory load and effect of attention that both may be affected in
acute stroke patients, in this study, the examiners kept the hand or
finger position until the patient had reached his final position. For each
item, two points were scored for correct imitation, one point was
given if the patient reached the correct posture after a second demonstration of the posture (Goldenberg and Strauss, 2002; Goldenberg
and Karnath, 2006). Inter-rater reliability in terms of rank correlations
(Kendall’s ) was good to excellent for both ImiHand ( = 0.800) and
ImiFinger ( = 0.846). Normative data were obtained from 30 elderly
subjects (Supplementary material).
Pantomime of tool use
Pantomime was tested using a modified version of the test developed
by Bartolo et al. (2008), which could also be performed with minimal
or even without verbal instructions. Patients were asked to mime the
use of 14 tools depicted as line drawings. For aphasic patients, the task
was repeatedly demonstrated by means of two example items until the
patient had understood the instructions. The drawing of the current
item was kept in view for the entire time while the patient pantomimed its use. Items were scored in all cases in which the patient
produced an overall recognizable movement. In case aphasic patients
showed no clear response or an unrecognizable movement, the item
was scored if the patient responded with overall recognizable
Imitation and pantomime in acute stroke
pantomimes to other test items, or, alternatively, if the instructions of
the other tests (imitation, Birmingham Object Recognition Battery
subtest 11, Corsi, see below) were readily understood. In this respect,
our approach followed the study by Heilman et al. (1997) who used a
tool-to-silhouette matching task to rule out object agnosia, and an
imitative block-stacking test to ascertain that the patients could
follow non-verbal commands. Similarly to a previous study (Goldenberg et al., 2007), patients were prompted to use the left hand if
paresis or fine motor coordination (which were tested beforehand)
interfered with performance. Even though right hand use may constitute a confounding factor when comparing pantomime with imitation
of meaningless gestures (performed with the left hand, see above),
this strategy was adopted as some patients, probably being highly
accustomed to using the right hand for everyday actions, insist on
using the right hand for pantomime. See Supplementary material for
normative data and rationale for modifications to the original test.
Error classification and scoring
Each item was marked as either correct (1 point) or incorrect (0
points). Incorrect items were grouped into two categories. First,
‘Content errors’ included semantic errors (i.e. categorically wrong
movements such as hammering upon the presentation of a knife),
no response, and non-recognizable movements (e.g. amorphous, hesitant back-and forth or side-to-side movements without resemblance to
the tool-associated action) (Heilman et al., 1997). ‘Movement errors’
referred to overall recognizable actions that were flawed in terms of
the hand configuration (e.g. using a whole hand grip when writing
with a pen), orientation (e.g. cutting side-to-side instead of back-andforth), distance (e.g. too little distance between hand and table when
ironing), or movement (e.g. not moving the fingers when playing the
piano). Three different scores were calculated (maximum 14 points for
each score): the number of correct items (PantoComplete), the
number of items without content error (Content score), and the
number of items without movement error (Movement score). Interrater reliability was good to excellent for total pantomime scores
( = 0.800) and the number of content errors ( = 0.824) but borderline for the number of movement errors ( = 0.680).
Additional tests
Additional tests included the Corsi block tapping test for short-term
and working memory (Kessels et al., 2000, 2008), subtest 11 of the
Birmingham Object Recognition Battery for object recognition
(Riddoch and Humphreys, 1993), and three paper-based neglect
tests, i.e. the Bells Test (Gauthier et al., 1989), Albert’s line cancellation test (Albert, 1973) and the Ota test (Ota et al., 2001). Of 96
patients, 92 completed the Token Test of the Aachen Aphasia Battery
(Huber et al., 1984); of the remaining four patients, two were rapidly
discharged and two were unable to complete testing.
MRI
For a detailed description of the number and modality of images obtained, see the online Supplementary material. In sum, lesions were
mapped on MRI scans obtained on average 1.9 days after symptom
onset (SD 2.8, min 0 max 9 days). MRI scans were obtained on
either a 3 T Trio scanner, or on a 1.5 T Avanto scanner (Siemens).
For the diffusion-weighted imaging obtained in 95 patients, we used
a standard sequence (23 slices, matrix = 128 128 pixel, voxel
size = 1.8 1.8 5 mm, repetition time = 3.1 s, echo time = 79 ms,
flip angle = 90 , six diffusion-encoding gradient directions with a
b-factor of 1000 s/mm2). All patients received FLAIR images (repetition time = 9000 ms, echo time = 93.0 ms, flip angle = 140 , matrix
Brain 2014: 137; 2796–2810
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200 256 pixel, voxel size = 0.94 0.94 5.00 mm, 23 slices).
As a prerequisite for spatial normalization, a high-resolution T1 anatomical scan was obtained from 91 patients (repetition time =
2200 ms, echto time = 2.15 ms, flip angle = 12 , matrix = 256 256
pixel, voxel size = 1 1 1 mm, 176 slices).
Lesion analysis
First, a rough delineation of the diffusion-weighted imaged lesion was
performed using a customized region-of-interest toolbox implemented
in SPM8 (http://www.fil.ion.ucl.ac.uk/spm/software/spm8). Individual
intensity thresholds were applied to find the best match between the
binary lesion map and the diffusion-restricted brain tissue.
Subsequently, the lesions maps were inspected in MRIcron (http://
www.cabiatl.com/mrico/mricon/stats.html) and manually adjusted if
necessary. In one case, no diffusion weighted image was available
and the lesion was drawn directly onto a FLAIR image.
For spatial normalization of the lesion maps, the underlying diffusion-weighted imaging scan (or FLAIR image) was co-registered to the
anatomical T1 scan (n = 91). High-resolution T1 scans were segmented
using the VBM8 toolbox (r435; http://dbm.neuro.uni-jena.de/vbm/
download/). Deformation field parameters for nonlinear normalization
into the stereotactic Montreal Neurological Institute (MNI) standard
space were then computed using the DARTEL (diffeomorphic anatomical registration through exponentiated lie algebra; Ashburner, 2007)
approach implemented in VBM8. Normalization quality of lesion maps
was visually checked by M.H. In five cases in which no T1 scan of
sufficient quality was available, parameters for normalization were obtained using FLAIR images. As smaller diffusion restricted areas may be
indiscernible in chronic MRI scans or CT scans, our approach of mapping lesions on acute diffusion weighted images may contribute significantly to a more precise determination of lesion locations compared
to previous studies (Buxbaum et al., 2014).
For VLSM, we used the non-parametric statistics implemented in
MRIcron (Rorden et al., 2007). Specifically, we performed the
Brunner-Munzel test, a rank test for continuous behavioural variables
and binary images to identify lesioned voxels associated with deficits in
specific tests. The resulting maps display voxels with a significant difference in the distribution of the behavioural measure depending on
whether the voxel was lesioned. Only voxels affected in at least five
patients were included into the analysis. To avoid inflated z-scores in
voxels with 510 subjects in either the lesion or no-lesion groups, we
used a recent version of NPM (Non-Parametric Mapping, the statistical
package included with MRIcron; version 12/12/2012) that uses a permutation-derived correction (Medina et al., 2010).
Separate Brunner-Munzel analyses were performed for the overall
pantomime and imitation scores (PantoComplete and ImiComplete) as
well as for the respective subtests (ImiHand, ImiFinger, Content and
Movement scores). Different approaches were pursued to single out
areas specifically associated with different subtests. First, similar to
other studies (Kalénine et al., 2010; Kümmerer et al., 2013), separate
logistic regression analyses were computed for pairs of (sub)scores
using one score as predictor variable and the other score as covariate
and vice versa. This approach allows for the analysis of the variance in
one score while controlling for the variance in another score. Pairs
included ImiHand versus ImiFinger, Content versus Movement scores
and PantoComplete versus ImiComplete. Furthermore, to account for
the correlation of lesion volume with pantomime and imitation deficits
(see below), separate analyses were performed for each subscore with
lesion volume as covariate.
However, the regression analyses described above do not allow one
to test whether a lesion in a given voxel leads to significantly stronger
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| Brain 2014: 137; 2796–2810
impairments in one versus another task. Thus, to more directly explore
the areas of the brain where damage predicts a significant difference
between imitation and pantomime subscores (ImiHand versus
ImiFinger, Content versus Movement scores), separate BrunnerMunzel analyses were performed with the respective score differences
(ImiHand-ImiFinger and Content-Movement and vice versa, respectively). To single out regions significantly associated with differences
between overall imitation and pantomime scores (ImiComplete and
PantoComplete), scores were first converted to per cent correct
before calculating score differences to account for the different score
ranges (0–40 points for ImiComplete, 0–14 points for PantoComplete).
To exclude that using the differences of raw scores (as used for score
differences between Movement and Content subscores, as well as for
differences between ImiHand and ImiFinger), or per cent correct transformed scores (used for differences between ImiComplete and
PantoComplete) may have biased the results in terms of false negative
or false positive findings, additional control analyses concerned an alternative standardization approach by transforming the different scores
to z-scores. However, given that the results patterns using differences
from raw/per cent-correct transformed and z-transformed scores were
highly similar and thus independent of the applied standardization
approach, results for z-transformed scores are not shown.
Following the convention established by previous studies (Karnath
et al., 2011; Kümmerer et al., 2013), the statistical threshold for the
analyses with overall scores of pantomime and imitation as well as subscores and subscore differences for pantomime was set to P 5 0.01
[using a false discovery rate correction (FDR) for multiple comparisons].
As for ImiFinger, no voxels survived the FDR corrected P 5 0.01 threshold, results for the imitation subtests ImiHand and ImiFinger (but not the
results for the overall imitation scores, ImiComplete) are displayed at an
FDR corrected threshold of P 5 0.05 for comparability.
For each statistical results map calculated as outlined above, the
number of voxels within the 90 different areas of the Automated
Anatomical Labelling atlas (AAL-Atlas) (Tzourio-Mazoyer et al.,
2002) were calculated using SPM8 and expressed for each anatomical
region as percentage of the volume of the anatomical area, and as
percentage and of the total volume of the statistical map.
Results are displayed on an in-house average template of 50 nonlinearly normalized T1 scans from a sample of healthy subjects who
had participated in other studies in our lab (age, mean SD
47 20.75, range 22–84 years; 25 male).
Results
Demographic and behavioural results
Demographic and behavioural data of the included patients are
given in Table 1. Of the 102 patients, six scored below cut-off
in the object recognition test and, given that our pantomime test
required intact object recognition, were excluded from further
analysis. Only one patient showed symptoms of neglect at the
time of testing for apraxia; this patient scored above cut-off for
pantomime and imitation. Thirty-five patients were aphasic as
defined by the Token Test (Huber et al., 1984).
M. Hoeren et al.
Table 1 Demographic data and general clinical scores
Mean
Age (years)
Sex (female/male)
Infarct volume (ml)
NIHSS on admission
NIHSS on discharge
Right arm motor NIHSS on testing
mRS on discharge
Barthel index on discharge
Thrombolysis (none / iv /
bridging or mechanical)
Apraxia test scores
ImiComplete
ImiFinger
ImiHand
PantoComplete
Content score
Movement score
Other test scores
Corsi span forward
Corsi span backwards
BORB-11
Token Test percentile rank
Min
Max
63
15
40 / 56
22.3
35.9
6.6
5.4
2.4
2.5
0.0
0.0
1.8
1.1
86
27
54/34/8
SD
26
85
36.5
18.4
18.1
10.8
12.7
12.1
4.4
2.1
2.9
3.7
3.1
2.1
11
7
4
0
0
3
40
20
20
14
14
14
4.7
4.6
31.3
81.7
1.2
1.4
1.1
28.1
2
0
28
2
7
7
32
99
0.2
0
0
0
0
25
243.0
24
12
0
4
100
ImiComplete, overall score for imitation (maximum 40 points); ImiFinger and
ImiHand, subscores for imitation of finger and hand postures, respectively (maximum 20 points); PantoComplete, overall score for pantomime (maximum 14
points), Content and Movement scores, pantomime subscores for content and
movement errors (maximum 14 points).
BORB-11 = subtest 11 of the Birmingham Object Recognition Battery (maximum
32 points); NIHSS = National Institutes of Health Stroke Scale; mRS = modified
Rankin Scale.
imitation of finger postures (cut-off score for either subtest 18/20
points); for pantomime, 27 patients scored below cut-off (11/14
points). Eighteen patients showed an isolated imitation deficit
(three ImiHand deficit only; 11 ImiFinger deficit only; four combined ImiHand and ImiFinger deficit), 10 had an isolated pantomime deficit, and 16 patients had a combined imitation and
pantomime deficits (nine pantomime and imiHand deficit; two
pantomime and ImiFinger; five pantomime, ImiHand and
ImiFinger). For correlations between scores, see Table 2.
There were 67 patients with at least one movement error, and 27
patients with at least one content error. Of the patients with content errors, 25 patients displayed non-recognizable movements, 10
showed no-response-errors, and one patient showed a semantic
error. All 27 patients with content errors indicated their ability to
understand the test instructions by means of at least partial success
in other tests. Thus, all patients in this group had at least 28 points
in the Birmingham object matching test, and were able to correctly
imitate some hand and finger postures (minimum 4/20 points in
ImiHand, 7/20 in ImiFinger). Moreover, only three patients failed
the pantomime task completely (0 points), thus indicating by means
of at least one correctly or at least overall recognizably executed
item that test instructions were understood.
Imitation and pantomime
Forty-four patients scored below cut-off in at least one subtest of
imitation or pantomime. For imitation of meaningless gestures, 21
had a deficit in imitation of hand postures, 22 showed defective
Correlations with clinical and demographic data
Table 3 gives an overview over the rank correlations between test
performances and possible confounding factors. On the whole, there
Imitation and pantomime in acute stroke
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Table 2 Rank correlations between test scores (Kendall’s )
ImiComplete
ImiHand
ImiFinger
PantoComplete
Content score
Movement score
ImiComplete
ImiHand
ImiFinger
PantoComplete
Content score
Movement score
1
0.742**
0.755**
0.484**
0.458**
0.289*
0.742**
1
0.401**
0.474**
0.434**
0.257**
0.755**
0.401**
1
0.342**
0.333**
0.214**
0.484**
0.474**
0.342**
1
0.623**
0.730**
0.485**
0.434**
0.333**
0.623**
1
0.205*
0.289**
0.257**
0.214**
0.730**
0.205*
1
*P 5 0.05; **P 5 0.01.
Table 3 Rank correlations between test scores, and demographic and clinical data (Kendall’s )
ImiComplete
Infarct volume
Age
NIHSS on admission
NIHSS on discharge
mRS on discharge
Barthel score on discharge
Right arm motor NIHSS
Token-Test percentile rank
BORB-11
Corsi span forward
Corsi span backwards
0.260**
0.281**
0.230**
0.227**
0.257**
0.226**
0.061
0.289
0.285**
0.335**
0.381**
ImiHand
ImiFinger
0.308**
0.188*
0.265**
0.305**
0.346**
0.294**
0.133
0.303
0.222*
0.244**
0.224**
0.144
0.324**
0.154*
0.108
0.118
0.150
0.002
0.156
0.212*
0.279**
0.419**
PantoComplete
0.376**
0.118
0.265**
0.214**
0.226**
0.316**
0.125
0.401**
0.355**
0.240**
0.213**
Content score
0.375**
0.119
0.294**
0.352**
0.309**
0.334**
0.213
0.469**
0.365**
0.284**
0.204*
Movement score
0.203**
0.075
0.127
0.055
0.062
0.135
0.017
0.184
0.161
0.059
0.091
*P 5 0.05; **P 5 0.01.
BORB-11 = subtest 11 of the Birmingham Object Recognition Battery; NIHSS = National Institutes of Health Stroke Scale.
were weak to moderate correlations of imitation and pantomime
scores with infarct volume, degree of overall neurological impairment
as well as object-recognition and short-term memory scores. Sex
differences were observed neither for PantoComplete, or number
or type of errors (Mann-Whitney U-Tests, lowest P 4 0.677), nor
for ImiHand or ImiFinger (lowest P 4 0.507). Patients who used
the left hand for pantomime (n = 24) compared to patients who
used the right hand (n = 71) performed significantly worse on
PantoComplete (Mann-Whitney U test, P = 0.003; mean
scores SD, 8.7 4.5 versus 11.6 3.2); however, while the
number of content errors was also significantly greater in the left
hand group (3.0 4.4 versus 0.7 2.4, P = 0.001), the differences
in the number of movement errors did not reach significance
(P = 0.15). Moreover, patients who used the left hand also performed worse on ImiHand (17.1 3.7 versus 18.5 2.5,
P = 0.01), had more extensive lesions (infarct volume 44.0 57.3
versus 15.0 21.2 ml, P = 0.004), and, consecutively, were more
impaired with respect to right upper extremity motor function
(National Institutes of Health Stroke Scale value 1.4 1.3 versus
0.2 0.7, P 5 0.001), as well as overall (P 5 0.004 for National
Institutes of Health Stroke Scale on admission and discharge, and
modified Rankin Scale on discharge).
Lesion analysis
Lesion distribution
The overlap of the binary normalized lesion maps of the 96 patients with intact object recognition that were included in the main
analysis is displayed in Fig. 1. As in a previous study (Kümmerer
et al., 2013), maximum lesion overlap (24/96 patients) was found
in subcortical areas. The lesion density within inferior frontal gyrus
was similar to the IPL.
Imitation
Results are depicted in Figs 2 and 3 and listed in detail in
Supplementary Table 1. For ImiComplete, significant voxels were
mainly found within lateral occipito-temporal cortex (LOTC), superior parietal lobule (SPL), as well as around the posterior intraparietal sulcus (IPS). As no regions were significantly associated
with ImiFinger at a threshold of P 5 0.01 FDR corrected, both
ImiHand and ImiFinger are displayed at a lowered threshold of
P 5 0.05 FDR corrected to allow for a comparison of these two
imitation modalities. Both ImiHand and ImiFinger were associated
with a larger proportion of predominantly posterior IPL areas such
as angular gyrus. Compared with ImiFinger, ImiHand showed less
SPL involvement. The subscore difference ImiHand
ImiFinger
and the corresponding logistic regression analysis indicated an association of LOTC damage with the behavioural pattern of relatively greater impairments of ImiHand compared with ImiFinger;
no significant results were found for the reverse difference.
Specific regions for imitation of meaningless gestures were found
neither in the analyses with the score difference ImiComplete
PantoComplete, nor in the corresponding logistic regression analysis. However, the association of imitation with SPL and posterior
IPS seemed more pronounced compared to pantomime, as for
pantomime, an involvement of the SPL became apparent only
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M. Hoeren et al.
Figure 1 Overlap of the binarized lesions of the 96 patients included in the main analysis. The colour bar indicates the degree of overlap
of lesions, e.g. bright yellow values indicate that in 20 of 96 subjects, tissue was affected by stroke.
Figure 2 VLSM map for the combined score for imitation of hand and finger postures (ImiComplete). Colour bars indicate z-scores.
Reported results are thresholded at P 5 0.01, FDR corrected.
Figure 3 VLSM maps for subtest for the imitation of finger postures (ImiFinger, A), and hand postures (ImiHand, B). Colour bars indicate
z-scores. Note that these results, in contrast to the other analyses, are plotted at a lowered threshold of P 5 0.05, FDR corrected.
after lowering the statistical threshold to P 5 0.05 FDR corrected
(data not shown).
Pantomime
PantoComplete was mainly related to IPL, LOTC, as well as insula
and extreme capsule (Fig. 4 and Supplementary Table 2). The score
difference PantoComplete
ImiComplete and the logistic regression analysis for PantoComplete with ImiComplete as covariate
indicated a greater importance of LOTC areas slightly anterior to
the cluster found for ImiComplete, anterior IPL (mainly supramarginal gyrus), as well as insula and extreme capsule for pantomiming
relative to imitation (Fig. 4 and Supplementary Table 2).
Imitation and pantomime in acute stroke
Brain 2014: 137; 2796–2810
| 2803
Figure 4 Results for pantomime. VLSM maps are shown for overall pantomime scores (PantoComplete, A), and for areas specific for
pantomime in contrast to imitation, i.e. for the score difference PantoComplete ImiComplete after conversion to percent correct (B), as
well as the regression analysis of PantoComplete with ImiComplete as covariate (C). Colour bars indicate z-scores. Reported results are
thresholded at P 5 0.01, FDR corrected.
Specific regions for different error categories
The main finding of the analyses for the Content score with and
without Movement scores as covariate, as well as the score difference Content
Movement was a greater extent of significant
voxels within the temporal lobe compared to PantoComplete
(Fig. 5 and Supplementary Table 3 for details). Analyses for different subtypes of content errors yielded significant results for nonrecognizable movements and no-response errors; while associated
lesion locations were overall similar to the results for Content
scores, the extent of significant voxels in the inferior parietal
lobule was greater for non-recognizable movements whereas for
no-response errors, the association with temporal regions seemed
more pronounced (Supplementary Fig. 1). No significant results
were found in the analyses for Movement scores with and without
Content scores as covariate, or Movement
Content. Different
movement error subtypes (e.g. hand configuration errors) were not
consistently associated with a specific lesion location.
Other analyses
There were no significant voxels for the logistic regression analyses
for sub- and total pantomime and imitation scores when lesion
size was added as a covariate.
Region of interest analysis within the
frontal lobe
To further explore the lack of associations with frontal lesions,
VLSM analyses of total scores and subscores were repeated with
a mask combining the regions from the Automated Anatomical
Labelling atlas (AAL-Atlas) (Tzourio-Mazoyer et al., 2002) for
pars opercularis, triangularis and orbitalis of the inferior frontal
gyrus as well as middle frontal and precentral gyri. Thus, sensitivity
was increased by means of a less stringent false discovery rate
correction. Additionally lowering the statistical threshold to
P 5 0.05 FDR corrected, only few significant voxels emerged for
ImiHand and ImiComplete around the inferior frontal junction
zone, and, for pantomime, within the inferior frontal gyrus
(Supplementary Figs 2 and 3).
Discussion
Using VLSM, we investigated the hypothesis that imitation of
meaningless gestures depends mainly on the dorso-dorsal stream
while pantomime of tool use additionally involves ventro-dorsal
and ventral streams due to additional requirements on stored
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M. Hoeren et al.
Figure 5 Specific areas for content errors. VLSM maps for the analysis with Content scores alone (A), for the analysis with the subscoredifference Content
Movement (B), and the regression analysis for Content scores with Movement scores as covariate (C). Colour bars
indicate z-scores. Reported results are thresholded at P 5 0.01, FDR corrected.
action representations, and semantic knowledge of tool-action associations, respectively. By performing separate analyses for the
pantomime error categories Movement and Content, we strove
to further disentangle ventro-dorsal and ventral streams. To our
knowledge, our study features the largest cohort of stroke patients
prospectively investigated with reliably-scored pantomime and imitation tests (but see also Manuel et al., 2013; Buxbaum et al.,
2014 for other large samples), and it is the first to report VLSM
data from acute stroke patients.
In addition to LOTC, which likely provides visual input to several
streams (see below), the overall ability to imitate meaningless
hand and finger postures was mainly associated with regions
implicated in the dorso-dorsal stream (Buxbaum and Kalénine,
2010; Binkofski and Buxbaum, 2012), such as posterior IPS, and
SPL (Fig. 2 and Supplementary Table 1). Overall pantomime abilities also relied on areas within the dorso-dorsal stream, but were
additionally related to ventro-dorsal stream regions such as the
anterior IPL and posterior middle temporal gyrus (Daprati and
Sirigu, 2006; Binkofski and Buxbaum, 2012), as well as regions
previously assigned to a ventral processing stream, i.e. fibres traversing the extreme capsule (Weiller et al., 2011; Rijntjes et al.,
2012; Vry et al., 2012; Hoeren et al., 2013) (Fig. 4 and
Supplementary Table 2). The involvement of the ventral stream
in pantomime was highlighted further by the specific relation of
content errors with anterior temporal lobe damage (Fig. 5 and
Supplementary Table 3). However, no areas were significantly
associated with movement errors. To our knowledge, our study
is the first study to describe lesion locations significantly associated
with content errors during pantomime of tool use. Moreover,
while previously, damage to the dorso-dorsal stream was mainly
linked to the occurrence of optic ataxia (Daprati and Sirigu, 2006;
Kalénine et al., 2010; Binkofski and Buxbaum, 2012), our data
suggest that the concept of the dorso-dorsal stream should be
expanded to account for the association between imitation deficits
and damage to posterior IPS and SPL.
Imitation relies on the dorso-dorsal
stream
Imitation of meaningless gestures has been suggested to involve
several distinct processes, including the maintenance of the body
schema dynamically keeping track of the spatial relations between
different body parts (Heilman et al., 1986; Buxbaum et al., 2000;
Schwoebel and Coslett, 2005; de Vignemont, 2010), as well as the
construction of a higher-level representation of the perceived gesture (Goldenberg, 1995; Goldenberg and Hagmann, 1997) that
may be mapped onto the body schema (de Vignemont, 2010).
In addition to LOTC, which may rather constitute an area
Imitation and pantomime in acute stroke
providing higher order visual information to several streams, our
results highlight the specific importance of dorso-dorsal stream
areas, in particular posterior IPS and SPL for the processes involved
in imitation (Fig. 2 and Supplementary Table 1). These results are
consistent with a number of previous reports reports (e.g.
Buxbaum, 2001; Koski et al., 2003; Mühlau et al., 2005;
Rumiati et al., 2005; Menz et al., 2009; Vanbellingen et al.,
2014), but are partly at variance with a recent study on chronic
stroke patients that also reported an association between LOTC
damage and imitation deficits, but, however, may have lacked
sufficient lesion density to detect an association between gesture
production deficits and lesions within SPL and IPS (Buxbaum et al.,
2014).
Integrating on-line sensory information about the positions of
the different body parts with efference copies of motor actions,
the body schema generates sensorimotor representations of the
body for the guidance of actions (Wolpert et al., 1998;
Buxbaum, 2001; Schwoebel and Coslett, 2005; Pellijeff et al.,
2006; de Vignemont, 2010). Imitation of meaningless gestures
may be particularly vulnerable to a dysfunction of the body
schema as unlike pantomime, imitation may not be compensated
by stored action representations (Buxbaum et al., 2000).
Particularly, SPL may be essential for the maintaining the body
schema, as data from monkeys and humans have demonstrated
that SPL integrates visual and proprioceptive input about the position of body parts to maintain spatial limb representations
(Lacquaniti et al., 1995; Hagura et al., 2007; Seelke et al.,
2012). SPL and posterior IPS may also be crucial for the visuospatial transformations involved in mapping observed postures into
‘somatesthetic spatial code’, i.e. the coordinates of the body
schema (Heilman et al., 1986; Buxbaum, 2001; Creem-Regehr
et al., 2007).
Areas within LOTC likely mediate in the decoding of observed
gestures, extracting features like identity or spatial relationships of
the body parts involved (Goldenberg, 1995, 2009; Goldenberg
and Hagmann, 1997). Thus, extrastriate body area, MT/V5 +
and the posterior STS have been associated with the perception
of body parts and biological motion, respectively (Downing et al.,
2001; Grossman and Blake, 2002; Grill-Spector and Malach, 2004;
Iacoboni, 2005; Peelen and Downing, 2007). Together, LOTC
areas likely provide input not only to the dorso-dorsal stream,
but also to ventro-dorsal and ventral pathways (Gallese, 2007).
This view is consistent with the proposal that both dorsal and
ventral streams process the same set of visual input for different
behavioural goals (Binkofski and Buxbaum, 2012).
In line with previous studies (Hermsdörfer et al., 2001; Mühlau
et al., 2005), both ImiHand and ImiFinger were also associated
with posterior IPL, albeit at a lower statistical threshold (Fig. 2 and
Supplementary Table 1). IPL has been suggested to facilitate imitation by generating more abstract gesture representations defining observed postures as sets of categorical spatial relationships
between a limited number of body parts (Goldenberg, 1995,
1999). This ‘body part coding’ (Goldenberg, 2009) is thought to
reduce working memory demands and likely requires the integration of higher-order visual information with stored conceptual
knowledge about body parts. Consequently, rather than an exclusive dorso-dorsal region, posterior IPL may function as a hub
Brain 2014: 137; 2796–2810
| 2805
connecting dorsal and ventral streams (see below). The comparatively weak association between imitation deficits and IPL lesions
in our study may have resulted from a reduced working memory
load as, in contrast to past studies (e.g. Goldenberg and Karnath,
2006) the examiner maintained the target posture until the patient
had completed the imitation. Possibly, this modification to the test
may also explain the distinctly higher scores (18/20 for ImiHand
and ImiFinger compared with 15/20 in previous studies, e.g.
Goldenberg and Karnath, 2006).
Differences between imitation of hand and finger
postures
As no significant voxels were found for ImiFinger at the FDR corrected threshold of P 5 0.01 used for all other analyses, both
ImiFinger and ImiHand are displayed at P 5 0.05 FDR corrected
to enable a comparison of the overall pattern of lesion locations
associated with deficits in either imitation subtest (Fig. 3).
Although a previous study based on lesion overlaps of chronic
stroke patients reported a fronto-parietal dissociation between imitation of meaningless hand and finger postures (Goldenberg and
Karnath, 2006), our VLSM data along the significant behavioural
correlation indicate the importance of the dorso-dorsal stream for
both imitation modalities. However, the overall statistically weaker
association of ImiFinger with occipito-parietal lesions may be consistent with the proposed additional involvement of other left and
right hemisphere regions in ImiFinger (Goldenberg, 1999;
Goldenberg and Karnath, 2006). The relatively more pronounced
associations of ImiFinger and ImiHand with SPL and IPL, respectively, are in line with a PET study (Hermsdörfer et al., 2001). The
significant voxels within LOTC found for the analysis with the
difference ImiHand
ImiFinger may have reflected simply the
greater overall association of ImiHand with the dorso-dorsal
stream areas, or, alternatively, higher demands on visual decoding,
e.g. due to the higher number of body parts involved.
Pantomime of tool use involves both
dorsal and ventral streams
Several regions associated with pantomime deficits overlapped
with those found for imitation (Figs 2, 4 and Supplementary
Tables 1 and 2). Along with the behavioural correlation, this overlap indicates that that mechanisms mainly related to the dorsodorsal stream are involved in either task. However, the association
of pantomime with specific dorso-dorsal stream areas, i.e. posterior IPS and SPL, was evident only from the VLSM analysis with
PantoComplete at a lower statistical threshold, as well as from the
absence of imitation-specific areas in the analysis with
ImiComplete
PantoComplete and the corresponding regression
analysis (see ‘Results’ section). This weaker association is in line
with lower demands on the body schema and mechanisms for
visuo-motor conversion (Buxbaum et al., 2000; Buxbaum, 2001;
de Vignemont, 2010).
With respect to areas involved in several streams, for pantomime, areas within LOTC likely decode the visual features of
the tool images (Grill-Spector and Malach, 2004; Taylor and
Downing, 2011). Although impossible to discern with VLSM
data, the LOTC regions involved likely differ at least partly from
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| Brain 2014: 137; 2796–2810
those necessary for the perception of hand and finger postures
(Rizzolatti and Matelli, 2003; for review see Grill-Spector and
Malach, 2004; Taylor and Downing, 2011). Posterior IPL, by contrast, may integrate perceived object features with motor engrams
stored within anterior IPL (Buxbaum et al., 2005), and possibly,
semantic knowledge about tools and objects (Binder et al., 2009;
Hoeren et al., 2013; Seghier, 2013). Thus, posterior IPL may contribute to the selection of the action appropriate for the currently
presented tool.
Compared to imitation, pantomime selectively depended on
posterior middle temporal gyrus and anterior IPL, as well as
insula and extreme capsule (Fig. 4B and C, Supplementary Table
2). Anterior IPL and posterior middle temporal gyrus have been
assigned to the ventro-dorsal stream involved in storing motor
engrams and knowledge about the manipulation of tools and objects (Kalénine et al., 2010; Binkofski and Buxbaum, 2012).
Particularly anterior IPL has been linked to the maintenance of
canonical action engrams (Heilman and Rothi, 2003; Buxbaum
et al., 2005, 2007; Peeters et al., 2009), also called ‘visuokinaesthetic engrams’ (Heilman et al., 1982), ‘action prototypes’
(Hermsdörfer et al., 2013), or ‘blueprints for movement’ (Rijntjes
et al., 1999). Shaped during motor learning (Weisberg et al.,
2007), these engrams are thought to specify invariant spatiotemporal features of skilled movements. Upon movement execution,
the engrams may be flexibly adapted according to current physical
constraints like the shape or size of a tool, or the effector used
(Rijntjes et al., 1999; Haaland et al., 2000; Binkofski and
Buxbaum, 2012; Hermsdörfer et al., 2012). Although the importance of the IPL for representational action aspects has recently
been challenged (Buxbaum et al., 2014), our results corroborate
the importance of the IPL for action engrams. Possibly, as
Buxbaum et al. (2014) studied chronic patients, the IPL functions
relevant to pantomime of tool use had shifted to other areas due
to brain reorganization.
Although posterior middle temporal gyrus is also involved in the
processing of manipulation knowledge (Kellenbach et al., 2003;
Tranel et al., 2003; Boronat et al., 2005; Valyear and Culham,
2010), it may also contribute to the integration of semantic knowledge about tools and objects with movement representations in
dorsal areas (Willems et al., 2009; Kalénine et al., 2010).
Moreover, the importance of posterior middle temporal gyrus for
action representations was recently highlighted by a large lesion
study on chronic stroke patients (Buxbaum et al., 2014).
The voxels found within insula and subinsular white matter
likely reflected damage to a ventral fibre tract traversing the extreme capsule. This tract has been shown to connect areas of the
posterior parietal lobe with the anterior inferior frontal gyrus (Vry
et al., 2012; Hoeren et al., 2013), and is considered a central
component of a domain-independent ventral stream also involved
in language (Weiller et al., 2011; Rijntjes et al., 2012). For pantomime, this ventral pathway may facilitate the top–down activation
of movement engrams, the selection of distinctive and relevant
movement features that ensure a high recognizability of the
pantomime, as well as the integration of motor programs with
semantic knowledge about the function of tools and objects
(Goldenberg et al., 2007; Vry et al., 2012). Similar lesion locations
M. Hoeren et al.
associated with pantomime deficits have been described previously
(Goldenberg et al., 2007; Manuel et al., 2013).
Correlates of different pantomime error types: selective
importance of the temporal lobe for content errors
Content errors, indicating an inability to correctly associate tools
with actions, are thought to result from disturbances within a
separate semantic system for action (Rothi et al., 1991; Heilman
et al., 1997; Cubelli et al., 2000). When asked to pantomime the
use of tools, patients may, thus, display unrecognizable movements, remain in a state of helpless perplexity, or perform actions
not usually associated with the tool (e.g. cutting with a spoon) (De
Renzi and Lucchelli, 1988; Ochipa et al., 1989, 1992; Heilman
et al., 1997).
The association of IPL lesions with content errors is consistent
with the view that a complete inability to pantomime the use of a
tool may result from a severe disruption of the action engram (De
Renzi and Lucchelli, 1988; Heilman et al., 1997). The greater parietal involvement compared to no-response errors indicates that
this may in particular apply to non-recognizable movements,
which could result from severe spatiotemporal errors rather than
from erroneous ‘content’ per se (Supplementary Fig. 1). However,
the additional involvement of the anterior temporal lobe, which
became particularly apparent when controlling for the number of
movement errors as a measure of ventro-dorsal stream dysfunction (Fig. 5B and C), highlights the importance of this region for
the action semantic system (Fig. 5 and Supplementary Table 3).
Alternatively, content errors may have resulted from more general
semantic impairments following lesions in the anterior temporal
lobe region (Patterson et al., 2007; Guo et al., 2013). In line
with this view, patients with semantic dementia and temporal
lobe atrophy have been documented to be unable to demonstrate
the prototypical use of tools despite preserved mechanical problem
solving abilities (Hodges et al., 1999). However, while in general,
severe amodal semantic following stroke seem to be rare (Hillis
et al., 1990), no detailed assessment was carried out for the present sample of patients to evaluate the integrity of other aspects
of semantic knowledge. In sum, the data confirm the importance
of the ventral stream for the selection of appropriate actions
(Goodale and Milner, 1992; Milner and Goodale, 2008).
Although in line with our hypothesis, the only weak correlation
between content and movement scores (Table 2) points to different underlying mechanisms, no significant result were found in the
VLSM-analysis for movement errors. Several reasons may have
contributed to this negative finding. First, compared with content
errors, the reliable identification of pathological movement features may be more difficult as up to three movement errors
could be observed even in healthy control subjects. Secondly,
lesion locations associated with movement errors may be more
variable compared to content errors, as not only defective movement engrams ensuing damage to the ventro-dorsal stream (Rothi
et al., 1991; Cubelli et al., 2000), but also disturbances of dorsodorsal stream functions like the body schema may lead to movement errors (Buxbaum et al., 2000; Buxbaum, 2001). Consistent
with this view, a recent report indicated that errors of the hand or
arm posture may predominantly arise from damage to the representational component of the action while errors of amplitude or
Imitation and pantomime in acute stroke
timing result from disturbances within regions for online movement control (Buxbaum et al., 2014). This dissociation could not
be reproduced in the present study as separate analyses for different error types, e.g. hand configuration errors or amplitude/
timing errors did not yield significant results. This difference may
have resulted from distinct scoring systems or differences in the
study populations.
Minor contribution of frontal lobe
lesions to pantomime and imitation
deficits
A rapid compensation by the contralateral hemisphere may account for the weak association between frontal lesions and
praxis deficits (Supplementary Figs 2 and 3) that stands in contrast with the findings of several past studies using functional
imaging and lesion overlaps (Leiguarda and Marsden, 2000;
Goldenberg and Karnath, 2006; Goldenberg et al., 2007).
Accordingly, a functional MRI study with aphasic patients with
left hemisphere strokes showed a rapid increase in activity
mainly in right frontal areas within the first 12.1 days poststroke (Saur et al., 2006). As we examined the study participants
after a mean of 5.3 days, we cannot exclude that some degree of
reorganization within the frontal lobes had already taken place at
the time of testing.
Limitations
The correlations between test scores and lesion size as well as
overall impairment likely resulted from the inclusion of consecutive
patients with a large range of lesion sizes, and, consecutively, of
overall impairment (Table 3). However, the clear differences between the VLSM results for pantomime and imitation are unlikely
to be attributable to these factors, given that confounds more
directly related to the tests, such as object recognition were meticulously assessed in each patient.
Our data suggest that rather than being a causative factor for
lower pantomime scores, left hand use seemed to be an indicator
for greater overall disability and larger lesions, which in turn were
more likely to lead to pantomime deficits. Thus, patients who were
prompted to use their left hand for pantomime due to right upper
extremity paresis displayed a significantly higher number of content errors, but not movement errors. The reverse pattern would
be expected if clumsiness due to left hand use had affected the
scores. This view is further supported by the lack of score differences of healthy controls using either the right or left hand for
pantomime. Moreover, imitation of meaningless hand postures
was also significantly more impaired in patients who used their
left hand for pantomime, although all patients used their left
hand for imitation.
Similarly, as the instructions of all tests could easily be understood non-verbally, the correlation of imitation and pantomime
scores with the Token Test rather reflects the joint involvement
of brain regions in language and praxis rather than a causal
relationship.
Brain 2014: 137; 2796–2810
| 2807
Lastly, although studies with acute compared to chronic stroke
patients allow for a more accurate lesion delineation, and, moreover, permit avoiding the effects of brain reorganization (Saur
et al., 2006), studies with acute patients may also suffer from
disadvantages. First, diaschisis, the dysfunction of one or more
functionally dependent cortical areas caused by a remote lesion,
may affect patients in the acute phase (von Monakow, 1985; Saur
et al., 2006; Jarso et al., 2013; Kümmerer et al., 2013). The effects of diaschisis are difficult to assess, yet as these changes are
thought to occur within a network of functionally related areas
(Price et al., 2001) false positive results, i.e. the detection of areas
unrelated to the task, are unlikely. Secondly, acute patients may
suffer more intensely from non-specific symptoms such as fatigability or reduced concentration. However, in our study, all patients indicated overall testability by at least partly complete tests
for working memory, object recognition and imitation.
Conclusion
In summary, our results indicate that the ability to imitate meaningless gestures largely relies on the dorso-dorsal stream. Thus, our
data suggest that damage to the dorso-dorsal stream may not
only result in optic ataxia (Daprati and Sirigu, 2006; Binkofski
and Buxbaum, 2012), but also imitation deficits. Pantomime of
tool use, conversely, requires the interplay of dorso-dorsal,
ventro-dorsal and ventral streams to enable the integration of
movement engrams with semantic knowledge as well as with
mechanisms for on-line control of actions. Our study particularly
highlights the significance of the ventral stream for conceptual
aspects of pantomime.
Acknowledgements
We thank Hansjörg Mast for assistance in data acquisition. We
thank Gabriele Lind, Sarah Höfer and Cornelia Pietschmann for
conducting the neuropsychological testing; without their careful
and patient examinations, this study would not have been possible. We thank two anonymous reviewers for their suggestions.
Funding
This work was supported by the BrainLinks-BrainTools Cluster of
Excellence funded by the German Research Foundation (DFG,
grant #EXC1086).
Supplementary material
Supplementary material is available at Brain online.
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