doi:10.1093/brain/awu111
Brain 2014: 137; 1971–1985
| 1971
BRAIN
A JOURNAL OF NEUROLOGY
Critical brain regions for tool-related and imitative
actions: a componential analysis
Laurel J. Buxbaum,1 Allison D. Shapiro1 and H. Branch Coslett2
1 Moss Rehabilitation Research Institute, 50 Township Line Rd, Elkins Park, PA, 19027, USA
2 Department of Neurology, University of Pennsylvania School of Medicine, 3400 Spruce Street, Philadelphia, PA, USA
Correspondence to: Laurel J. Buxbaum,
Moss Rehabilitation Research Institute,
50 Township Line Rd.,
Elkins Park,
PA 19027 USA,
E-mail: [email protected]
See doi:10.1093/brain/awu122 for the scientific commentary on this article.
Numerous functional neuroimaging studies suggest that widespread bilateral parietal, temporal, and frontal regions are involved in
tool-related and pantomimed gesture performance, but the role of these regions in specific aspects of gestural tasks remains unclear.
In the largest prospective study of apraxia-related lesions to date, we performed voxel-based lesion–symptom mapping with data
from 71 left hemisphere stroke participants to assess the critical neural substrates of three types of actions: gestures produced in
response to viewed tools, imitation of tool-specific gestures demonstrated by the examiner, and imitation of meaningless gestures.
Thus, two of the three gesture types were tool-related, and two of the three were imitative, enabling pairwise comparisons designed
to highlight commonalities and differences. Gestures were scored separately for postural (hand/arm positioning) and kinematic
(amplitude/timing) accuracy. Lesioned voxels in the left posterior temporal gyrus were significantly associated with lower scores on
the posture component for both of the tool-related gesture tasks. Poor performance on the kinematic component of all three gesture
tasks was significantly associated with lesions in left inferior parietal and frontal regions. These data enable us to propose a
componential neuroanatomic model of action that delineates the specific components required for different gestural action tasks.
Thus, visual posture information and kinematic capacities are differentially critical to the three types of actions studied here: the
kinematic aspect is particularly critical for imitation of meaningless movement, capacity for tool-action posture representations are
particularly necessary for pantomimed gestures to the sight of tools, and both capacities inform imitation of tool-related movements.
These distinctions enable us to advance traditional accounts of apraxia.
Keywords: action; tools; apraxia; imitation; gesture
Abbreviations: AAL = Automatic Anatomic Labelling; GestTool = gesture to the sight of tool; ImNov = imitation of novel gestures;
ImTool = imitation of tool-related gestures; VLSM = voxel-based lesion–symptom mapping
Introduction
The ability to perform complex tool-related actions and to imitate
the actions of others is a hallmark of human motor performance.
Deficits in both of these skills are central to the syndrome of limb
apraxia, a heterogeneous and complex disorder of action planning
and execution that cannot be attributed to weakness or sensory
loss. Patients with apraxia perform gestural movements with errors
in timing, sequencing, spatial organization, and less commonly,
content. Despite over 140 years of investigation (Steinthal,
Received December 30, 2013. Revised March 18, 2014. Accepted March 19, 2014. Advance Access publication April 27, 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]
1972
| Brain 2014: 137; 1971–1985
1871; Liepmann, 1900) and its frequent presence in left hemisphere stroke, Alzheimer’s disease, and corticobasal syndrome,
limb apraxia remains relatively poorly understood. Nevertheless,
recent research has demonstrated that apraxia has important implications for understanding the organization of object and action
knowledge, motor simulation and planning, and the neuroanatomic substrates of these functions (Buxbaum and Kalenine,
2010; Binkofski and Buxbaum, 2013).
Although theoretical models of the praxis system differ in their
details, many include both representational and production-related
or kinematic action components (Roy and Square, 1985; Rothi
et al., 1991; Heilman and Gonzalez Rothi, 1993; Cubelli et al.,
2000; Buxbaum, 2001; and see Petreska et al., 2007 for a review).
The representational component provides a processing advantage
to the performance of familiar as compared to novel object-related
actions (Buxbaum et al., 2005a), and has been aligned with conceptual action knowledge, also termed action semantics (Roy and
Square, 1985). We have previously suggested that these action
representations are likely to be patterns of co-occurrence of posture and movement features abstracted across multiple instances
of spatiomotor and visual experience with a given class of similar
actions (e.g. the arm and hand postures associated with using all
hammers, regardless of their size and weight or the characteristics
of the surface being hammered) (Buxbaum, 2001). In terms of the
tests of gesture production historically associated with praxis testing, a strong measure of the representational component of praxis
is ‘pantomimed gesture production in response to viewed tools’.
Pantomime is generally held to be more sensitive than actual tool
use because the shape and weight of tools in the hand is likely to
provide feedback that alters the kinematics of movement, which in
turn may augment deficient gesture representations (Goldenberg
et al., 2004).
The kinematic component of praxis may be conceptualized as
the basis for the planning of movement trajectories in terms of
extent, direction and timing. Gesture kinematics may be particularly sensitive to current task constraints (e.g. the precise size and
orientation of the hand and arm movements required to use a
particularly-sized hammer on a surface of particular orientation
to drive a particular type of nail). With reference to traditional
praxis assessment, the kinematic component is perhaps most sensitively assessed with imitation of novel, meaningless gestures.
Imitation of meaningless gestures (unlike imitation of known gestures) is thought to depend entirely on a so-called ‘direct’ route to
action in which visual input must be transcoded into parameters
for movement of the actor’s body, without the benefit of input
from learned gesture representations (Rothi et al., 1992).
To this point, however, the neuroanatomic loci of these components of the praxis system are poorly understood. Apraxic production deficits in left hemisphere stroke have been observed after
inferior parietal lobe and prefrontal lesions (Buxbaum et al., 2007;
Goldenberg et al., 2007b), but also in patients with temporal and
subcortical damage (Goldenberg, 1995; Tessari et al., 2007).
Possible differences in patterns of performance attributable to lesions in these different loci have not been systematically explored.
In this context, numerous recent functional neuroimaging studies
have assessed the production of gestures using imitation, and to a
lesser degree, pantomime tasks in neurologically-intact
L. J. Buxbaum et al.
participants. A recent meta-analysis of gesture imitation (Caspers
et al., 2010) revealed a large bilateral network of brain regions
including inferior parietal lobe, temporo-occipital, premotor, primary somatosensory, and intraparietal areas that was activated
irrespective of the hand used. Similarly, gesture pantomime has
been associated with activation in numerous bilateral areas, including motor, premotor, inferior and superior parietal, and temporal
regions (Hermsdoerfer et al., 2007).
In contrast, apraxia in stroke populations is also almost invariably a left hemisphere syndrome in right-handed and some lefthanded individuals (Goldenberg, 2013). This pattern suggests that
the right hemisphere activations associated with praxis in many
neuroimaging studies may be epiphenomenal. Alternatively, it is
possible that right hemisphere regions play a supporting, perhaps
synergistic role in the facilitation of spatiomotor processing.
Similarly, it is unclear which of the observed left hemisphere activations may be epiphenomenal or supportive rather than critical.
Thus, lesion studies play an important role in our understanding of
the importance and relative roles of differing brain regions in the
components of praxis.
Previous literature helps in the identification of several candidate
left hemisphere regions. Recent evidence suggests that the left
posterior middle temporal gyrus is critical for representing semantic action knowledge. Lesions to this region impair recognition of
tool use actions (Kalenine et al., 2010) and the ability to evaluate
pictured actions (Tranel et al., 2003). Consistent with these data,
left posterior middle temporal gyrus is consistently activated in
action knowledge tasks with healthy subjects (Watson et al.,
2013) with both picture and word stimuli (Kable et al., 2002,
2005; Assmus et al., 2007; Vingerhoets et al., 2009; Wallentin
et al., 2011).
A second left hemisphere region of probable importance is the
left inferior parietal lobe, long recognized as a substrate for skilled
gesture production (Heilman et al., 1983; Heilman and Gonzalez
Rothi, 1993). Patients with left inferior parietal lobe lesions produce spatial and temporal errors during imitation of tool use
pantomimes (Halsband et al., 2001). Moreover, inferior parietal
lobe-lesioned patients tend to be more impaired in imitating
meaningless as compared to meaningful gestures (Kolb and
Milner, 1981; Goldenberg and Hagmann, 1997; Haaland et al.,
2000; Weiss et al., 2001; Tessari et al., 2007). As noted, the
former may be disproportionately reliant on kinematic processing.
Consistent with this reasoning, we demonstrated in a previous
study using voxel-based lesion–symptom mapping (VLSM) that
parietal lesions disrupt detection of errors in spatiotemporal (kinematic) gestural information (Kalenine et al., 2010; but see
Goldenberg, 2009 for an alternative account focused on apprehension of categorical spatial relationships).
Additional regions of probable importance in praxis production
are left motor, premotor, and prefrontal cortices, particularly the
middle and inferior frontal gyri. Theta burst stimulation of the left
inferior frontal gyrus interferes with gesture production (Bohlhalter
et al., 2011). In patients with corticobasal syndrome, gesture production deficits are associated with left frontal cortical and subcortical volume loss (Borroni et al., 2008; Huey et al., 2009).
Moreover, left inferior frontal gyrus and sensorimotor cortex are
activated in functional neuroimaging studies of gesture imitation
Tool-related and imitative actions
and production (Muhlau et al., 2005; Hamilton and Grafton,
2009), and left middle frontal or inferior frontal gyrus stroke
may result in deficits in gesture imitation (Haaland et al., 2000;
Goldenberg et al., 2007a).
Based on these data, we hypothesize that the representational
component of praxis (which we and others align with semantic
action knowledge) (Kalenine et al., 2010) is largely subserved by
the left posterior middle temporal gyrus, and the kinematic component primarily by the left inferior parietal lobe. To assess these
hypotheses, we used VLSM to assess the cortical brain regions
associated with impairments in three types of gestures performed
with the ipsilesional (left) hand of left hemisphere stroke patients:
gestures produced in response to viewed tools (GestTool), imitation of tool-specific gestures demonstrated by the examiner
(ImTool), and imitation of novel, meaningless gestures (ImNov).
Thus, two of the three gesture types were tool-related, and two of
the three were imitative, enabling pairwise comparisons designed
to highlight conjunctions and disparities between tasks.
Additionally, gestures were scored separately for postural (hand/
arm positioning) and kinematic (amplitude/timing) accuracy to
assess the hypothesis that representational and kinematic capacities would be differentially critical to the three types of actions.
Specifically, we hypothesized that the kinematic aspect should be
particularly critical for imitation of meaningless movement, capacity for tool-action representation should be necessary for pantomimed gestures to the sight of tools, and both capacities should
inform imitation of tool-related movements.
Materials and methods
Participants
Seventy-three individuals who suffered a left-hemisphere stroke
including the cortex were recruited for the study. Sixty-four of the
strokes were ischaemic and nine were haemorrhagic. Participants
were recruited from a large registry at the Moss Rehabilitation
Research Institute. Patients over the age of 80 years or with histories
of comorbid neurological disorders, alcohol or drug abuse, psychosis,
or severe language comprehension deficits were excluded. All patients
gave informed consent to participate in the behavioural testing in accordance with the guidelines of the Institutional Review Board of
Einstein Healthcare Network and the Declaration of Helsinki and
were paid for their participation. Fifty-three patients also provided informed consent to participate in an MRI or CT imaging protocol at the
University of Pennsylvania School of Medicine. All participants were
paid for their participation and reimbursed for travel expenses. Two
participants were excluded after brain imaging revealed bilateral ischaemic infarction.
Demographic and experimental behavioural data for the remaining
71 participants (33 females; mean age 58 years, age range 35–80) are
reported in Table 1.
Behavioural tasks
Gesture to tool
Subjects were presented serially with 10 household tools (e.g. scissors,
fork, comb) and asked to demonstrate precisely without touching the
Brain 2014: 137; 1971–1985
| 1973
tool how they would if they were holding it with the (less impaired)
left hand. Gestures were videotaped and later coded as correct or
incorrect on each of five dimensions: content, hand posture, arm posture, amplitude, and timing. Scoring was performed according to a
detailed error taxonomy by trained coders who demonstrated reliability
with previous coders in our laboratory (Buxbaum et al., 2005a) as
defined by Cohen’s Kappa 4 0.85 (‘very good’ agreement, Altman,
1991). The Supplementary material provides details of the scoring
criteria.
Postural scores were calculated by averaging the hand and arm
posture component scores, which were moderately strongly correlated
(P 5 0.001) for each gesture type [GestTool: r(69) = 0.46, ImTool:
r(69) = 0.75, ImNov: r(69) = 0.79]. Kinematic scores were calculated
by averaging the amplitude and timing component scores, also moderately strongly correlated (P 5 0.001) [GestTool: r(69) = 0.64, ImTool:
r(69) = 0.70, ImNov: r(69) = 0.54]. Total gesture scores for each item
were calculated by averaging all four component scores.
Imitation of tool-related gesture
Participants were shown videoclips of an experimenter performing 10
transitive pantomimes associated with household tools (e.g. scissors,
screwdriver, toothbrush). Participants were asked to imitate the experimenter’s pantomime as precisely as possible. In this task, as well as in
the novel imitation task described below, the experimenter used the
right hand and faced the camera in second person perspective.
Participants mirrored the gestures with the left hand. Each gesture
was shown twice in succession, and the subject was permitted to
begin while observing the target gesture. Gestures were videotaped
and later coded by the same coders using the same scoring criteria
applied to GestTool performance.
Imitation of novel gesture
Participants were shown videos of an experimenter performing 10
novel gestures with the left hand. The novel gesture task was developed with reference to the gestures assessed in the ImTool condition. Specifically, for each tool-related gesture from the ImTool task,
the plane of movement (vertical/horizontal), joints moved (shoulder/
elbow/wrist/fingers), grip type (hand open/clenched/partially open),
and oscillations (present/absent) were tabulated. The items of the
ImNov task preserved the characteristics of the meaningful gestures
with respect to these attributes (see Buxbaum, 2001 for details of
stimulus development). Each gesture was shown twice in succession,
and subjects were permitted to begin imitating while observing.
Participants’ gestures were videotaped and scored as described above.
Imaging, lesion segmentation and
warping to template
Details of imaging, segmentation, and warping methods are provided
in the Supplementary material. High-resolution structural brain images
were collected from 53 participants. For 18 participants for whom MRI
or CT research scans could not be obtained, a recent clinical CT or
MRI was judged by the project neurologist (H.B.C.) to be of sufficient
quality and resolution for lesion segmentation.
A research team member manually segmented the brain lesions of
19 of the participants who underwent research MRI scans. The patient
structural scans and lesion masks were then warped to a common
1 1 1 mm template [Montreal Neurological Institute (MNI) space
‘Colin27’]; (Holmes et al., 1998). For the rest of the participants who
received research scans (n = 34; CT = 21, MRI = 13) and those who
had clinical scans (n = 18), H.B.C. drew a lesion mask directly onto the
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| Brain 2014: 137; 1971–1985
L. J. Buxbaum et al.
Table 1 Demographics and characteristics of the 71 patients participating in the study
Subject
GestTool
(%)
ImTool
(%)
ImNov
(%)
Lesion Volume
(voxels)
Gender
Hand
Education (y)
Age
Months
post
01
02
03
04
05
06
07
08
09
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
45.0
82.5
87.5
63.9
90.0
50.0
85.0
80.0
63.9
97.5
75.0
87.5
85.0
97.5
75.0
85.0
62.5
87.5
65.0
95.0
57.5
55.0
92.5
82.5
87.5
50.0
92.5
92.5
92.5
90.0
90.0
60.0
37.5
90.0
62.5
67.5
87.5
60.0
87.5
65.0
77.5
75.0
97.5
100.0
92.5
80.0
97.5
50.0
85.0
97.2
75.0
70.0
85.0
55.0
87.5
90.0
85.0
75.0
75.0
100.0
57.5
100.0
55.0
100.0
82.5
53.3
88.3
75.8
74.1
75.9
92.5
55.0
100.0
70.0
86.7
55.0
100.0
75.0
50.0
64.2
100.0
95.0
77.6
100.0
100.0
100.0
100.0
100.0
37.5
47.5
100.0
47.5
70.0
100.0
70.0
100.0
80.0
100.0
85.0
90.0
90.0
82.5
77.5
77.5
72.5
76.7
100.0
60.0
67.5
100.0
85.0
100.0
100.0
75.0
72.5
72.5
100.0
60.0
92.5
77.5
85.0
65.0
55.0
72.5
72.5
75.0
77.5
95.0
57.5
90.0
62.5
82.5
57.5
95.0
65.0
25.0
72.5
90.0
92.5
72.5
92.5
87.5
92.5
92.5
92.5
40.0
50.0
95.0
57.5
62.5
95.0
50.0
92.5
50.0
95.0
75.0
90.0
90.0
82.5
77.5
77.5
52.5
70.0
85.0
57.5
67.5
92.5
90.0
90.0
90.0
70.0
6572
12252
60218
196024
50218
27095
118909
204861
16670
40102
6342
20369
34186
109589
181834
60271
155492
1913
135867
7507
83076
138731
44506
189818
88958
54830
90534
40759
41049
14749
48288
56061
188649
10583
41363
27223
33904
31436
13995
36717
72680
49432
7916
94098
3913
23437
114398
202634
8557
165844
185280
68474
105131
124897
15956
46576
70434
F
M
F
F
M
F
F
M
M
M
F
M
M
F
F
F
M
F
M
M
M
M
M
F
M
F
M
M
F
F
M
F
F
F
M
F
F
M
F
F
M
M
M
M
F
F
M
F
M
M
M
M
M
F
F
F
M
R
R
R
R
R
R
R
L
R
R
R
R
R
R
R
R
R
L
R
L
R
R
R
R
R
L
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
12
16
18
18
14
12
14
8
8
11
16
11
8
13
17
12
12
12
13
10
12
16
11
16
12
12
12
11
14
15
19
16
12
13
16
12
11
11
16
12
20
12
13
14
12
12
16
10
16
16
13
16
21
16
12
12
12
79
63
50
54
68
41
39
71
74
62
56
57
78
47
48
51
64
52
60
51
40
58
51
72
68
49
54
42
54
44
64
80
63
77
56
67
66
79
55
58
55
50
61
69
66
50
66
41
59
55
64
49
57
40
44
35
78
69
7
5
165
9
12
50
152
20
45
59
62
39
82
23
16
82
9
142
13
26
135
82
170
319
14
89
22
8
9
65
10
143
8
9
91
61
27
79
6
74
17
17
20
77
145
14
127
29
22
42
35
114
2
10
7
41
(continued)
Tool-related and imitative actions
Brain 2014: 137; 1971–1985
| 1975
Table 1 Continued
Subject
GestTool
(%)
ImTool
(%)
ImNov
(%)
58
59
60
61
62
63
64
65
66
67
68
69
70
71
87.5
77.5
87.5
85.0
80.6
82.5
56.3
97.5
97.2
97.5
80.6
90.0
100.0
87.5
64.2
71.7
66.1
84.2
65.8
80.0
52.7
94.2
87.5
86.7
61.7
81.7
67.5
100.0
65.0
75.0
67.5
87.5
67.5
67.5
60.0
95.0
82.5
77.5
50.0
75.0
67.5
95.0
Lesion Volume
(voxels)
Gender
Hand
Education (y)
Age
75994
264697
114029
43844
57332
19811
266719
45215
68902
10133
41726
27377
71050
20132
M
M
F
M
F
F
F
M
M
M
F
F
M
M
R
R
R
R
R
R
R
R
R
R
R
R
R
R
11
19
17
16
14
12
16
18
14
12
12
12
12
12
61
59
50
64
74
60
55
55
42
60
56
54
71
64
Colin27 volume. The Colin27 template was rotated to match the pitch
of the imaged patient brain. All lesion masks were thresholded and
quantized to produce a 0/1 map: voxels containing a mask value
40.5 were assigned a value of 1, and all others were assigned a
value of 0 (Fig. 1).
Voxel-based lesion–symptom mapping
VLSM analyses were conducted using the VoxBo brain imaging package (Kimberg and Aguirre, 2001). At each voxel, VoxBo performs a
one-tailed, independent sample t-test on the behavioural scores of
patients with and without lesions. To correct for multiple comparisons,
voxels with values exceeding a false discovery rate (FDR) threshold of
q = 0.05 were considered significant (Genovese et al., 2002). Only
voxels damaged in at least five participants were included in the analyses. The number of qualifying voxels was 384 896, or 52% of the
738 535 voxels in the left hemisphere based on the Automatic
Anatomic Labelling (AAL) atlas (Tzourio-Mazoyer et al., 2002).
In addition to raw behavioural measures, residualized scores were
computed by regressing one score against another to remove the
shared variance between scores. Residualized scores enabled assessment of voxels associated with performance that was disproportionately impaired on one task or component given performance on
another.
For all VLSM analyses, neuroanatomic labels for significant regions
were generated both with Brodmann and AAL atlases as implemented
in MRIcron.
Results
Behavioural results
As shown in Table 1, scores on the three gesture tasks were well
distributed. Cut-off scores for normal performance (two standard
deviations below the mean of age-matched healthy controls) were
79.8, 80.6 and 84.8 on GestTool, ImTool and ImNov, respectively,
based on normative data published previously (Buxbaum et al.,
2005a, 2007). On these criteria, 34, 41 and 32 patients performed
abnormally on GestTool, ImTool, and ImNov, respectively.
Months
post
27
55
23
20
21
8
12
14
9
10
22
20
14
14
Patients’ scores were equivalent on the GestTool and ImNov
tasks [mean 80.1 and 79.8, respectively, t(70) = 0.19, P = 0.85],
and more impaired on the ImTool task [mean 75.6, t(70) 4 2.5,
P 5 0.02 for both pairwise comparisons]. Scores on all three tasks
were moderately strongly correlated [r(69) 4 0.62, P 5 0.001 for
all three pairwise correlations]. Figure 2 shows examples of errors
in the GestTool condition.
Lesion analyses
Total scores
Figure 3 shows an overlap of the number of patients with lesions
in each voxel and suggests the relative power of each voxel for
detecting an association, if one exists. The map shows good coverage of the regions of interest in the posterior temporal, inferior
parietal, and frontal lobes, with 32 patients having lesions in the
regions of maximum overlap.
Table 2 and Fig. 4 provide VLSM results for the GestTool,
ImTool and ImNov tasks. For the GestTool task, a large region
in the posterior temporal cortex encroaching on extrastriate
visual cortex (Brodmann area 19) exceeded the FDR statistical
threshold. Smaller significant regions were observed in the inferior
parietal lobe and primary sensory area (S1), middle and inferior
frontal gyri, thalamus, and angular gyrus. For the ImTool task, a
large region exceeding the statistical threshold was again observed
in the posterior temporal lobe. In addition, a second region was
observed in primary somatosensory area (S1), primary motor area
(M1), and supramarginal gyrus. For the ImNov task, a large region
was seen in the posterior temporal lobe, along with additional
sizeable regions of significance in supramarginal gyrus, S1, M1
and angular gyrus, as well as other smaller non-contiguous posterior temporal areas.
As a supplementary analysis, we identified for each subject the
proportion of voxels lesioned in the regions that were identified as
significant in the group VLSM analysis. As expected, these proportions for each task were inversely correlated with magnitude of
behavioural deficits for each task (GestTool: r = 0.59,
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| Brain 2014: 137; 1971–1985
L. J. Buxbaum et al.
Figure 1 Illustration of the 71 left-hemisphere lesions displayed on a template brain. Lesions are represented on the surface of the brain
but display both cortical and subcortical damage to an 8-voxel search depth.
P 5 0.0001; ImTool: r =
P 5 0.0001).
0.61, P 5 0.0001; ImNov: r =
0.62,
Conjunction analyses
To characterize regions common to the two tool-related gesture
tasks (GestTool and ImTool), we performed a conjunction analysis
of voxels surpassing the FDR-corrected threshold in both analyses
(Nichols et al., 2005) by overlaying significant voxels from each
analysis on the same template using MRIcron. As Fig. 5 and
Table 2 show, there was a large common region in the posterior
temporal lobe, encroaching on extrastriate visual cortex and
angular gyrus.
Similarly, to characterize the regions common to the two imitation tasks (ImTool and ImNov), we performed a conjunction analysis of voxels that were significant in both tasks. Figure 5 and
Table 2 show that there were several common brain regions,
Tool-related and imitative actions
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Figure 2 Examples of hand and arm posture errors made by study participants on the pantomime to sight of tool task (GestTool). (A)
Hand and arm posture errors. In pantomiming eating with a fork, the participant shakes fist with thumb out (hand posture error) and
maintains arm in a fixed position lateral to the body throughout (arm posture error). (B) Hand posture error. In pantomiming winding a
watch, the participant forms a static precision grip (‘pinch’) and rotates the entire hand in a circle parallel to the watch-face.
including a large region in the posterior temporal lobe, and smaller
regions including M1 and S1, supramarginal gyrus, and angular
gyrus.
Posture and kinematic subscores
Next, we examined whether impairments on the three gesture
tasks were characterized by differential deficits in the postural or
kinematic components of actions. Table 3 shows all significant
results of these VLSM analyses.
Residual analyses
Figure 3 Map depicting lesion overlap of the 71 participants.
Only voxels lesioned in at least five subjects were included.
The regions rendered in purple and blue correspond to an
overlap of 5–15 participants. The regions rendered in aqua
and green correspond to an overlap of 16–23 participants.
Regions rendered in warm colours (yellow to dark red)
were lesioned in at least one-third of the sample (overlap
of 5 24 participants).
The ImTool task is unique among the three tasks we assessed in
that it is both imitative and tool-related. To disentangle the contributions of those two aspects of ImTool, we performed residual
analyses in which we controlled for the other two tasks. First, we
examined voxels associated with residualized scores for the posture and kinematic gesture components of ImTool controlling for
ImNov. In common to both imitation tasks is the requirement to
process the visual input of the body movements to be imitated
and to transform this input into an analogous plan of action to be
performed with one’s own limb. Removing this common variance
by way of a residual analysis enables examination of the uniquely
tool-related component of the ImTool task. As shown in Fig. 6 and
Table 3, the posture component of ImTool controlling for ImNov
was associated with a large cluster in the posterior temporal lobe,
extrastriate visual cortex, and angular gyrus. The kinematic component of ImTool controlling for ImNov was associated with no
significant voxels, even at a relaxed threshold of q = 0.1. This null
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| Brain 2014: 137; 1971–1985
L. J. Buxbaum et al.
Table 2 Brodmann’s and AAL regions of significant voxels in the GestTool, ImTool and ImNov analyses, intersection of
significant tool-related voxels, and intersection of significant imitation-related voxels
Peak
Gesture condition
AAL regions*
Brodmann areas*
Voxels
z-value
GestTool
Temporal_mid, temporal_inf, occipital_mid,
occipital_inf, fusiform, temporal_pole_sup,
temporal_sup, insula, hippocampus
Parietal_inf, postcentral
Frontal_mid, frontal_inf_tri
Thalamus
Angular, occipital_mid, temporal_mid
Temporal_mid, temporal_inf, occipital_mid,
occipital_inf, fusiform, temporal_sup
Postcentral, parietal_inf, supramarginal,
precentral
Temporal_inf, temporal_mid, occipital_inf,
fusiform
Temporal_sup, temporal_mid, supramarginal,
angular
Parietal_inf, supramarginal
Postcentral, precentral
Angular
Temporal_mid, occipital_mid, occipital_inf
Temporal_mid, temporal_inf, occipital_inf,
occipital_mid, fusiform, temporal_sup
Temporal_inf, temporal_mid, occipital_inf,
fusiform
Postcentral, precentral
Parietal_inf, supramarginal
Temporal_mid, temporal_sup
Temporal_mid, occipital_mid, occipital_inf
37, 21, 20, 19, 39,
48, 22, 38, 36
26221
5.18
51
43
6
48, 40, 3
44, 46, 45, 48
48
39
37, 21, 20, 19, 22,
39, 18, 42
3, 4, 40, 48, 2, 6, 43
1417
656
199
106
22407
4.16
3.81
4.32
3.39
5.22
23
39
27
39
41
28
26
17
60
65
34
33
4
25
7
3276
4.39
43
12
37, 20, 21
5844
4.59
52
35
22, 42, 21, 39, 48,
37, 41
40, 2, 3
4, 3, 6
39
37
37, 21, 20, 19, 39, 22
1199
3.85
56
49
13
1153
746
198
192
18514
4.02
4.32
3.62
4.26
51
43
53
53
55
35
12
58
71
49
38
37
33
3
23
37, 20, 21
5582
52
56
19
4, 3, 6
40, 2, 3
22, 21, 37, 39, 42
37
717
564
534
192
42
51
63
51
16
40
52
71
ImTool
ImNov
Tool-related conjunction
Imitation conjunction
x
y
z
37
15
35
37
10
3
*Brodmann and AAL regions listed in descending order of number of voxels involved within that area. Brodmann areas with 510 significant voxels not shown.
Inf = inferior; sup = superior.
Figure 4 Maps of the reliability (Z-scores) of the difference between patients with and without lesions in each voxel in (A) gesture to the
sight of tools (GestTool), (B) imitation of tool-related gestures (ImTool), and (C) imitation of novel gestures (rendered on the MNI space
ch2bet volume). For each of the three maps, voxels rendered in warm/hot colours correspond to Z-scores 4 3.02, 2.7, and 2.7, respectively, that reached the FDR-corrected threshold of q 5 0.05. Voxels rendered in blue correspond to voxels associated with FDRcorrected thresholds between q = 0.05 and q = 0.1.
Tool-related and imitative actions
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Figure 5 Maps of the conjunction of the voxels reaching the FDR-corrected threshold of P 5 0.05 in two of the three gesture conditions.
(A) Conjunction of voxels meeting the threshold for the two tool-related tasks (gesture to the sight of tools and imitation of tool-related
gestures). (B) Conjunction of voxels meeting the threshold for the two imitation tasks (imitation of tool-related gestures and imitation of
novel gestures).
Table 3 Brodmann and AAL regions of significant voxels in the posture subcomponent scores of the GestTool and ImTool
tasks, in the kinematic subcomponent scores of the ImTool and ImNov tasks, in the posture scores of ImTool controlling for
ImNov, and the kinematics scores of ImTool controlling for GestTool
Peak
x
y
z
Gesture condition
AAL regions*
Brodmann areas
Voxels
z-value
GestTool posture
Temporal_mid, temporal_inf, occipital_mid,
occipital_inf, fusiform, temporal_sup,
temporal_pole_sup, hippocampus
Temporal_mid, temporal_inf
Frontal_mid
Temporal_mid, temporal_inf, occipital_mid,
occipital_inf, fusiform, temporal_sup
Angular
Parietal_inf, supramarginal
Temporal_mid, temporal_inf, occipital_inf,
occipital_mid, fusiform, temporal_sup
Postcentral, parietal_inf, precentral,
supramarginal, rolandic_oper,
temporal_sup
Temporal_pole_sup, insula
Temporal_sup, temporal_inf
Frontal_inf_orb, insula
Temporal_inf, temporal_mid,
occipital_inf, fusiform
Postcentral, precentral, parietal_inf
Parietal_Inf, supramarginal
Postcentral, rolandic_oper
Temporal_mid, occipital_mid, occipital_inf
Temporal_sup, temporal_mid
Temporal_mid, temporal_inf, occipital_inf,
occipital_mid, fusiform
Postcentral, precentral, supramarginal,
parietal_Inf
37, 21, 20, 19, 39,
22, 48, 36, 38
22835
5.83
56
45
20, 21
46, 45
37, 21, 20, 19, 22,
39, 18, 42
39
2, 40, 3
37, 20, 21, 19, 39,
22, 48
3, 48, 4, 43, 6, 2,
40, 1, 22
361
126
23565
3.08
3.69
5.42
64
41
41
25
36
65
16
39
7
140
112
15425
3.29
3.33
4.91
55
57
56
62
28
38
34
41
16
13868
5.12
41
13
38
191
176
122
6196
3.69
3.74
3.78
5.35
26
64
27
42
53
25
43
4, 3, 6, 43, 48
40, 2, 3
1, 2, 3
37
22
37, 21, 20, 19, 39, 22
1213
445
247
164
101
14143
4.45
3.68
3.68
4.5
3.39
4.98
41
57
61
50
56
51
13
28
12
71
49
67
38
41
22
2
13
10
4, 3, 43, 6, 2, 48, 1
2467
4.87
61
14
41
ImTool posture
ImTool kinematics
ImNov kinematics
Posture: ImTool
controlling for ImNov
Kinematics: ImTool
controlling for GestTool
38,
22,
47,
20,
48, 34
21
38
37, 21
6
*Brodmann and AAL regions listed in descending order of number of voxels involved within that area. Brodmann areas with 510 significant voxels not shown.
Inf = inferior; sup = superior.
5
20
11
14
2
1980
| Brain 2014: 137; 1971–1985
L. J. Buxbaum et al.
Figure 6 Maps of the reliability (Z-scores) of the difference between patients with and without lesions in each voxel in (A) posture scores
on ImTool controlling for posture scores on ImNov, (B) kinematic scores on ImTool controlling for kinematic scores on GestTool (rendered
on the MNI space ch2bet volume). For each of the two maps, voxels rendered in warm/hot colours correspond to Z-scores 4 3.4 and 2.9,
respectively, that reached the FDR-corrected threshold of q 5 0.05. Voxels rendered in blue correspond to voxels associated with FDRcorrected thresholds between q = 0.05 and q = 0.1.
effect is likely to result from the substantial overlap in voxels
associated with the kinematic component in these two tasks
(Table 3).
Finally, we assessed the voxels associated with impaired performance on ImTool controlling for GestTool. By removing the
variance associated with access to the actions associated with
tools, irrespective of whether the input is gestural or a tool, this
analysis enabled assessment of the aspects of the ImTool task that
are specifically relevant to imitation. There were no significant
voxels associated with the posture component of ImTool controlling for GestTool, even at a relaxed threshold of q = 0.1. This null
effect is likely to derive from the substantial overlap in voxels
associated with the posture component for these two tasks
(Table 3). For the kinematic component of ImTool controlling for
GestTool, there was a large significant region that included M1,
S1 and S2.
Discussion
We performed VLSM with 71 left-hemisphere stroke patients to
assess the critical substrates of producing tool-related and imitative
gestures. To our knowledge, this is the largest sample of stroke
patients with lesion data to have been prospectively tested with
reliably-scored gesture tasks (see also Manuel et al., 2013 for a
retrospective study using clinical data). While past functional neuroimaging studies have revealed a broadly distributed bilateral network of regions activated in gesture tasks, the present data
permitted us to precisely delineate the regions which, when
lesioned, result in deficits in tool-related and imitative gesture production. Moreover, separate scoring of the postural and kinematic
aspects of these tasks enabled us to assess the role of different
brain regions in supporting these components of praxis.
Consistent with predictions derived from previous studies and
our own model of the praxis system (Buxbaum, 2001), impairments in all three of the gesture tasks we studied were associated
with lesions in left posterior temporal, inferior parietal, motor, and
premotor regions. Perhaps more interestingly, the data revealed
that tool-related actions, whether imitative or in response to
viewed tools, are critically dependent on a large region of left
posterior middle and inferior temporal lobe, as well as bordering
regions of the occipital lobe. Both imitation tasks, in contrast,
whether in response to familiar or novel actions, are dependent
on a smaller posterior temporal region, as well as primary and
secondary motor and sensory cortices and inferior parietal lobe.
Additionally, we hypothesized that tool-related and imitative
actions would depend differentially on the integrity of postural
and kinematic subcomponents of actions, respectively. Analyses
with raw data as well as more refined residual analyses demonstrated that the postural components of tool-related actions are
associated with posterior temporal regions, whereas the kinematic
components of imitative actions rely upon regions specialized for
motor, tactile, spatial, and body-related processing. There is thus a
nearly complete double dissociation in the brain regions specialized
for postural versus kinematic components of gestural action. In
contrast, the posture component for novel imitation and the kinematic component for gesture to the sight of tool were not associated with significant voxels. We may speculate that the former
null effect lies with the novelty of the gestures; there is no ‘stored’
component to the actions being imitated, and it is the stored
component that is largely postural and mediated by the posterior
middle temporal gyrus. We may speculate, conversely, that the
latter null effect was obtained because gesture to the sight of
tool relies relatively more reliably on the stored, postural
component.
Tool-related and imitative actions
Posterior temporal lobe and extrastriate
cortex
The conjunction of the two tool-related tasks (ImTool and
GestTool) showed a large area of significance in the posterior
temporal lobe, extending into extrastriate cortex and marginally
into the angular gyrus. Moreover, the residual analysis of ImTool
posture scores controlling for ImNov posture scores indicated the
same region of significance, suggesting that deficits in the postural
element drive the significance of the tool-related conjunction results. The posterior temporal lobe is viewed as a major component
of the ventral ‘what’ pathway, specialized for object recognition
(Ungerleider and Mishkin, 1982). Thus, a novel aspect of the present data is evidence that the posterior temporal lobe is critical for
tool-related gesture production, and in particular, its postural components. Importantly, evidence for posterior temporal (as well as
extrastriate visual cortex) involvement was observed not only in
the GestTool condition, but even when no tool was present in the
ImTool condition, indicating that the effects are not attributable to
demands on tool recognition.
Instead, the data are consistent with an increasingly rich description of the computations that are carried out in a temporal-occipital region that includes area MT + , extrastriate body area, and
posterior temporal lobe. Area MT + , also known as area V5
(Watson et al., 1993), is a region that seems to encode the
speed and direction of rigid, unarticulated motion, as is characteristic of tools (see also Beauchamp, 2005; Beauchamp and Martin,
2007). Inferior to area MT + in the posterior inferior temporal
sulcus is the extrastriate body area (Downing et al., 2001,
2006), a region playing a role in both the perception and production of hand and arm actions (Astafiev et al., 2004; Orlov et al.,
2010; Gallivan et al., 2013). The present data thus add to a
growing body of evidence that extrastriate visual cortex plays a
role in action processing.
Anterior to these regions lies the posterior middle temporal
gyrus, a region with known relevance for the representation of
action knowledge. For example, posterior middle temporal gyrus
lesions disrupt the ability to match action verbs to videos of gestural actions (Tranel et al., 2003; Kalenine et al., 2010), and posterior middle temporal gyrus is consistently activated in functional
neuroimaging studies assessing semantic tool knowledge. Watson
and Chatterjee (2012) (see also Watson et al., 2013) have argued
that the proximity of posterior middle temporal gyrus to area
MT + facilitates the derivation of abstract representations from
visual motion in posterior middle temporal gyrus (Kable et al.,
2002, 2005).
The proposal that posterior middle temporal gyrus representations
are abstractions of various instances of visual experience is partly
consistent with our previous proposals (Buxbaum, 2001; Binkofski
and Buxbaum, 2013), but more strongly emphasizes the putatively
visual format of the posterior middle temporal gyrus component of
distributed gesture representations. As a consequence of repeated
experiences, a given skilled gesture can be recognized readily despite
variations in viewing angle, gesture size and shape associated with
the physical properties of the exemplar of the tool being handled,
task goals, and environmental constraints.
Brain 2014: 137; 1971–1985
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The present finding of specialization of the posterior temporal
lobe for the production of postural aspects of tool-related actions
extends what is known of the role this region plays in mediating
semantic concepts for manipulable objects (Kalenine et al., 2009,
2010; see also Almeida et al., 2013; Mahon et al., 2013 for
related data). Moreover, the present data suggest that the postural aspects of gesture may be among the ‘features’ upon which
a system of tool-related action knowledge is organized (Klatzky
et al., 1987; Lee et al., 2013; Watson and Buxbaum, under revision). Thus, the visual similarity of the postural aspects of actions
may shape relationships between tool representations in the posterior temporal lobe (see Bracci and Peelen, 2013 for related data).
Finally, there was also evidence for some involvement of the
posterior temporal region in kinematic aspects of gesture (Fig. 6B).
Parallel to what has been described in theoretical models of the
stages of lexical and phonological access in the language domain
(Goldrick and Rapp, 2007), the temporal lobe aspect of kinematic
representations may contain some degree of abstraction over multiple instances, and thus be less specified in terms of spatiomotor
parameters than the parietal lobe kinematic component.
Inferior parietal lobe
Although the inferior parietal lobe was critical to all three tasks,
the largest swath of significant anterior and posterior parietal regions was revealed in the two imitation tasks (ImTool and ImNov)
and, accordingly, their conjunction, including S1, angular gyrus,
and supramarginal gyrus. These data are consistent with a
number of functional imaging studies (Muhlau et al., 2005),
including a recent activation likelihood estimation meta-analysis
showing that inferior parietal lobe is commonly activated in imitation tasks (Molenberghs et al., 2010, 2012).
Extending these data, the present results showed that the kinematic components of the imitation tasks drive the significance of
the results in the inferior parietal lobe. These findings are consistent with observed deficits in the spatiotemporal aspects of gesture
imitation and recognition in patients with inferior parietal lobe lesions (Halsband et al., 2001; Goldenberg, 2009; Kalenine et al.,
2010), and with data showing that lesions to this region may
disproportionately affect meaningless imitation (Goldenberg,
2009) as compared with tool-related movements (Manuel et al.,
2013; but see Vingerhoets et al., 2009; Peeters et al., 2013; and
Sunderland et al., 2013 for evidence for supramarginal gyrus involvement in tool-related actions). Finally, the secondary somatosensory area (S2, also known as Brodmann area 43), a region in
the parietal operculum, was also implicated in the kinematic aspects of the imitation tasks. The finding of S2 involvement may be
interpreted in light of the role of this region in both input and
output processing, i.e. ‘mirror properties’ (Molenberghs et al.,
2012; see also Mengotti et al., 2013).
Frontal lobe
In addition to the double dissociation between temporal and parietal significance in postural versus kinematic aspects of movement, respectively, another striking aspect of the present data is
a second double-dissociation in the regions of the frontal lobe
1982
| Brain 2014: 137; 1971–1985
critical for the three different gesture tasks assessed. Both imitation
tasks were associated with significant voxels in M1 as well as
premotor cortex (Brodmann area 6). Conversely, the gesture to
the sight of tools task (GestTool) showed little to no Brodmann
area 6 involvement. Instead, frontal involvement in the GestTool
task was more anterior, in middle frontal gyrus and inferior frontal
gyrus of prefrontal cortex (Table 2). Moreover, at least some of
the significance in these regions was driven by the postural and
not kinematic aspects of action (GestTool posture analysis,
Table 3).
Left inferior and middle frontal gyrus have long been recognized
as important contributors to the performance of gestural movements. Haaland et al. (2000) demonstrated that middle frontal
gyrus was the sole region of overlap in patients characterized as
having ideomotor apraxia on the basis of an imitation task. On the
other hand, Goldenberg et al. (2007a) showed that pantomime of
tool use from photographs depends critically on inferior frontal
gyrus (Bohlhalter et al., 2011). The previously-noted meta-analysis
of functional MRI data from Caspers et al. (2010) indicated that
numerous areas in the frontal lobe, including Brodmann areas 44,
45 and 46, were activated in imitation tasks.
Thus, the precise role of different prefrontal regions in imitation
and pantomime is unclear. One possibility is that relatively dorsal
versus ventral prefrontal regions contribute to the response selection as compared to semantic selection requirements of gestural
tasks. A number of investigations report that selection among
competing motor responses mainly activates dorsolateral prefrontal cortex, a portion of middle frontal gyrus (Schumacher
and D’Esposito, 2002; Schumacher et al., 2003; Ridderinkhof
et al., 2004), whereas selection among competing semantic alternatives activates ventrolateral prefrontal cortex in the inferior frontal gyrus (Thompson-Schill et al., 1997; Crosson et al., 2001;
Tremblay and Gracco, 2006, but see Thompson-Schill et al.,
1998; Fletcher and Henson, 2001; Rowe and Passingham, 2001;
Nagel et al., 2008). In the present data, we observed both middle
frontal gyrus and inferior frontal gyrus involvement in the
GestTool task, but not in the imitation tasks. This may reflect
the possibility that although gesture to the sight of tools taxes
both response selection (i.e. manipulable objects may be associated with more than one response) and semantic selection (i.e.
selecting the tool features relevant for tool-use), the two imitation
tasks do not include these selection requirements. On the other
hand, the strong interconnectivity of motor, premotor, and prefrontal cortex with the parietal lobe suggests that frontal regions
would not be expected to play a specific role only in tool-related
movements (Ramayya et al., 2010; and see Groh-Bordin et al.,
2009 for evidence from meaningless gesture imitation). Thus, the
precise role of prefrontal cortex in gesture tasks requires additional
investigation.
Absence of superior frontoparietal and
intraparietal sulcus significance
As with most stroke samples, the vast majority of our patients
suffered strokes of the middle cerebral artery, which perfuses
much of the convexity of the hemisphere, but not the superior
L. J. Buxbaum et al.
parietal or superior frontal lobes. Numerous functional neuroimaging studies have described activation in superior parietal and
intraparietal sulcus regions during gesture tasks (Johnson-Frey
et al., 2005b; Kroliczak and Frey, 2009; Menz et al., 2009;
Agnew et al., 2012). Given that the subset of patients with lesions
in these regions was relatively small (8–15 subjects), our analyses
may have lacked sufficient power to detect significant effects in
the relevant voxels. At a relaxed statistical threshold, we observed
several small sub-threshold regions in the anterior intraparietal
sulcus in the GestTool task, as well as in a region including superior M1 and superior Brodmann area 6 in the residual analysis for
the kinematics of ImTool controlling for GestTool. These data are
consistent with the putative role of the dorso-dorsal visual processing stream in the spatiomotor aspects of movement
(Buxbaum, 2001; Rizzolatti and Matelli, 2003), and with the fact
that superior frontoparietal regions are frequently affected in patients with corticobasal syndrome, who exhibit a form of limb
apraxia that tends to affect meaningless more than meaningful
gestures (Buxbaum et al., 2007). Future investigations with even
larger samples will be required to confirm these subthreshold
results.
The distributed visuokinaesthetic
engram: implications for theoretical
models of gesture production
Although several accounts of gesture production distinguish between representational (or semantic) and ‘on-line’ or ‘productionrelated’ aspects of action in the left hemisphere (Roy and Square,
1985; Gonzalez Rothi et al., 1992), the present data are the first,
to our knowledge, to provide direct evidence that postural and
kinematic components of gestural action are neuroanatomically
distinct. We proposed that the kinematic component is most sensitively assessed with imitation of novel, meaningless gestures, and
the semantic component with pantomimed gesture production in
response to viewed tools. We observed a dorsal versus ventral
distinction between these action components, with imitation of
novel gestures relying strongly on the inferior parietal lobe, and
gesture to the sight of tools dependent upon the posterior temporal lobe. Moreover, we also showed that it is the kinematic
aspects of gestural action, in particular, that rely upon inferior
parietal and frontal regions, as compared with the postural aspects
of (meaningful) action, which are dependent upon the left posterior temporal lobe. These data permit us to refine the claim that
there are ‘direct’ and ‘indirect’ routes to action (Rothi et al., 1992;
Rumiati and Humphreys, 1998) with evidence that the two routes
are in fact aspects of a distributed system supported by relatively
more dorsal versus ventral regions, respectively. Beyond this, an
important contribution of the present data is the demonstration
that aspects of processing required for gesture production are
subserved by regions traditionally conceived as part of the ‘ventral’
visual processing stream.
The proposal that gesture posture representations are based
upon abstracted patterns of visual feature co-occurrence is similar
to several accounts of the organization of the visual semantic
system in the posterior temporal lobe (McNorgan et al., 2007;
Tool-related and imitative actions
Dilkina and Lambon Ralph, 2012). By extension, findings that
tool-related actions depend on the posterior temporal lobe, and
that posture scores drive posterior temporal significance, suggest
that abstraction over multiple instances of experience in seeing
tool actions of the self and others may be derived at least in
part from visual motion information (Watson and Chatterjee,
2011). In contrast, the current details of an action’s timing and
trajectory, fleshed out on-line on the basis of environmental constraints, may be relatively more spatiomotor in format. This differentiation, in turn, suggests that an important process occurring
between the temporal and parietal lobe is gradual transformation
of information from one format to another. Thus, at least in the
case of tool-related actions, kinematic processing in the parietal
lobe may be conceptualized as a translational capacity that enables
transformation of a visual-motion representation in the posterior
temporal lobe to one closer to readiness for motor output as it
passes through the parietal lobe (see Pisella et al., 2006 for a
related proposal).
We suggest that the component that the inferior parietal lobe
contributes is the computation of movement plans in terms of
dynamic changes in the relative spatial positions of body parts
needed to reach a goal configuration. Such movement planning
in ‘intrinsic’ spatial coordinates (Rosenbaum et al., 2001; Jax et al.,
2006; Orban de Xivry et al., 2011; Parmar et al., 2011; Brayanov
et al., 2012) is viewed as a preparatory step toward specification
of the precise muscles that must participate in the movement.
Unlike the visual tool-use representations subserved by the posterior temporal lobe, the computation of intrinsic coordinate control relies upon somatosensory processing. Consequently, patients
with deficits in intrinsic coordinate control are abnormally reliant
upon visual feedback of their own limb position in posture imitation tasks (Jax et al., 2006; see also Haaland et al., 1999;
Buxbaum et al., 2005b).
Role of left and right hemisphere
regions in gesture production
Finally, as noted above, many functional neuroimaging studies
have demonstrated that numerous bilateral regions are activated
in gesture production tasks, regardless of the hand used. There are
several explanations for the discrepancy between these findings
and those from the patient literature, including those reported
here, which suggest that imitation and pantomime may be severely disrupted by lesions to the left hemisphere alone. One possibility is that bilateral activation reflects the potential for acting
with both hands despite the unimanual nature of most tasks performed in the scanner. A second, related possibility is that right
hemisphere activations may reflect strong connectivity between
homologous left and right hemisphere regions subserving action
(see Culham et al., 2006 for a similar argument). The present data
suggest that the observed right hemisphere activations may reflect
a relatively subtle (perhaps modulatory) role in gesture production,
and underscore the continued importance of detailed studies of
lesioned patients in advancing knowledge of the functional architecture of the human brain.
Brain 2014: 137; 1971–1985
| 1983
Acknowledgements
Many thanks to Christine Watson, who assisted with lesion analyses and provided helpful suggestions on an earlier draft of this
manuscript, to the research assistants who tested participants and
scored data, to two anonymous reviewers for their constructive
and insightful comments, and to the many participants who volunteered their time and efforts to this study.
Funding
Supported by NIH R01-NS065049 to Laurel Buxbaum.
Supplementary material
Supplementary material is available at Brain online.
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