NeuroImage 43 (2008) 634–644
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NeuroImage
j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / y n i m g
Action word meaning representations in cytoarchitectonically defined primary and
premotor cortices
Natasha Postle a, Katie L. McMahon b, Roderick Ashton a, Matthew Meredith b, Greig I. de Zubicaray b,⁎
a
b
School of Psychology, University of Queensland, Brisbane, QLD, Australia
Functional MRI Laboratory, Centre for Magnetic Resonance, University of Queensland, Brisbane, QLD, Australia
a r t i c l e
i n f o
Article history:
Received 7 April 2008
Revised 8 July 2008
Accepted 5 August 2008
Available online 16 August 2008
Keywords:
Language comprehension
Motor function
Mirror neurons
Somatotopy
Verbs
Semantic memory
a b s t r a c t
Recent models of language comprehension have assumed a tight coupling between the semantic
representations of action words and cortical motor areas. We combined functional MRI with cytoarchitectonically defined probabilistic maps of left hemisphere primary and premotor cortices to analyse responses of
functionally delineated execution- and observation-related regions during comprehension of action word
meanings associated with specific effectors (e.g., punch, bite or stomp) and processing of items with various
levels of lexical information (non body part-related meanings, nonwords, and visual character strings). The
comprehension of effector specific action word meanings did not elicit preferential activity corresponding to
the somatotopic organisation of effectors in either primary or premotor cortex. However, generic action word
meanings did show increased BOLD signal responses compared to all other classes of lexical stimuli in the
pre-SMA. As expected, the majority of the BOLD responses elicited by the lexical stimuli were in association
cortex adjacent to the motor areas. We contrast our results with those of previous studies reporting
significant effects for only 1 or 2 effectors outside cytoarchitectonically defined motor regions and discuss the
importance of controlling for potentially confounding lexical variables such as imageability. We conclude that
there is no strong evidence for a somatotopic organisation of action word meaning representations and argue
the pre-SMA might have a role in maintaining abstract representations of action words as instructional cues.
© 2008 Elsevier Inc. All rights reserved.
Introduction
It is now generally accepted that word meaning is represented in
multiple areas of human cortex. This much was proposed by models of
language comprehension in the mid-late nineteenth century. The
classical Wernicke–Lichtheim model considered concepts to be
distributed throughout the cerebral cortex, aroused by associations
among speech perception and production related memory “images” in
the left hemisphere superior temporal and inferior frontal cortices. As
early as 1885, Lichtheim had proposed anatomically distributed and
interconnected conceptual centres (see his Fig. 7; Compston, 2006;
Smith, 1996), while Freud (1891) would later propose a distributed
object concept system linked to word meanings (Henderson, 1992).
Modern extensions and revisions of these early models continue to
adhere to this precept, often making the additional assumption that
representation of word meaning involves distributed networks of
motor and somatosensory areas (e.g., Gallese and Lakoff, 2005; Martin
and Chao, 2001; Tranel et al., 2001).
Some recent models of language comprehension have assumed a
direct coupling between action meaning representations and cortical
motor areas. One mechanism proposed to give rise to such a coupling
⁎ Corresponding author. Fax: +61 7 3365 3833.
E-mail address: [email protected] (G.I. de Zubicaray).
1053-8119/$ – see front matter © 2008 Elsevier Inc. All rights reserved.
doi:10.1016/j.neuroimage.2008.08.006
is Hebbian learning, whereby “any two cells or systems of cells that are
repeatedly active at the same time will tend to become ‘associated’, so
that activity in one facilitates activity in the other” (Hebb, 1949, p. 70).
Hence, the frequent co-presentation of an action word with the
execution of the action the word refers to might result in a
representation being associated with those motor areas (Pulvermüller,
1996, 2005). Alternatively, a class of visuomotor neurons in premotor
cortex – mirror neurons – that respond congruently when an action is
both observed and executed might serve to transform visual
information into knowledge coded at an abstract level (Rizzolatti
and Craighero, 2004). This mechanism might permit action knowledge to be retrieved by action related words (verbs).
Indirect evidence for cortical motor area involvement in action
word meaning representation has been provided by transcranial
magnetic stimulation (TMS), behavioural and neuroimaging studies.
For example, several TMS studies have shown that processing of
action related words and sentences is modulated by TMS-induced
changes in excitability of left hemisphere cortical motor areas. During
application of TMS, Pulvermüller et al. (2005) demonstrated faster
lexical decisions to visually presented action words, while Buccino et
al. (2005) noted responses slowed when participants listened to
effector related action sentences. Oliveri et al. (2004) and Buccino et
al. (2005) reported, respectively, that motor evoked potentials (MEPs)
recorded from effector muscles were enhanced or reduced when TMS
N. Postle et al. / NeuroImage 43 (2008) 634–644
was applied at long or short temporal intervals following action word
presentation. Behavioural studies have also shown that action word
processing can affect motor performance deleteriously when presented shortly after action onset (b200 ms; e.g., Boulenger et al.,
2006). In order to explain these apparently contradictory facilitation
and interference effects, Boulenger et al. (2006) have recently
suggested the former could reflect post-lexical engagement of motor
imagery mechanisms while the latter might be due to competition for
common motor resources occurring during lexical access. More
recently, Tomasino et al. (2008) reported that TMS applied at both
long and short intervals following action word presentation facilitated
motor responses when participants were instructed to imagine
themselves performing the action, although not for simple reading
or frequency judgement conditions.
Neuroimaging studies have provided relatively consistent evidence
that retrieval of action word meanings activates cortical areas within
the vicinity of the left precentral gyrus (e.g., Canessa et al., 2008;
Rüschemeyer et al., 2007; Vigliocco et al., 2006; see Pulvermüller,
2005 for an overview of earlier work). A more precise localisation to
actual motor areas has been suggested by several recent studies that
attempted to link action word meaning representations (e.g., punch,
stomp or bite) associated with specific effectors (i.e., hand, foot or
mouth) to somatotopically organised motor areas (e.g., Aziz-Zadeh et
al., 2006; Hauk et al., 2004; Tettamanti et al., 2005). In order to
demonstrate a congruent somatotopic organisation of action meaning
representations, two of these functional MRI studies first identified
areas involved in action execution (Hauk et al., 2004) and observation
(Aziz-Zadeh et al., 2006) within inferior frontal, precentral and middle
frontal gyri according to the involvement of their related effectors.
These functionally defined motor regions were then interrogated for
activity during reading of effector related action words or sentences.
These studies reported BOLD signal differences for comparisons
between effector action words and a single control condition that
were in some cases only indicative of a trend (e.g., effector pairwise
comparisons at p b .1; e.g., Aziz-Zadeh et al., 2006) or only significant
for two effectors when ROI overlap was the criterion (e.g., Hauk et al.,
2004; see Kung et al. (2007) for a systematic critique of ROI overlap
analyses). To our knowledge, no neuroimaging study has yet reported
significant effects for all three effectors consistent with a complete
somatotopic organisation.
Unfortunately, macrostructural features such as gyri and sulci tend
not to be reliable indicators of cytoarchitectonic borders (Amunts et al.,
2007). Premotor (PM) cortex in particular has no macroanatomical
landmark to indicate the border between it and the prefrontal cortex
anteriorly where more cognitive functions predominate (Geyer, 2003).
Neuroimaging and stimulation studies have indicated a ventral to
dorsal somatotopic organisation paralleling that of the primary motor
cortex (area 4), and like the monkey (e.g., Godschalk et al., 1995),
successive overlap of effector representations (Sanes and Schieber,
2001; Schubotz and von Cramon, 2003). However, unlike the lateral
surface of monkey PM cortex, the dorsal (PMd) and ventral (PMv)
sectors of area 6 in humans have no cytoarchitectonic features that
might distinguish them (Picard and Strick, 1996). In addition, within
the medial subdivision of PM cortex, the rostrally located presupplementary motor area (pre-SMA) shows little evidence of distinct
effector related areas, and may instead support more abstract or
cognitive functions, while the caudally situated SMA-proper has a
clearer rostrocaudal somatotopic organisation (Picard and Strick,1996).
Given the issues associated with localising responses accurately to
motor areas in neuroimaging studies, we plotted the peak maxima
reported by previous investigations in relation to cytoarchitectonic
maximum probability maps (MPMs) of human primary and PM cortex
derived from microcellular studies of post-mortem brains (i.e., areas 4
and 6; Eickhoff et al., 2006; Geyer, 2003). The MPM technique is robust
to areal misclassifications of voxels and provides a “sufficient” coverage
of the cytoarchitectonic volume (Eickhoff et al., 2006). We plotted
635
relatively large 10 mm spheres around the peak maxima from these
studies rather than their reported spatial extents as different thresholds or thresholding strategies used across studies result in activations
of varying sizes (see Eickhoff et al., 2007). We reasoned that if action
meaning representations are indeed organised somatotopically, then
one would expect them to be located within the cytoarchitectonic
borders of primary motor and PM cortex where motor somatotopy has
been demonstrated by stimulation and neuroimaging studies. As can
be seen from Fig. 1, this was not the case. In some instances, there was
little agreement across studies for peaks reported for a given effector,
an issue that we will discuss in more detail later (e.g., Aziz-Zadeh et al.,
2006; Hauk et al., 2004; Tettamanti et al., 2005).
It is important to note that even if the activity reported by these
studies had been located within the cytoarchitectonic MPMs, it would
not constitute definitive proof that these areas mediate semantic
representations of action words. An alternative interpretation is that
this activity may reflect the by-product of imagery of an action (e.g.,
Jeannerod, 2001), emerging only following identification of the action
concept and not being part of the representation of the action word
per se (Willems and Hagoort, 2007). For example, Tomasino et al.
(2007) reported motor cortical activity when their participants
imagined the situation described in an action phrase, but not when
they performed a secondary letter detection task designed to prevent
imagery. In an attempt to minimise the influence of imagery, studies
have typically administered the comprehension task first, followed by
action execution (Hauk et al., 2004) or observation tasks (Aziz-Zadeh
et al., 2006).
A more direct experimental control would be to include a
condition involving imageable, concrete words. Comparisons to date
have been between action word meanings and abstract word meanings (Aziz-Zadeh et al., 2006; Tettamanti et al., 2005) or visual
character strings (Hauk et al., 2004), neither of which elicit
comparable imagery. In order to control for motor imagery per se,
action words would need to be employed as control stimuli, which
would clearly introduce an experimental confound. However, a
number of neuroimaging studies have reported that reading concrete
words unrelated to motor function evokes activity in left hemisphere
motor areas when contrasted with reading of less imageable abstract
words (e.g., D'Esposito et al., 1997; Mellet et al., 1998; Pulvermüller
and Hauk, 2006), indicating that they might prove adequate for
eliciting generic imagery related activity in motor areas.
In the present study, we combined functional MRI with cytoarchitectonically defined probabilistic maps of primary and PM cortex to
analyse the responses of both movement execution- and observationrelated regions during retrieval of action word meanings associated
with specific effectors. The use of both action observation and
execution conditions to demonstrate overlapping activity is a
necessary requirement for confirming the operation of mirror neurons
(see Turella et al., 2008). It is worth noting that the neuroimaging
studies cited in support of shared action word meaning comprehension and mirror neuron activity have tended to employ only action
observation tasks (e.g., Aziz-Zadeh et al., 2006) or omitted action tasks
altogether (e.g., Tettamanti et al., 2005). We also employed a range of
conditions controlling for various levels of lexical information,
including concrete words of equivalent imageability unrelated to
body parts or actions, regular phonology (nonwords) and visual
character recognition (hashes). This represents, to our knowledge, the
first systematic attempt to test a proposed somatotopic organisation
of action word meaning representations with fMRI.
Materials and methods
Participants
Eighteen (13 females, 5 males) healthy, right handed, native
English speaking volunteers participated in this study. The mean age
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N. Postle et al. / NeuroImage 43 (2008) 634–644
Fig. 1. Peak maxima from fMRI studies reporting overlap of action word meaning representations with left hemisphere effector areas in relation to cytoarchitectonic maximum
probability maps (MPMs; Eickhoff et al., 2006; Geyer, 2003) of primary motor (in red) and premotor (in blue) cortices. 10 mm spheres centred on reported maxima are shown overlaid
on coronal slices from a single subject's brain in MNI atlas space and colour-coded according to study.
was 28.72 years (SD = 7.21). Informed consent was obtained from all
participants and the experimental protocol was approved by the
University of Queensland's Medical Research Ethics Committee.
Materials
Verbal stimuli
Action word stimuli were 75 English language effector related
verbs comprising 25 each specific to the hand, foot and mouth (see
Supplementary material). Following Hauk et al. (2004), both transitive
and intransitive verbs were used in order to obtain a sufficient number
of stimuli for each effector type. These were presented in infinitive
form as single words, consistent with previous studies (e.g., Hauk et
al., 2004; Pulvermüller et al. 2005; Rüschemeyer et al., 2007). An
additional 25 concrete nouns unrelated to body parts or actions1, 25
nonwords and a series of six hashes (######) were included to
control for generic (i.e., non-body part related) meaning, phonological
and visual character processing (see Table 1; a full list of stimuli may
be requested from the corresponding author).
All words were one to two syllables and three to seven letters in
length. Stimuli were matched across categories for the number of
syllables, number of letters, orthographic and phonological neighbourhood sizes (Davis, 2003), and lexical frequency of the effector
related and unrelated words as determined by the CELEX lexical
database (Baayen et al., 1995). The effector related and unrelated
1
Although the unrelated words are concrete nouns rather than verbs, studies using
both TMS and neuroimaging have demonstrated consistently that the activity elicited
in primary and PM cortex during word reading is not modulated by grammatical class
(e.g., Bedny and Thompson-Schill, 2006; Gerfo et al., 2008; Oliveri et al., 2004;
Vigliocco et al., 2006).
words were also matched for imageability (see Table 2). Each effector
related word was predominantly associated with its appropriate
effector and each unrelated word was not associated with any body
part. This was determined by pilot testing of 92 effector related and 33
unrelated words (from which the target words were chosen) by an
independent sample of ten native or longstanding English-speakers (7
females, 3 males; M age = 23.90, SD age = 9.30) who indicated what (if
any) body part they associated with each word using a similar rating
procedure to that of Hauk et al. (2004) with a five point scale (1 = word
does not remind me of this body part at all; 5 = word very much
reminds me of this body part). These participants also rated each
word's imageability on a five point scale (1 = not imageable at all;
5 = very imageable). The nonwords were obtained from the ARC NonWord Database (Rastle et al., 2002) and contained a relatively even
mix of letters.
Video stimuli
Video stimuli consisted of 30 silent movie clips, with 10 each
involving the hand, foot or mouth performing simple actions
repeatedly for 5 s. The frame was cropped such that only the relevant
Table 1
Examples of word and nonword stimuli used in the lexical task
Hand words
Leg words
Mouth words
Unrelated words
Nonwords
Pick
Draw
Hold
Grip
Stir
Kick
Step
Limp
Wade
Hike
Chew
Suck
Kiss
Sing
Grin
Moon
Lake
Hill
Wall
Rain
Vuxt
Oits
Bume
Tron
Biln
N. Postle et al. / NeuroImage 43 (2008) 634–644
637
Table 2
Matching variables for the lexical stimuli used in the study
Matching variables
Category
Letters
Syllables
Frequencya
Orthographic
neighbours
Phonological
neighbours
Imageability
Effector
association
Mouth
Hand
Foot
Unrelated
Nonwords
4.76 (1.2)
4.56 (1.08)
4.6 (1.12)
4.6 (1.19)
4.6 (1.19)
1.2 (.41)
1.04 (.2)
1.2 (.41)
1.28 (.46)
1.16 (.37)
80.80
98.56
79.08
115.64
NA
6.0 (4.42)
6.0 (5.95)
6.0 (4.87)
7.08 (5.19)
NA
16.2 (8.845)
15.4 (9.08)
12.76 (8.3)
16.2 (10.42)
NA
4.1 (.58)
4.11 (.47)
3.94 (.67)
3.79 (.38)
NA
4.6 (.35)
4.48 (.29)
4.6 (.27)
0.0 (.0)
NA
(122.82)
(134.11)
(155.86)
(161.84)
Data are means with standard deviations in parentheses. NA: Not applicable.
a
CELEX lexical frequency per million.
body part was visible. There were also 10 control videos that depicted
a variety of frequently encountered natural and man-made stimuli
moving as they would in their natural environments for 5 s. No
humans or animals were depicted in these control videos.
Behavioural tasks
Lexical task
Participants completed the lexical task first to minimise the
involvement of motor imagery, followed by the video-based movement observation and execution localisation task in separate imaging
runs. In the lexical task, stimuli were presented in blocks of five items
from each of the six categories (hand, foot, mouth, and unrelated
words, nonwords and hashes) in pseudorandom order. A different
pseudorandom ordering of conditions was employed across participants. Each item was presented for 3 s such that each block lasted for
15 s. After the presentation of six blocks (one for each category), a
fixation cross was presented for 15 s. This sequence of six blocks
followed by fixation was repeated until all words had been presented
(i.e. 5 times). Participants silently read the words and when the
fixation cross or hashes were presented, watched the stimuli without
mentally reciting any words.
Action observation task
The video stimuli were presented for 10 s followed by either a
green or red dot (20 mm diameter) for 10 s, and then a blank screen for
5 s. Participants passively viewed the videos. A green dot always
followed action videos and a red dot always followed the control
videos. This sequence was repeated until all the 40 videos had been
presented. The order of presentation of the videos was randomised.
Action execution task
The green dot presented following an action video cued participants to replicate the movement of the effector in the video for 10 s
(using their right hand/foot or mouth; e.g., clench and release fist, curl
and release toes, move tongue from side to side). When the red dot
was presented they remained still.
Post scanning tasks
After scanning was completed, participants completed three postexperiment memory tasks where they were required to describe the
video stimuli to the experimenter, discriminate the 100 target words
from 20 other words (five hand, foot, mouth and unrelated) and
discriminate the 25 target nonwords from 25 other nonwords. These
memory tasks were included to ensure all participants attended to the
different word meanings and processed all words beyond mere visual
perception.
Image acquisition
Images were acquired using a 4 T Bruker MedSpec system. A
transverse electromagnetic (TEM) head coil was used for radiofrequency transmission and reception (Vaughan et al., 2002). T2
weighted gradient echoplanar images (EPI) were used to obtain blood
oxygen level dependent (BOLD; Ogawa et al., 1990) images during the
lexical and video tasks, with an echo time (TE) of 30 ms. During the
lexical task, 176 brain volumes were acquired, each volume consisting
of 36 planes, with an in-plane resolution of 3.60 × 3.60 mm and a slice
thickness of 3 mm (.6 mm gap), and a repetition time (TR) of 3 s.
During the video task, 405 brain volumes of identical resolution to
those of the lexical task were acquired, with a TR of 2.50 s. Geometric
distortions in the echo planar images caused by magnetic field
inhomogeneities at high-field were corrected on the scanner console
using a point-spread mapping approach (Zaitsev et al., 2003). The first
five volumes were ignored so tissue magnetization could reach a
steady state. Foam padding was used to limit head movement. A highresolution MP-RAGE 3D T1 image was acquired within the same
session, with an inversion recovery time (TI) of 700 ms, TR of 1500 ms,
echo TE of 3.35 ms and a resolution of .73 mm3.
Image analyses
The functional images from each participant were realigned using
rigid body motion correction and a mean image generated (Freire et al.
2002). This mean image was coregistered with the subject's MP-RAGE
3D T1 image, and the latter normalised to the standard T1 template
image in MNI atlas space using statistical parametric mapping
software (SPM5; Wellcome Department of Imaging Neuroscience,
Queen Square, London, UK). The resulting transformation to atlas
space was next applied to the functional timeseries from which the
mean had been generated, and the normalised volumes subsequently
resampled to 3 mm3 voxels and smoothed with an isotropic Gaussian
kernel (full width half maximum = 8 mm). Global signal effects were
estimated and removed using a voxel-level linear model (Macey et al.,
2004). A conservative decision was made to exclude the imaging data
from one participant whose T1-weighted structural image required
additional affine transformations to atlas space. The analyses were
conducted on the data from the remaining 17 participants.
Two sets of fixed effects analyses were conducted for each
participant's data within SPM5. The first involved regressors for the
four observation and three execution conditions of the video-based
task, while the second comprised regressors for the six categories of
stimuli in the lexical task. Blocks of stimuli were modelled with a
synthetic hemodynamic response function (HRF) according to their
respective durations. Serial correlations were modelled in the context
of the AR(1) model. Low frequency fluctuations were removed with a
128 s high pass filter. The main contrasts of interest for the videobased task involved comparing the movement observation and
execution conditions with the control observation condition and
fixation/baseline, respectively.
At the second level group random effects analysis, linear contrasts
of the parameter estimates were subjected to one-sample t-tests. As
we were primarily concerned with detecting somatotopic activation
within the boundaries of the left hemisphere primary motor and
premotor cortices, search volumes for these areas were constructed
from the maximum probability maps of area 4 (4a and 4p inclusive)
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N. Postle et al. / NeuroImage 43 (2008) 634–644
and area 6 of Eickhoff et al. (2006), respectively (Geyer, 2003).
Observation and execution related activation surviving a height
threshold of p b .001 and cluster threshold of N25 contiguous voxels
within these search volumes was then used to derive cluster-based
regions of interest (ROIs) for interrogating the activation elicited in the
lexical task. In order to avoid overlapping representations among
effectors in either the observation or execution conditions, contrasts
for each effector were exclusively masked (at p b .05, uncorrected)
with contrasts involving the other two effectors (see Tettamanti et al.
2005 for a similar approach). For example, the mouth N control
contrast was exclusively masked with both the hand N control and
foot N control contrasts. The mean percent BOLD signals for each of the
six lexical conditions were then extracted from each of the 12 action
cluster ROIs (i.e., 2 × motor areas × 3 effectors × 2 observation/execution
conditions) using Marsbar software (v0.41; http://marsbar.sourceforge.net). Activations were visualised using MRICron software
(http://www.sph.sc.edu/comd/rorden/mricron/).
We also performed a similar analysis to that of Tettamanti et al.
(2005) for the lexical task data alone using a height threshold of
p b .001 and cluster threshold of N25 contiguous voxels within areas 4
and 6. Contrasts for each effector related action word condition were
exclusively masked (at p b .05, uncorrected) with contrasts involving
the other two effector action word conditions. For example, the mouth
words N unrelated words contrast was exclusively masked with both
the hand words N unrelated words and foot words N unrelated words
contrasts. Finally, we conducted all analyses without masking to
identify observation and execution related activation across the
language dominant left hemisphere, and contrasted activation in the
lexical conditions with visual character strings, following Hauk et al.
(2004), using identical height and cluster thresholds.
conducting planned comparisons with repeated measures ANOVAs
followed by paired t-tests. The use of planned comparisons is justified
given the theoretical proposals for congruent effector specific
semantic and motor action representations (e.g., Gallese and Lakoff,
2005; Pulvermüller, 2005), and prior comparisons of this type in
neuroimaging studies (Aziz-Zadeh et al., 2006; Hauk et al., 2004;
Tettamanti et al., 2005).
BOLD signal responses for lexical stimuli in cytoarchitectonically and
functionally defined mouth, hand and foot action execution areas
Only two ROIs showed non-significant trends (p b .1) toward an
effect of lexical stimulus category within a cytoarchitectonically
defined motor area that showed effector specific activation for action
execution. This was the mouth ROI for both area 4 (F[5] = 2.02, p = .084)
and area 6 (F[5] = 1.93, p = .098). Otherwise, no significant effects were
found for any ROI interrogated (p N .05 for all). Fig. 2 (top) shows the
ROIs interrogated and the corresponding plots of BOLD signal
responses according to lexical category. Post hoc contrasts with paired
t-tests on responses extracted from mouth area 4 showed relatively
increased activation for mouth words versus hashes (t[1,16] = 2.47,
p b .05, two-tailed) and trends for mouth words having increased
activation compared to hand words (t[1,16] = 1.98, p = .065) and hand
words having reduced activation compared to unrelated words (t
[1,16] = −1.87, p = .079). A near identical pattern was revealed within
area 6 (mouth N hashes, t[1,16] = 2.17, p b .05; mouth N hand, t[1,16] =
2.22, p b .05; hand b unrelated, t[1,16] = −1.78, p = .094) (Fig. 2, bottom).
All other contrasts were non-significant.
BOLD signal responses for lexical stimuli in cytoarchitectonically and
functionally defined mouth, hand and foot action observation areas
Results
Cytoarchitectonically and functionally defined motor areas associated
with action execution and observation of specific effectors
The analyses of the action execution and observation conditions
revealed BOLD signal responses associated selectively with each
effector and organised in the expected ventral-to-dorsal manner
(mouth ventrally, followed by hand and then foot dorsally) for the
cytoarchitectonically defined areas 4 and 6. In addition, for both
execution and observation conditions, the activation associated with
each effector showed an expected posterior-to-anterior continuity
across the lateral surfaces of both areas 4 and 6. Peak maxima for each
effector according to execution and observation conditions are
provided in Table 3. There is good agreement between peaks detected
for action execution and observation according to each effector within
areas 4 and 6, consistent with the proposed operation of mirror
neurons.
Next, we examined mean BOLD signal responses associated with
processing of categories of lexical stimuli within the areas identified
for each effector in the action execution and observation conditions by
Table 3
Peak maxima for execution and observation of effector actions
Effector
Mouth
Hand
Foot
Combined
BA4 (primary motor cortex)
BA6 (premotor cortex)
Execution
Observation
Execution
Observation
−54, −9, 36
(6.18)
−39, −30, 60
(7.07)
−6, − 27, 63
(6.28)
−39, −12, 48
(4.51)
−54, − 9, 36
(4.46)
−33, −27, 63
(4.70)
−9, −42, 63
(5.44)
−33, −33, 51
(4.46)
−57, −3, 33
(5.58)
−36, −24, 63
(6.74)
−3, −12, 60
(6.51)
−9, 0, 60
(4.78)
−51, − 6, 51
(4.35)
−36, −27, 66
(4.52)
−9, − 9, −66
(4.99)
−6, 3, 54
(4.97)
Z-scores in parentheses.
Within the ROIs that showed effector specific activation associated
with action observation, we found a significant effect of lexical
stimulus category only in the foot observation ROI of area 6 (F[5] =
4.75, p b .001) and a trend toward an effect in the mouth ROI also in
area 6 (F[5] = 2.27, p = .055). Fig. 3 (area 4 at top and area 6 at bottom)
shows the ROIs interrogated and the corresponding plots of BOLD
signal responses according to category of lexical stimuli. Within the
foot ROI, post hoc contrasts with paired t-tests revealed that foot
words had increased BOLD signal relative to hand words (t[1,16] = 2.27,
p b .05), hashes (t[1,16] = 3.59, p b .01), unrelated words (t[1,16] = 2.70,
p b .05), and nonwords (t[1,16] = 3.56, p b .01), although not mouth
words (t[1,16] = 1.69, p = .11), while mouth words showed a trend
toward increasing signal compared to hashes (t[1,16] = 2.01, p = .061)
and nonwords (t[1,16] = 1.90, p = .075). Within the mouth ROI that
showed a non-significant trend, post hoc contrasts with paired t-tests
revealed that mouth words had increased BOLD signal relative to
hashes (t[1,16] = 2.39, p b .05). All other contrasts were non-significant.
BOLD signal responses for lexical stimuli in cytoarchitectonically and
functionally defined action execution and observation areas for
combined effectors
We next combined the effector execution conditions in order to
identify activity common to all effectors. The peak maxima for these
regions are summarised in Table 3. The peak response in area 6 was
located medially, corresponding to the boundary between the SMAproper and pre-SMA according to the meta-analytically derived
human motor area template (HMAT; Mayka et al., 2006) after
transformation from MNI to Talairach atlas coordinates (using mni2tal
conversion; http://imaging.mrc-cbu.cam.ac.uk/imaging/MniTalairach). We then used these generic action execution ROIs to interrogate
the lexical category stimuli, this time combining the effector related
action word conditions. This allowed us to examine whether the
general category of action words showed increased activity in motor
N. Postle et al. / NeuroImage 43 (2008) 634–644
639
Fig. 2. Axial slices depicting activity elicited by execution of mouth (green), hand (red) and foot (blue) actions in primary motor (BA4ap; top) and premotor (BA6; bottom) cortices, and
mean percent BOLD signal detected within these regions during presentation of the different categories of lexical stimuli. Error bars indicate SEM.
execution areas relative to other categories of lexical stimuli.
Repeated measures ANOVAs failed to reveal significant effects of
lexical category in area 4 (F[3] = 1.83, p N .05). However, a significant
effect was found in area 6 (F[3] = 6.52, p b .001). Post hoc contrasts
with paired t-tests on the responses in area 6 showed action words
had increased responses relative to hashes (t[1,16] = 3.68, p b .005) and
nonwords (t[1,16] = 3.27, p b .01), although not to unrelated words (t
[1,16] = 1.64, p N .05). Fig. 4 (top) shows the ROIs interrogated and plots
of BOLD signal responses.
A similar analysis was conducted for the effector observation
conditions in order to identify activity common to all effectors (Table
2). The peak response in area 6 was located medially in the pre-SMA
according to the HMAT (Mayka et al., 2006). These generic action
observation ROIs were used to interrogate the lexical category stimuli
(Fig. 4, bottom). Again, the effector related action word conditions
were combined to examine whether the overall category of action
words showed increased activity in general motor observation areas
relative to other categories of lexical stimuli. Repeated measures
ANOVAs failed to reveal significant effects of lexical category in area 4
(F[3] = 1.76, p N .05). However, a significant effect was found in area 6 (F
[3] = 9.17, p b .001). Fig. 4 (top and bottom) shows the ROIs interrogated
and plots of BOLD signal responses. Post hoc contrasts with paired
640
N. Postle et al. / NeuroImage 43 (2008) 634–644
Fig. 3. Axial slices depicting activity elicited by observation of mouth (green), hand (red) and foot (blue) actions in primary motor (BA4ap; top) and premotor (BA6; bottom) cortices,
and mean percent BOLD signal detected within these regions during presentation of the different categories of lexical stimuli. Error bars indicate SEM.
t-tests on the responses in area 6 showed action words had increased
responses relative to hashes (t[1,16] = 3.88, p b .001), unrelated words
(t[1,16] = 2.49, p b .05) and nonwords (t[1,16] = 3.95, p b .001).
BOLD signal responses for effector related action words in
cytoarchitectonically defined areas 4 and 6
This analysis failed to reveal any significant activity for the
comparisons of the individual effector related action words and
unrelated words in either area 4 or 6. We therefore combined the
effector related action word conditions to examine whether the
overall category of action words showed increased activity relative to
unrelated words. This analysis revealed a single cluster of significant
activity in the pre-SMA (peak x, y, z = 0, 12, 57; Z = 4.45), confirmed
with the HMAT (Mayka et al., 2006).
BOLD signal responses for action execution, action observation, and
lexical stimuli conditions outside cortical motor areas
Bold signal responses elicited across the language dominant left
hemisphere by the action execution, action observation, and lexical
stimuli conditions are presented in Supplementary material.
N. Postle et al. / NeuroImage 43 (2008) 634–644
641
Fig. 4. Coronal slices depicting activity elicited by execution (top) and observation (bottom) of combined mouth, hand and foot actions in primary motor (BA4ap; in red) and premotor
(BA6; in blue) cortices, and mean percent BOLD signal detected within these regions during presentation of the different categories of lexical stimuli. Error bars indicate SEM.
Post scanning test
Memory task
Of the 25 words within each semantic category, on average, each
participant correctly recognised 19.72 (SD = 4.00) of the hand-related,
19.83 (SD = 4.44) of the foot-related, 18.94 (SD = 4.68) of the mouthrelated, 19.17 (SD = 5.66) of the body part-unrelated and 14.33
(SD = 4.77) of the nonwords. Of the 10 videos within each category,
participants correctly recalled approximately 5.28 (SD = 1.78) of the
hand-related, 5.33 (SD = 1.57) of the foot-related, 6.39 (SD = 2.38) of the
mouth-related and 6.22 (SD = 1.93) of the control videos. ANOVAs
revealed that no one type of video stimuli was recalled substantially
more often than any other (p N .05), and the only significant difference
among lexical stimuli was that nonwords were recognised less often
than other types of target words (p b .05).
Discussion
This study is the first to assess whether action meaning
representations in the left hemisphere primary and premotor cortices
show a congruent somatotopic organisation in relation to both the
execution and observation of actions of specific effectors. In addition,
642
N. Postle et al. / NeuroImage 43 (2008) 634–644
it is the first to define these motor areas for interrogation according to
a combination of cytoarchitectonic and functional information, and to
include a lexical condition controlling for imagery that might be
elicited subsequent to the comprehension of word meanings. The use
of cytoarchitectonic maps ensured that we interrogated responses
solely within objectively defined primary and PM cortical areas,
excluding responses in areas of the surrounding frontal cortex
responsible for more cognitive functions. While not supportive of a
somatotopic mapping of action meaning representations, our results
are in agreement with findings from TMS and neuroimaging studies of
more general action word processing activating cortical areas within
the vicinity of the left precentral gyrus adjacent to the motor areas
(e.g., Canessa et al., 2008; Rüschemeyer et al., 2007; Vigliocco et al.,
2006; see Willems and Hagoort, 2007 for a review).
Primary motor and premotor cortical areas associated with execution
and observation of effector specific actions
The execution of simple movements with specific effectors resulted
in graded activation along the lateral surfaces of the primary and PM
cortices with an expected somatotopic organisation. Mouth representations were located ventrally, followed by hand and foot representations dorsally (Penfield and Welch, 1951; Woolsey et al., 1952). The
somatotopic organisation extended in a continuous fashion across the
lateral surface of area 4 into the caudal portion of area 6 (comprising
PMv and PMd). These results are consistent with a now large
neuroimaging literature in humans (e.g., Alkadhi et al., 2002; Ehrsson
et al., 2003; Stippich et al., 2007; Picard and Strick, 2001; Schubotz and
von Cramon, 2003). The observation of movements made with specific
effectors likewise resulted in activity organised in a somatotopic
fashion comparable to that associated with execution, with locations of
peak responses showing good accordance, thus providing evidence
similar to that cited in support of a proposed human mirror neuron
system (Buccino et al., 2004; see Turella et al., 2008).
Somatotopically organised action word meaning representations
We did not detect congruent activation for action words associated
with specific effectors in the somatotopically organised primary or PM
ROIs identified functionally by either execution or observation of
actions by those effectors. Nor were responses in effector specific areas
selective to action words, as they also showed responses to varying
levels of lexical information, especially unrelated imageable concrete
meanings and nonwords with regular phonology. The only effector ROI
to show a trend in the predicted direction was the PM foot observation
ROI. Of interest, this ROI was located in the pre-SMA/SMA where we
found increased activation for generic action words compared to other
classes of lexical stimuli (discussed below). It is possible that some foot
words were comprehended as whole body actions (e.g., walk, jump),
potentially contributing to this activation. Alternatively, as Pulvermüller et al. (2005) suggested, leg words might have a stronger reliance on
“semantic action-related features” compared to other effector words,
as leg actions tend to be more similar to each other (e.g., walk, run and
jog involve many of the same movements). However, within this ROI
foot action words did not show increased signal compared to mouth
words, and the latter words also showed trends (ps b .08) for increased
signal compared to other lexical stimuli.
A critical difference between the design of our study and that of
previous studies is the use of cytoarchitectural information. We used
probability maps derived from microcellular studies of post-mortem
brains, ensuring that we interrogated responses evoked solely in
primary and PM cortex (Eickhoff et al., 2006; Geyer, 2003). As we noted
in the Introduction, the peak maxima reported by previous studies for
overlapping action meaning representations did not accord well with
the cytoarchitectonic boundaries of the motor areas (see Fig. 1).
Moreover, there was little agreement across studies for peaks reported
for a given effector, especially foot-related words. In particular, the
peaks from the Hauk et al. (2004) study that used single word stimuli
did not accord well with the peaks from the studies that used sentence
stimuli (Aziz-Zadeh et al., 2006; Tettamanti et al., 2005). This lack of
consistency suggests that the activity reported by previous studies
might represent stimuli- or task-dependent factors.
In addition, we employed unrelated concrete words of equivalent
imageability as control stimuli, as they are known to activate left PM
cortex when compared with less imageable, abstract words (e.g.,
D'Esposito et al., 1997; Mellet et al., 1998; Pulvermüller and Hauk,
2006). Previous studies had compared effector action words with
abstract words or visual character strings, leaving open the possibility
that the activity they observed was due to differences in imagery
elicited between conditions (Aziz-Zadeh et al., 2006; Hauk et al.,
2004; Tettamanti et al., 2005). The absence of differential activity in
the present study indicates that this is likely to have been the case. We
also found that nonwords modulated activity in several of the PM
cortex action ROIs. Left PM cortex activity is a common finding during
nonword reading, and is often attributed to processes of orthography–
phonology conversion or covert articulation (see Dietz et al., 2005;
Mechelli et al., 2005; Snyder et al., 2007). Our data appear consistent
with the latter explanation, as the strongest responses for nonwords
were observed in the mouth PM cortex ROIs.
The pre-SMA and the representation of instructions for action
Given the absence of compelling evidence of a congruent motor
somatotopy for action word meaning representations, we next
identified action execution and observation ROIs within areas 4 and 6
that were common to all effectors, and assessed whether these areas
showed a selectivity for action word meaning representations in
general. The generic action execution and observation ROIs identified in
the PM cortex in this manner were both sensitive to the category of
lexical stimuli presented (action words N unrelated words N nonwords N
hashes), with the observation-related ROI showing the clearest
dissociation. The peaks of these ROIs were located within the medial
wall of the frontal cortex and, when converted to Talairach coordinates,
were either on or anterior to a perpendicular line crossing the ventral
anterior commissure used to delineate the pre-SMA rostrally and SMAproper caudally (the VCA line; Picard and Strick, 1996). The primary
motor cortex did not show a similar pattern of responses.
The pre-SMA is now viewed as having a cognitive–motor rather
than strictly motor role, due to its representations being relatively
effector-independent and its not being connected directly to the
primary motor cortex, unlike SMA-proper (Picard and Strick, 1996,
2001). It also has connections with prefrontal cortex, again differing
from SMA-proper (Johansen-Berg et al., 2004). As such, our observation of selectively increased activity in this region for the class of
action words does not appear consistent with explanations emphasising either Hebbian learning (e.g., Pulvermüller, 1996, 2005) or mirror
neuron related mechanisms (e.g., Rizzolatti and Craighero, 2004;
Tettamanti et al., 2005) framed in terms of actual motor programs. In
their meta-analysis, Grèzes and Decety (2001) noted that the pre-SMA
was activated primarily during action observation tasks with instructions to imitate. We used this same type of task in the present study. In
the monkey, some pre-SMA neurons represent relatively specific
instructions for action (Hoshi and Tanji, 2004). As the imperative form
of a verb serves as an instruction (e.g., “sit!”), the activation we
observed in the pre-SMA might therefore reflect a shared representation for an instruction cue.
According to this account, verbs serve as instruction cues by
enabling the retrieval of an appropriate motor program, i.e, they
represent information required for motor planning. An instruction to
imitate similarly requires subjects to retrieve an appropriate motor
program from visual information. They then execute the program after
a delay. If this account is accurate, one would expect greater activation
N. Postle et al. / NeuroImage 43 (2008) 634–644
associated with action word comprehension in the observation rather
than execution ROI, as we found. Given the activation we observed
was common to all effectors, such a representation would probably be
relatively abstract (e.g., a general instruction to perform an action). As
such, it might be considered compatible with a more general notion of
“embodied cognition”, i.e., one that does not assume a direct coupling
between action meaning comprehension and cortical motor areas
(e.g., Wilson, 2002). In addition, it does not preclude the possibility of
a modality-specific representation of action word meaning elsewhere
in association cortices (e.g., Hoenig et al., in press). Indeed, our wholebrain analyses indicated that the majority of the BOLD responses
elicited by retrieving action word meanings occurred in association
cortex adjacent to the motor areas (see Supplementary material).
Methodological considerations
The maps of somatotopic motor activation reported here were
elicited by execution and observation of simple, intransitive movements. Intransitive movements have been used frequently to
demonstrate somatotopy in terms of motor execution, observation
and imagery (e.g., Alkadhi et al., 2002; Ehrsson et al., 2003; Stippich et
al., 2007). While our results accord well with this previous research, it
is worth noting that the motor somatotopy reported for observation
and imagery of object-related movements does not always match that
reported for intransitive movements (e.g., Buccino et al., 2001;
Chouinard and Paus, 2006). As Pinker and Jackendoff (2005) point
out, activity during observation of object-related movements might be
more specific to the semantic goal of the action (i.e., manipulating the
object). Much of the research concerning observation of object-related
hand movements in humans has revealed activity within frontal
cortex along an assumed macrostructural border between PMv and
area 44/45 (Broca's area; see Rizzolatti and Craighero, 2004).
Additionally, the maps of motor somatotopic activation were
derived conservatively using an exclusive masking technique. That is,
pixels mutually activated by different effectors were excluded from
the ROIs. Previous fMRI studies investigating motor somatotopy have
employed similar statistical techniques to minimise the influence of
overlapping representations (e.g., Alkadhi et al., 2002; Ehrsson et al.,
2003; Stippich et al., 2007). Like Tettamanti et al. (2005), we used the
exclusive masking technique to identify activation associated with
effector specific action word meaning representations.
One major limitation of the present study and previous investigations that presented English language verbs in isolation (e.g., Hauk et
al., 2004; Pulvermüller et al., 2005) is that there is considerable verb–
noun homonymy in English (e.g., the word “walk” can denote both a
noun “the walk” and verb “to walk”). Therefore we cannot be certain
that the action word stimuli were read as verbs rather than nouns. The
implications of this are not entirely clear, as neuroimaging and TMS
studies have shown that while primary and PM cortex respond to
action word meanings, they are insensitive to manipulations of
grammatical class involving these words (e.g., Oliveri et al., 2004;
Vigliocco et al., 2006). Ambiguity is also inherent in the earlier studies
that used abstract sentence stimuli (Aziz-Zadeh et al., 2006;
Tettamanti et al., 2005). As Rüschemeyer et al. (2007) noted, these
studies confounded sentential objects with concrete or abstract
meanings according to the verb used (e.g., in the abstract sentence
“He grasped the idea”, idea is an abstract noun). Hence, the activation
observed could have been due to the action word meaning or object
noun meaning, or a combination of both.
Our choice of a block rather than an event related design for
presenting the lexical stimuli was based upon the superior efficiency
of the former in detecting BOLD responses (Bandettini and Cox, 2000;
Friston et al., 1999). Direct comparisons of block and event related
designs in word reading experiments have likewise shown the
expected advantage in terms of response amplitude for the former
(e.g., Chee et al., 2003). Recent neuroimaging studies of action word
643
meaning representation have likewise employed block designs (e.g.,
Vigliocco et al., 2006; single words), some with far fewer stimuli (e.g.,
only 5 sentences repeated eight times per condition; Aziz-Zadeh et al.,
2006; Tettamanti et al., 2005). Nevertheless, the use of a block design
could have been suboptimal for detecting early processes associated
with accessing word meaning. In order to address this issue, we reanalysed the fMRI data as an event related design following Mechelli
et al. (2003). The results were essentially the same, although with the
expected lower amplitude. However, we acknowledge that techniques
with superior temporal resolution to fMRI, such as event related
potentials (ERPs), are likely to be more sensitive to early processes
associated with accessing word meaning, particularly when used in
combination with fMRI (e.g., Hoenig et al., in press). Finally, as we used
fewer words per condition than Hauk et al. (2004), there is a
possibility that our results reflect a reduction in power relative to their
study. However, we think this explanation unlikely as other fMRI
studies have used either fewer (23; e.g., Rüschemeyer et al., 2007) or
the same number of words per condition to successfully image the
neural correlates of single word reading (25; e.g., Cohen et al., 2002). It
is also worth noting that the larger lists employed by Hauk et al.
(2004) contained words rated by their participants as belonging to
more than one category (see their Fig. 1b, p. 302).
Summary and conclusions
Although a number of recent theories of action word meaning
representation have assumed the involvement of a distributed
network of cortical somatosensory and motor areas, only a few have
proposed a tight coupling with motor somatotopy (e.g., Gallese and
Lakoff, 2005; Pulvermüller, 2005). There is considerable evidence
from TMS and neuroimaging studies of more general action word
processing activating association cortex within the vicinity of the left
precentral gyrus, and our results can be considered in agreement with
these findings (e.g., Canessa et al., 2008; Rüschemeyer et al., 2007;
Vigliocco et al., 2006; see Willems and Hagoort, 2007 for a review). As
others have noted, a finding of motor cortex activity during action
word comprehension does not prove definitively that semantic
representations are being accessed in these areas (Willems and
Hagoort, 2007). Even so, only this and a handful of other neuroimaging studies have explicitly examined the issue of a congruent motor
somatotopy of action meaning representations and, as we have argued
above, the evidence from these studies should be considered in
relation to a combination of cytoarchitectonic and functional criteria.
These criteria should include controlling for a range of potentially
confounding lexical variables, and in the case of a proposed mirror
neuron mechanism, include both action execution and observation
conditions to demonstrate overlapping activity (Turella et al., 2008). In
addition, a demonstration that lesions to discrete motor areas have
deleterious effects on the understanding of action words is required in
order to support the theory (Willems and Hagoort, 2007), and to date
the available lesion evidence is not supportive.
Appendix A. Supplementary data
Supplementary data associated with this article can be found, in
the online version, at doi:10.1016/j.neuroimage.2008.08.006.
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