Download Category-specific Conceptual Processing of

Cerebral Cortex August 2006;16:1193--1201
doi:10.1093/cercor/bhj060
Advance Access publication October 26, 2005
Category-specific Conceptual Processing of
Color and Form in Left Fronto-temporal
Cortex
To investigate the cortical basis of color and form concepts, we
examined event-related functional magnetic resonance imaging
(fMRI) responses to matched words related to abstract color and
form information. Silent word reading elicited activity in left
temporal and frontal cortex, where category-specific activity
differences were also observed. Whereas color words preferentially activated anterior parahippocampal gyrus, form words evoked
category-specific activity in fusiform and middle temporal gyrus as
well as premotor and dorsolateral prefrontal areas in inferior and
middle frontal gyri. These results demonstrate that word meanings
and concepts are not processed by a unique cortical area, but by
different sets of areas, each of which may contribute differentially
to conceptual semantic processing. We hypothesize that the
anterior parahippocampal activation to color words indexes
computation of the visual feature conjunctions and disjunctions
necessary for classifying visual stimuli under a color concept. The
predominant premotor and prefrontal activation to form words
suggests action-related information processing and may reflect the
involvement of neuronal elements responding in an either-or fashion
to mirror neurons related to adumbrating shapes.
Keywords: abstract concepts, fMRI, language, prefrontal cortex, reading
Introduction
A great challenge in cognitive neuroscience is to define the
cortical areas engaged in processing semantic meaning of words
and concepts. Many researchers agree that temporal cortex
provides a unique substrate for semantic binding. Definitions of
relevant areas within the temporal lobe range from temporal pole
(Hodges, 2001; Rogers et al., 2004) to anterior superior temporal
gyrus (Scott and Johnsrude, 2003), posterior inferior temporal
areas (Price et al., 2001) and posterior superior temporal sulcus
(Hickok and Poeppel, 2000). Activation in temporal cortex,
including posterior fusiform and parahippocampal gyri, was
found to be specific to categories of knowledge (Chao et al.,
1999; O’Craven and Kanwisher, 2000), suggesting that areas
of temporal cortex may contribute differentially to semantic
category processing.
A different line of research emphasizes the relevance of
frontal cortex, especially premotor and inferior frontal cortex,
for meaning processing (Posner and Pavese, 1998; Rizzolatti
et al., 2001). Mirror neurons that bind information about actions
and their corresponding perceptual patterns have been discovered in inferior premotor cortex of monkeys and apparently
contribute to action-related cognitive processes, including
observation or imagination of actions in humans (Jeannerod
and Frak, 1999; Buccino et al., 2001). Processing action verbs
and tool words with semantic relationship to actions was found
to elicit stronger fronto-central cortical activation than object
The Author 2005. Published by Oxford University Press. All rights reserved.
For permissions, please e-mail: [email protected]
Friedemann Pulvermüller and Olaf Hauk
Medical Research Council, Cognition and Brain Sciences Unit,
Cambridge CB2 2EF, UK
words (Preissl et al., 1995; Martin et al., 1996; Pulvermüller et al.,
1999). Among the action words, those related to movements of
the face, arm or leg activated fronto-central cortex in a somatotopic fashion (Hauk et al., 2004; Shtyrov et al., 2004), consistent
with the claim that sensorimotor cortex processes actionrelated aspects of word meaning (Pulvermüller, 2001, 2005).
These results can be explained by the so-called sensorimotor
theory of conceptual and semantic processing: sensory and
action-related semantic features are attached to a symbol by
correlation, typically when a child perceives words in the
context of specific objects and actions (Wernicke, 1874; Freud,
1891; Warrington and Shallice, 1984; Shallice, 1988; Humphreys
and Forde, 2001; Kiefer and Spitzer, 2001). Because perceptions
through different senses and actions are processed by different
areas of cortex, this explains a dissociation into categories of
knowledge, for example visually related and motor categories
(Warrington and Shallice, 1984), and even fine-grained semantic categories, such as face-, arm- and leg-action words
(Pulvermüller, 2001, 2005). Although the sensorimotor theory
explains a range of neuropsychological dissociations in patients
with disease of the brain (Humphreys and Forde, 2001) and
a multitude of facts revealed by neuroimaging experiments
(Pulvermüller, 1999; Martin and Chao, 2001), it has systematic
difficulty explaining abstract knowledge (Grossman et al., 2002;
Jackendoff, 2002). Words such as ‘rhomb’, ‘hope’ and ‘nevertheless’ do not refer to objects in the world but have abstract
meaning, and the brain areas where such abstract knowledge is
stored are still largely unknown.
Neuroimaging work comparing symbols with abstract and
concrete meaning has shed light on the issue, but could not
determine an area, or set of areas, consistently activated by
abstract meaning processing. Some results suggested differential laterality: highly abstract grammatical function words such
as ‘it’ and ‘the’ led to pronounced left-lateralized neurophysiological activity, which contrasted with the more bilateral
responses to concrete nouns and verbs (Neville et al., 1992;
Pulvermüller et al., 1995). Also, more strongly left-lateralized
brain responses to abstract nouns compared with concrete
nouns were revealed by event-related potential (ERP) experiments (Kounios and Holcomb, 1994). However, a general
difference in laterality related to abstractness could not be
confirmed (Friederici et al., 2000). Recent imaging work using
functional magnetic resonance imaging (fMRI) indicated lefthemispheric correlates of abstract semantics in Broca’s area
(Fiebach and Friederici, 2004), angular gyrus (Skosnik et al.,
2002), superior (Wise et al., 2000) and posterior temporal
cortex (Grossman et al., 2002), or a widespread set of areas
including temporal pole along with inferior temporal and
inferior frontal cortex (Noppeney and Price, 2004). In contrast
with previous findings of a predominantly left-hemispheric
locus of abstract semantics, a few studies also reported stronger
activation for abstract words relative to concrete words in
different areas of the right non-dominant hemisphere (Kiehl
et al., 1999; Perani et al., 1999; Grossman et al., 2002). However,
consistent with the differential laterality hypothesis, a recent
study by Binder and colleagues reported that concrete word
identification led to activation of distributed sources in both
hemispheres, whereas abstract words activated a left frontal
region including areas in the inferior and middle frontal gyri and
lateral premotor cortex (Binder et al., 2005).
This variability of results may be due, in part, to the fact that in
all earlier studies, widely defined categories of abstract and
concrete words were compared with each other. Since the brain
basis of concrete action and object meaning can vary substantially,
it is reasonable to assume similar local specificity for abstract
concepts as well. Crucially, the cognitive abstraction processes
necessary for understanding grammatical function words, such as
‘it’ or ‘nevertheless’, are fundamentally different from those
related to emotionally related words, such as ‘hope’, which are,
in turn, different from those triggered by words referring to visual
shapes, such as ‘rhomb’. Thus, the cognitive processes of
abstraction differ between subtypes of abstract words, and so
may the loci of their cortical processing. To elucidate processes of
abstraction, it may therefore be useful to focus on subtypes of
words with specific abstract semantic features.
Here, we investigated items that still have links to action and
object features, but abstract away from concrete entities by
referring to form or color features many objects have in
common. We looked at words semantically related to color
and form, whose meaning is at an intermediate level on the
continuum between highly concrete, imageable, object-related
words and highly abstract words. According to the MRC
Psycholinguistic Database (Coltheart, 1981; Wilson, 1988),
concreteness ratings for highly concrete words are >600 (e.g.
‘mouse’, 624; ‘eye’, 634), whereas highly abstract words are
rated as <400 (‘love’, 311; ‘plan’, 357). Our stimuli were in the
intermediate range (between 400 and 600: ‘blonde’, 502; ‘curve’,
447). As our stimuli were carefully matched for important
properties, including physical features, visual imageability,
familiarity, abstractness and a range of psycholinguistic variables, a unitary semantic system approach would predict
congruent activation of this system for both word categories.
A version of the sensorimotor theory, however, may predict
differential activation of frontal and temporal circuits as
a function of the action- and object-relatedness of the semantics
of the stimulus words.
Whereas a concrete word, e.g. ‘door’ directly relates to its
reference object, a form or color word, e.g. ‘rectangle’, refers to
a feature of most of its reference objects that needs to be
separated and extracted from other object features. This visual
feature extraction process can be computed by neurons in the
vicinity of the areas engaged in object processing. Elementary
color features of visual stimuli are processed already in primary
visual cortex (Hubel, 1995) and temporo-occipital areas have
been found to preferentially respond to color processing
(McKeefry and Zeki, 1997). To compute a color concept —
which covers a range of possible colors, with different levels of
brightness and saturation — several alternative feature conjunctions must be classified together, possibly by neural units at
higher levels located at gradually more anterior cortical sites.
Neural correlates of color concept processing may therefore be
1194 Category-specific Conceptual Processing of Color and Form
d
Pulvermüller and Hauk
present in the temporal lobe, anterior to the temporo-occipital
and fusiform areas preferentially activated during color perception (Martin et al., 1995). In animal research, neurons in anterior
peri- and entorhinal areas have been proposed to compute
increasingly complex conjunctions and disjunctions of features
represented by neurons in inferior temporal lobe and closer to
the visual input (Bussey and Saksida, 2002; Bussey et al., 2002;
Tyler et al., 2004). In the same way, concrete objects can be
classified as exhibiting the same shape (e.g. rhomb shape).
Establishing a form/shape concept necessitates computation of
disjunctions over large sets of concrete objects and elementary
visual feature. Again, the neural substrate of progressively
abstract computations may be in primary visual (elementary
visual features: Hubel, 1995), lateral occipital (object shapes:
Kourtzi and Kanwisher, 2001) and inferior and medial temporal
cortex. However, in contrast to color concepts, shape concepts
always have a motor correspondence, since shapes, but not
colors, can be outlined or adumbrated by specific sequences of
body movements. Also, when looking at a shape, eye movements
follow the shape contour. Because the form of objects can be
outlined with different body parts, the brain basis of abstract
form concepts may comprise sensorimotor, especially premotor
cortex, where action representations are still somatotopic
(Rizzolatti et al., 2001), but also neurons in prefrontal cortex
related to motor planning (Fuster et al., 2000). Prefrontal cortex
just anterior to premotor cortex would be ideally placed for
computing conjunctions and disjunctions over sets of specific
action programs and could therefore provide a neural substrate
for action aspects of abstract form.
Here, we set out to investigate the brain basis of words related
to abstract color and form concepts (e.g. ‘brown’, ‘blonde’ and
‘bronze’ versus ‘rhomb’, ‘square’, ‘arc’). Word groups matched
for physical features, visual imageability, familiarity, abstractness
and a range of psycholinguistic variables were presented in
a passive reading task while event-related blood-flow changes
were measured. We hypothesized that the color- and formrelated meaning of these words is reflected by category-specific
activation in temporal lobe, and that form-related words
specifically activate premotor and prefrontal cortex.
Materials and Methods
Imaging Methods
Fourteen monolingual, right-handed, healthy native English speakers
participated in the study. Their mean age was 25 years (SD 5). Subjects
were scanned in a 3 T Bruker MR system using a head coil. Echo planar
imaging (EPI) sequence parameters were TR = 3.02 s, TE = 115 ms, flip
angle = 90. The functional images consisted of 21 slices covering the
whole brain (slice thickness 4 mm, inter-slice distance 1 mm, in-plane
resolution 1.6 3 1.6 mm, FOV 20 cm, matrix size 21 3 128 3 128).
Imaging data were processed using SPM99 software (Wellcome Department of Cognitive Neurology, London).
Images were corrected for slice timing, and then realigned to the first
image using sinc interpolation. Phase-maps were used to correct for
inaccuracies resulting from inhomogeneities in the magnetic field
(Jezzard and Balaban, 1995; Cusack et al., 2003). Any non-brain parts
were removed from the T1-weighted structural images using a surface
model approach (‘skull-stripping’) (Smith, 2002). The EPI images were
co-registered to these skull-stripped structural T1-images using a mutual
information co-registration procedure (Maes et al., 1997). The structural MRI was normalized to the 152 subject T1 template of the Montreal
Neurological Institute (MNI). The resulting transformation parameters
were applied to the co-registered EPI images. During the spatial
normalization process, images were resampled with a spatial resolution
Figure 1. Cortical activation during passive reading of concrete words semantically related to visual information (P = 0.001, uncorrected). A lateral view is shown on the upper left
and frontal slices of an average brain are displayed from top left to bottom right. The diagram at the bottom left gives semantic ratings (and their standard errors) for color and form
words; ratings of semantic relatedness to general visual information, form information and color information are given (see Materials and Methods).
of 2 3 2 3 2 mm3. Finally, all normalized images were spatially smoothed
with a 12 mm full-width half-maximum Gaussian kernel, globally
normalized, and single-subject statistical contrasts were computed
using the general linear model (Friston et al., 1998). Low-frequency
noise was removed with a high-pass filter with time constant 60 s. Group
data were analyzed with a random-effects analysis. A brain locus was
considered to be activated in a particular condition if 20 or more
adjacent voxels all passed the threshold of P = 0.001 (uncorrected). In
some cases, correction for multiple comparisons in the left hemisphere
was administered using the False Discovery Rate correction approach
(P < 0.05) (Genovese et al., 2002). Stereotaxic coordinates for voxels
with maximal z-values within activation clusters are reported in Talairach
space (Talairach and Tournoux, 1988).
Clusters in the left language-dominant hemisphere, which were found
to be active in the random-effects analysis of the contrast words versus
matched hash mark stings (Fig. 1), were used to define three ‘canonical’
regions of interest (ROIs), in inferior frontal (IF), fusiform (FUS) and
parahippocampal gyrus (PH) respectively (see Table 1). Additional
‘supplementary’ ROIs were defined on the basis of earlier findings.
Since previous research found an area in the middle temporal gyrus
whose activation related to semantic and lexical processing (Chao et al.,
1999; Devlin et al., 2004), a middle temporal gyrus (MT) ROI was
selected (3 3 3 3 3 voxels centered at –60/–40/0). Because a large
proportion of precentral gyrus was activated by action words in an
earlier study (Hauk et al., 2004) and recent work indicated involvement
of premotor cortex in abstract word processing (Binder et al., 2005),
possible involvement of premotor cortex dorsal to the inferior frontal
language area was probed (–45/0/35). As abstract action concept
processing was predicted in dorsolateral prefrontal cortex and earlier
work confirmed involvement of the middle frontal gyrus in abstract
concept processing (Binder et al., 2005), an additional ROI was placed
in a dorsolateral prefrontal area and anterior to premotor cortex (–50/
25/25). Previous research has documented activation of this region in
a range of tasks tapping into typical prefrontal functions, as for example,
abstract mappings between stimuli and responses (Duncan and Owen,
Table 1
Areas activated by words relative to strings of hash marks of the same length
Brain region
Talairach x, y, z
All words
Fusiform gyrus, BA 20
Fusiform gyrus
Inferior frontal gyrus, BA 45
Parahippocampal gyrus
LH
LH
LH
LH
ÿ36 ÿ38 ÿ18
ÿ42 ÿ47 ÿ13
ÿ46
28
10
ÿ28 ÿ12 ÿ15
T(13)
5.54
4.64
4.91
4.69
Talairach coordinates along with t-values are given for the maximally activated voxel in each local
cluster. All clusters that passed the significance threshold at P \ 0.001 are listed. The FDR
correction cutoff was at T 5 3.8.
2000). For each subject and each of the six ROIs, average parameter
estimates over voxels were calculated. These values were subjected to
ANOVAs including the factors Region of Interest and Word Category
(color and form). An additional ANOVA was carried out separately on
data from canonical ROIs only. Paired two-tailed t-tests were used as
planned comparison tests for between condition differences in individual ROIs. The mean values scaled to HRF-peak percentage signal
change relative to the mean over all voxels and scans within the
corresponding ROI and standard errors over subjects are shown in
Figure 2.
Stimuli and Experimental Design
Words semantically related to visual information, 50 color- and 50 formrelated items, were selected using established procedures (Pulvermüller
et al., 1999). Stimulus groups were matched for word length counted in
letters and syllables (4.3 versus 4.1 letters, all monosyllabic), standardized lexical frequency (27.9 versus 30.9 occurrences/million words:
Francis and Kucera, 1982) (also matched according to Baayen et al.,
1993), imageability and concreteness/abstractness [mean concreteness
ratings (SE): 533 (9.2) versus 522 (8.6): Coltheart, 1981; Wilson, 1988].
Cerebral Cortex August 2006, V 16 N 8 1195
Figure 2. (Top right) Cortical activation during passive reading of color (in green) and form-related words (red). (Center) Frontal slices of the MNI average brain showing regions
where specific activation was seen during reading of color (green/blue/purple) or form (red/orange/yellow) words. (Bottom left) Effect sizes for color and form words in the six ROIs
in the left hemisphere (rescaled to HRF peak percentage signal change relative to the mean over all voxels and scans within the corresponding ROI): IF, inferior frontal gyrus; PF,
dorsolateral prefrontal cortex; PM, dorsolateral premotor cortex; PH, parahippocampal gyrus; MT, middle temporal gyrus; FUS, fusiform gyrus. The little brain at the bottom right
gives the approximate locations of the six ROIs.
Stimulus word groups were also matched for their semantic relationship
to objects that can be visually perceived, but from which they differed in
terms of their semantic relatedness to shape and color, as assessed in
a rating study (Fig. 1, bottom). Subjects were asked whether they
considered the word as being semantically related to (i) an object that
can be perceived visually, (ii) a visual shape or form and (iii) a color.
Ratings were given on a scale from 1 to 7, following procedures
described in an earlier publication (Hauk and Pulvermüller, 2004). One
hundred and fifty filler words and 50 pseudo-words were added in order
to avoid focussing the subjects’ attention on specific aspects of the
stimuli. The filler words included the face- and arm-related words used
in the study by Hauk and colleagues (Hauk, 2004). Stimuli employed
during 150 baseline trials consisted of strings of meaningless hash marks
varying in length and matched to the word stimuli in length. In addition,
50 null events were included during which a fixation cross remained
was displayed. Stimuli were presented for 100 ms, and the stimulus
onset asynchrony (SOA) between two stimuli was 2.5 s, so that stimulus
presentation and scanner trigger were out of phase by ~500 ms. Two
pseudo-randomized stimulus sequences were alternated between subjects. For statistical analysis, the SPM99 canonical haemodynamic
response function (HRF) was used to model the activation time course.
Results
Words activated an area in the left fusiform gyrus in the inferior
temporal lobe (activation peaks at –36/–38/–24 and –42/–47/
–13) close to and overlapping with the site labeled the visual
word form area (VWFA, –42/–57/–15: McCandliss et al., 2003).
In addition, an area of inferior frontal cortex comprising the
posterior part of Broca’s area, Brodmann’s area 44, and its
anterior section, Brodmann area 45, became active (activation
1196 Category-specific Conceptual Processing of Color and Form
d
Pulvermüller and Hauk
Table 2
Areas activated by words associated with color and form information
Brain region
Talairach x, y, z
T(13)
Color words
Parahippocampal gyrus
Cerebellum
Fusiform gyrus, BA 20
LH ÿ30 ÿ14 ÿ20
LH ÿ36 ÿ40 ÿ24
LH ÿ44 ÿ48 ÿ20
5.60
4.38
3.98
Form words
Fusiform gyrus, BA 20
Middle temporal gyrus, BA 19/39
Middle temporal gyrus, BA 21
Inferior frontal gyrus, BA 47
Precentral gyrus, BA 6
Middle frontal gyrus, BA 46
Middle and inferior frontal gyrus, BA 9
Precentral gyrus, BA 4
Lentiform Nucleus, Putamen
LH
LH
LH
LH
LH
LH
LH
RH
LH
ÿ38
ÿ38
ÿ57
ÿ34
ÿ49
ÿ46
ÿ53
36
ÿ20
ÿ36 ÿ18
ÿ63
18
ÿ43
4
17 ÿ2
0
35
26
19
13
29
ÿ26
55
10
7
6.21
4.88
4.28
7.03
6.29
5.85
4.91
5.38
4.73
Talairach coordinates along with t-values are given for the maximally activated voxel in each local
cluster. All clusters that passed the significance threshold at P \ 0.001 are listed. The FDR
correction cutoff was at T 5 4.3.
peaks at –52/10/20 and –46/28/12). The activation of the VWFA
together with inferior frontal areas during passive reading of
single words is consistent with earlier findings (e.g. Dehaene
et al., 2002; Hauk et al., 2004). There was an additional
activation focus in anterior parahippocampal gyrus (–28/–12/
–18; see Fig. 1, Table 1). No significant activation was seen in the
right hemisphere.
Comparison of color and form words showed that both word
categories activated the inferior temporal VWFA. This activation
was more pronounced for form than for color words. Closer
examination indicated that posterior parts of the activated
fusiform area was most responsive to color words, whereas
anterior fusiform activation was strongest for form words
(–44/–48/–20 versus –38/–36/–18; see Table 2 and Fig. 2).
The parahippocampal area was significantly activated by color
words, but not by form words. Additional areas in middle
temporal gyrus were activated specifically by form words.
The most robust and widespread activation elicited by form
words was found in left frontal cortex. Significant activation
peaks were present in premotor cortex (BA 6, –50/–2/38),
inferior prefrontal cortex (BA 45 and 47, –34/18/–2) and
dorsolateral prefrontal cortex (BA 9 and 46, –54/12/32 and
–46/26/19).
To demonstrate that stimulus types activate specific brain
regions to different degrees, it is necessary to directly compare
the activity patterns they elicit in predefined ROIs. A repeated
measures two-way ANOVA was therefore performed to assess
significance of word-category-specific activation in the three
canonical ROIs defined on the basis of the words versus hash
marks contrast. This revealed a significant interaction of the
factors Word Category and Region of Interest [F (2,26) = 9.11,
P < 0.001]. Analysis of all six ROIs (fusiform, parahippocampal,
middle-temporal, premotor, inferior-frontal and dorsolateral
prefrontal areas) confirmed the critical interaction of the factor
Word Category with Region of Interest [F (5,65) = 3.16, P <
0.01]. There was also a significant main effect of the factor Word
Category [F (1,13) = 6.22, P < 0.02], suggesting stronger
activation to form words than to color words. For the three
canonical ROIs, planned comparison tests revealed stronger
activation to form than color words in inferior frontal and
fusiform gyri and the reverse, stronger activation to color than
form words, in parahippocampal gyrus (F-values > 4.5, P-values
< 0.05). Planned comparison tests performed for the three
‘supplementary’ ROIs revealed significant between-category
differences in middle-temporal and prefrontal cortex (F > 4.5,
P < 0.05), but not in the premotor region (P = 0.15, NS). In
summary, these results show that five of the six ROIs were activated differentially by the word categories under investigation.
Discussion
Using event-related fMRI while subjects performed a passive
reading task, we observed inferior temporal and inferior frontal
activation of the left dominant hemisphere to words semantically related to form and color information. Critically, color and
form words elicited category-specific cortical activation differences in focal areas of frontal and temporal cortex. Parahippocampal areas were more strongly activated by color
words than by form words, and stronger activity to form words
than to color words was seen in fusiform gyrus, middle temporal
gyrus and prefrontal cortex in the inferior and middle frontal
gyri. These results provide further evidence that words from
different semantic categories —color and form words in the
present work— can activate cortical areas to different degrees,
possibly revealing the cortical topographies of their categoryspecific distributed semantic memory networks or cell assemblies. These findings are in line with previous neuropsychological
evidence suggesting that dissociable brain systems contribute
to conceptual processing of color and form information (Zeki
et al., 1999; Miceli et al., 2001).
General Word-related Activation
Passive reading of all word stimuli grouped together led to
enhanced blood flow in the left temporal lobe, in fusiform
cortex, anterior to an area previously related to the processing
of prelexical word-related or letter string information (Cohen
et al., 2000; Dehaene et al., 2002). Because the stimulus words
under study were highly imageable and semantically related to
objects known through the visual channel, the present data are
also open to the interpretation that word-evoked fusiform
activation indicates semantic processing (Price, 2000; Price
and Devlin, 2003). In this context, it is noteworthy that the
fusiform activation maximum elicited by color words was
posterior to that elicited by form words, and that fusiform
activation was generally stronger for form words than for color
words. This argues in favor of a semantic origin of the present
fusiform activation, i.e. a specialization of subareas of fusiform
gyrus in the conceptual processing of color and/or form
information. Apart from temporal cortex, left-inferior frontal
cortex, including Broca’s area, was also generally activated by all
word forms. This confirms earlier reports on a general role of
this brain region in word processing (Price et al., 1996; Binder
et al., 1997; Pulvermüller et al., 2003; Wilson et al., 2004). The
inferior-frontal neurons included in word-related neuronal
ensembles would thus be activated not only during speech
but during language comprehension as well (Pulvermüller and
Preissl, 1991). The role of these inferior frontal neurons may
be analogous to that of mirror neurons with a role in action
control but also responding to perceptual aspects of actions
(Gallese et al., 1996; Iacoboni et al., 1999; Rizzolatti et al., 2001;
Kohler et al., 2002), in this case acoustic signals uniquely
identifying lexical elements (Fadiga et al., 2002). However, we
cannot decide on the basis of the present neuroimaging data
whether the inferior frontal activation is due to mirror neurons
or to canonical multimodal neurons that do not respond
specifically to actions, but rather to objects involved in actions
(Rizzolatti and Craighero, 2004). The left-hemispheric parahippocampal activation not generally seen for words could
tentatively be attributed to the abstract meaning aspects of the
stimulus words (but see Discussion below).
Category-specific Semantic Activation
Category-specific activation was reported in a variety of earlier
studies (e.g. Dehaene, 1995; Martin et al., 1995, 1996). However,
as argued previously (for review, see Pulvermüller, 1999), much
earlier work did not control for important physical, psychological and psycholinguistic stimulus features, therefore making it
difficult to draw inferences on a semantic origin of the observed
effects. Although category-specific brain activation was not
always observed when these factors were empirically assessed
and controlled for (Devlin et al., 2002), a number of studies
confirmed differences between the brain activation patterns
elicited by words from different semantic categories. Differences were found between widely defined and increasingly
specific categories, ranging from content and function words,
nouns and verbs, animal and tool names, to action word
subtypes with different meaning (e.g. Brown and Lehmann,
1979; Preissl et al., 1995; Pulvermüller et al., 1995, 2005; Cappa
et al., 1998; Koenig et al., 1998; Chao et al., 1999; Kiefer, 2001;
Hauk et al., 2004; Devlin et al., 2005). The present study
provided particularly extensive stimulus control and matching of word categories for variables including word length,
Cerebral Cortex August 2006, V 16 N 8 1197
standardized lexical frequency, familiarity, abstractness, imageability and the degree to which the words were semantically
related to visually perceivable objects. On the other hand,
empirical evidence was gathered that stimulus groups differed
significantly on semantic scales of color- and form-relatedness
(Fig. 1), a difference at the cognitive level that was reflected by
differential activations of a range of cortical areas. The differential activation to color and form words in different sets of
regions of interest argues in favor of an interpretation in terms
of semantic and conceptual information linked to the word
stimuli at an abstract level.
Specific Activation in Temporal Lobe
Our results provide evidence that cortical areas differentially
contribute to the semantics of color and form words and
therefore support established theories of category-specific semantic processes in human cortex (Warrington and McCarthy,
1983; Shallice, 1988). Information about color and form is
mainly extracted from the visual input and therefore cortical
processing differences were expected in the inferior-temporal
ventral stream of visual processing. The observed category
differences in fusiform gyrus and middle temporal gyrus are
consistent with previous imaging work and neuropsychological
studies revealing distinct inferior temporal systems preferentially engaging in color and form processing (e.g. Martin et al.,
1995; Martin and Chao, 2001; McClelland and Rogers, 2003). An
explanation in terms of different inferior temporal neural
systems specialized for color and form information can account
for the differential activation of fusiform gyrus, in particular the
12 mm distance between form and color word maxima. The
specific activation of parahippocampal cortex to color words is
consistent with results of recent studies of fine-grained neuropsychological deficits in processing color-knowledge related to
objects, suggesting that ‘the mesial temporal stuctures are
specifically involved in representing or accessing object color
knowledge’ (Miceli et al., 2001).
As color and form words differentially activated areas in
parahippocampal, fusiform and middle temporal gyrus, it might
be possible to relate these differences to aspects of the meaning
of these stimuli. Parahippocampal activation specific to color
words can tentatively be explained by the visual feature
conjunction model (Bussey and Saksida, 2002; Bussey et al.,
2002): to classify visual information under a concept, such as
a color, logical operations including ‘and’ and ‘either-or’
computations need to be performed by neural elements over
a range of input patterns. It is well known that this requires
additional sets of neural elements operating on the input
(Kleene, 1956; Minsky and Papert, 1969; McClelland and
Rumelhart, 1985), which in the inferior visual stream must be
located progressively anterior to visual cortex. It is possible that
feature conjunctions and disjunctions for color concepts, e.g.
binding the different tones and luminances covered by a given
color concept, are computed by parahippocampal neurons
receiving input from posterior color-related inferior temporal
areas. This is consistent with the idea that aspects of color
concepts linked to words are processed by anterior temporal
sites, thereby supporting the posterior--anterior model of visual
feature abstraction (Bussey and Saksida, 2002; Bussey et al.,
2002; Tyler et al., 2004). However, as form words did not
activate parahippocampal cortex although their meaning, similarly to color words, is abstract and independent of any specific
object (feature conjunctions and disjunctions), it appears that
other areas in temporal cortex can contribute to conjunctive
processing too. For form words, the fusiform and middle
temporal cortices are relevant here and the suggestion may
therefore be that there are different streams in temporal lobe
that can play a category-specific role in feature conjunction or
disjunction processing.
Specific Activation in Frontal Lobe
All words under study were strongly related to visually defined
perceptual information, but lacked any obvious action meaning,
as, for example, tool names and action verbs usually do.
Established theories of category-specificity would therefore
predict activity differences between color and form words
related to visual information processing in temporal lobe, but
not in frontal cortex. The specific inferior frontal and middle
frontal activation to form words can be tentatively accounted
for as follows. An action relationship of form words is evident
from the fact that a shape or form can always be outlined or
adumbrated by a specific set of body movements. Premotor
activation seen for form words may therefore be related to
implicit action aspects of the meaning of form words. However,
there is a clear difference between the action relatedness of
a concrete action word, e.g. ‘kick’, and an abstract form word,
e.g. ‘rhomb’. The former relates to a defined body part whereas
Figure 3. Lateral view of the brain with activation maps for abstract form/shape words (in red) contrasted with the areas activated by concrete action words related to specific
body parts (face in blue, arm in green; diagram on the left) and actions performed with these body parts (diagram on the right) (cutoffs: P < 0.001, uncorrected, for words,
P < 0.05, FDR-corrected, for actions). Note that form words elicited prefrontal activation in the first and second frontal gyrus not evoked by concrete action words or actions (yellow
circle). All word activations overlapped in the left inferior frontal cortex (white area, diagram on the left) but actions and abstract word processing did not elicit overlapping activation
patterns (right diagram).
1198 Category-specific Conceptual Processing of Color and Form
d
Pulvermüller and Hauk
the latter refers to a shape that can be adumbrated using the
hand or finger, but equally well by a head movement or a series
of saccades. The form-related action concept should therefore
include information that abstracts away the body part information but leaves open the alternatives of using different body
parts for perceptually related actions, which we could expect in
prefrontal cortex adjacent to premotor areas.
To directly test this prediction, an experiment on action
words related to different body parts (face-, arm- and leg-related
action words, such as ‘lick’, ‘pick’ and ‘kick’, see Hauk et al.,
2004) was done with the participants in the color-/form-word
study (see Materials and Methods). Consistent with the earlier
findings, face- and arm-words produced somatotopic activation
in motor and premotor cortex, which partly overlapped with
activation during movements of corresponding body parts. The
left inferior-frontal activation to form words overlapped with
action word activation (Fig. 3, diagram on the left), but no clear
overlap was seen between word activation and the precentral
activation observed during simple body movements (diagram on
the right). Crucially, frontal activation elicited by form words
was not restricted to premotor areas (as for concrete action
words), but extended into prefrontal cortex in both inferior and
middle frontal gyri including Brodmann areas 9 and 46. These
areas are anterior to premotor cortex and therefore ideally
located for controlling premotor activity. We suggest that the
dorso-lateral prefrontal activation specific to form words relates
to the activation of neural networks computing conjunctions
and disjunctions on concrete action patterns therefore specifying action concepts at an abstract level. The activation of a left
inferior frontal area, including middle frontal gyrus and premotor cortex, is consistent with earlier findings about abstract
words in general (Binder et al., 2005). As the premotor
activation, which reached significance for form words, did not
reliably differentiate this word category from color words, the
dorsolateral prefrontal focus seen more active for form than
color words might be of particular functional relevance for
computing abstract form-related action concepts (yellow
circles in Fig. 3).
Conclusion
On the basis of these data, the sensorimotor theory of
conceptual and semantic processing (Warrington and Shallice,
1984; Humphreys and Forde, 2001) can be extended to incorporate a model of concepts that may be considered as
partially abstract. Neuron populations storing abstract concepts
would accordingly be housed in areas adjacent to, and connected with, areas where more elementary and concrete
concepts are laid down. Modality-specific systems may be
located in inferior temporal, middle temporal and parahippocampal gyri that compute feature conjunctions and dysjunctions on visual form and color features. The mirror and/or
canonical neuron system in premotor cortex as a site where
actions and perceptions are linked together offers a unique
basis for action-related abstraction, which could be carried out
by neurons in the adjacent prefrontal cortex performing eitheror operations on motor patterns stored in premotor cortex.
This view, which covers partially abstract concepts still
grounded in action or visual concepts, suggests similar mechanisms of abstraction in different cortical lobes for specific
abstract categories. Although future research is necessary to
decide whether this view can be generalized to the various
types of abstract words and concepts, corroborating evidence
from studies of highly abstract lexical items suggests that the
prefrontal circuits play a general role in the computation of
abstract semantic information.
In conclusion, we report evidence that two subtypes of
partially abstract concepts have their respective brain basis in
specific temporal and frontal areas. Color/form word-evoked
category-specific activation in fusiform, middle temporal and
inferior frontal gyri may be shared in part with other semantic
categories. Specific activation in dorsolateral prefrontal and
parahippocampal gyri may be most characteristic for abstraction processes necessary for classifying sensory and motor
patterns into color and form concepts.
Notes
We thank Rik Henson, Ingrid Johnsrude, Ferath Kherif, Bettina Mohr,
Yury Shytov and two anonymous referees for their help at different
stages of this work. This work was supported by the Medical Research
Council (UK) and by the European Community under the ‘Information
Society Technologies Programme’ (IST-2001-35282).
Address correspondence to Friedemann Pulvermüller, MRC Cognition and Brain Sciences Unit, 15 Chaucer Road, Cambridge CB2 2EF, UK.
Email: [email protected].
References
Baayan H, Piepenbrock R, van Rijn H (1993) The CELEX lexical
database (CD-ROM). University of Pennsylvania, PA: Linguistic Data
Consortium.
Binder JR, Frost JA, Hammeke TA, Cox RW, Rao SM, Prieto T (1997)
Human brain language areas identified by functional magnetic
resonance imaging. J Neurosci 17:353--362.
Binder JR, Westbury CF, McKiernan KA, Possing ET, Medler DA (2005)
Distinct brain systems for processing concrete and abstract concepts. J Cogn Neurosci 17:905--917.
Brown WS, Lehmann D (1979) Verb and noun meaning of homophone
words activate different cortical generators: a topographic study of
evoked potential fields. Exp Brain Res 2:159--168.
Buccino G, Binkofski F, Fink GR, Fadiga L, Fogassi L, Gallese V, Seitz RJ,
Zilles K, Rizzolatti G, Freund HJ (2001) Action observation activates
premotor and parietal areas in a somatotopic manner: an fMRI study.
Eur J Neurosci 13:400--404.
Bussey TJ, Saksida LM (2002) The organization of visual object
representations: a connectionist model of effects of lesions in
perirhinal cortex. Eur J Neurosci 15:355--364.
Bussey TJ, Saksida LM, Murray EA (2002) Perirhinal cortex resolves
feature ambiguity in complex visual discriminations. Eur J Neurosci
15:365--374.
Cappa SF, Perani D, Schnur T, Tettamanti M, Fazio F (1998) The effects of
semantic category and knowledge type on lexical-semantic access:
a PET study. Neuroimage 8:350--359.
Chao LL, Haxby JV, Martin A (1999) Attribute-based neural substrates in
temporal cortex for perceiving and knowing about objects. Nat
Neurosci 2:913--919.
Cohen L, Dehaene S, Naccache L, Lehericy S, Dehaene-Lambertz G,
Henaff MA, Michel F (2000) The visual word form area: spatial
and temporal characterization of an initial stage of reading in
normal subjects and posterior split-brain patients. Brain 123 (Pt 2):
291--307.
Coltheart M (1981) The MRC Psycholinguistic Database. Q J Exp Physiol
33A:497--505.
Cusack R, Brett M, Osswald K (2003) An evaluation of the use of
magnetic field maps to undistort echo-planar images. Neuroimage
18:127--142.
Dehaene S (1995) Electrophysiological evidence for category-specific
word processing in the normal human brain. Neuroreport 6:
2153--2157.
Cerebral Cortex August 2006, V 16 N 8 1199
Dehaene S, Le Clec HG, Poline JB, Le Bihan D, Cohen L (2002) The visual
word form area: a prelexical representation of visual words in the
fusiform gyrus. Neuroreport 13:321--325.
Devlin JT, Jamison HL, Matthews PM, Gonnerman LM (2004) Morphology and the internal structure of words. Proc Natl Acad Sci USA 101:
14984--14988.
Devlin JT, Rushworth MF, Matthews PM (2005) Category-related
activation for written words in the posterior fusiform is task specific.
Neuropsychologia 43:69--74.
Devlin JT, Russell RP, Davis MH, Price CJ, Moss HE, Fadili MJ, Tyler LK
(2002) Is there an anatomical basis for category-specificity? Semantic
memory studies in PET and fMRI. Neuropsychologia 40:54--75.
Duncan J, Owen AM (2000) Common regions of the human frontal
lobe recruited by diverse cognitive demands. Trends Neurosci 23:
475--483.
Fadiga L, Craighero L, Buccino G, Rizzolatti G (2002) Speech listening
specifically modulates the excitability of tongue muscles: a TMS
study. Eur J Neurosci 15:399--402.
Fiebach CJ, Friederici AD (2004) Processing concrete words: fMRI
evidence against a specific right-hemisphere involvement. Neuropsychologia 42:62--70.
Francis WN, Kucera H (1982) Computational analysis of english usage:
lexicon and grammar. Boston, MA: Houghton Mifflin.
Freud S (1891) Zur Auffassung der Aphasien. Leipzig, Wien: Franz
Deuticke.
Friederici AD, Opitz B, von Cramon DY (2000) Segregating semantic and
syntactic aspects of processing in the human brain: an fMRI
investigation of different word types. Cereb Cortex 10:698--705.
Friston KJ, Fletcher P, Josephs O, Holmes A, Rugg MD, Turner R (1998)
Event-related fMRI: characterizing differential responses. Neuroimage 7:30--40.
Fuster JM, Bodner M, Kroger JK (2000) Cross-modal and cross-temporal
association in neurons of frontal cortex. Nature 405:347--351.
Gallese V, Fadiga L, Fogassi L, Rizzolatti G (1996) Action recognition in
the premotor cortex. Brain 119:593--609.
Genovese CR, Lazar NA, Nichols T (2002) Thresholding of statistical
maps in functional neuroimaging using the false discovery rate.
Neuroimage 15:870--878.
Grossman M, Koenig P, DeVita C, Glosser G, Alsop D, Detre J, Gee J
(2002) The neural basis for category-specific knowledge: an fMRI
study. Neuroimage 15:936--948.
Hauk O, Johnsrude I, Pulvermüller F (2004) Somatotopic representation
of action words in the motor and premotor cortex. Neuron 41:
301--307.
Hauk O, Pulvermüller F (2004) Neurophysiological distinction of action
words in the fronto-central cortex. Hum Brain Mapp 21:191--201.
Hickok G, Poeppel D (2000) Towards a functional neuroanatomy of
speech perception. Trends Cogn Sci 4:131--138.
Hodges JR (2001) Frontotemporal dementia (Pick’s disease): clinical
features and assessment. Neurology 56:S6--10.
Hubel D (1995) Eye, brain, and vision. New York: Scientific American
Library.
Humphreys GW, Forde EM (2001) Hierarchies, similarity, and interactivity in object recognition: ‘category-specific’ neuropsychological
deficits. Behav Brain Sci 24:453--509.
Iacoboni M, Woods RP, Brass M, Bekkering H, Mazziotta JC, Rizzolatti G
(1999) Cortical mechanisms of human imitation. Science
286:2526--2528.
Jackendoff R (2002) Foundations of language: brain, meaning, grammar,
evolution. Oxford, UK: Oxford University Press.
Jeannerod M, Frak V (1999) Mental imaging of motor activity in humans.
Curr Opin Neurobiol 9:735--739.
Jezzard P, Balaban RS (1995) Correction for geometric distortion in
echo planar images from B0 field variations. Magn Reson Med
34:65--73.
Kiefer M (2001) Perceptual and semantic sources of category-specific
effects: event-related potentials during picture and word categorization. Mem Cogn 29:100--116.
Kiefer M, Spitzer M (2001) The limits of a distributed account of
conceptual knowledge. Trends Cogn Sci 5:469--471.
1200 Category-specific Conceptual Processing of Color and Form
d
Pulvermüller and Hauk
Kiehl KA, Liddle PF, Smith AM, Mendrek A, Forster BB, Hare RD (1999)
Neural pathways involved in the processing of concrete and abstract
words. Hum Brain Mapp 7:225--233.
Kleene SC (1956) Representation of events in nerve nets and finite
automata. In: Automata studies (Shannon CE, McCarthy J, eds), pp. 3-41. Princeton, NJ: Princeton University Press.
Koenig T, Kochi K, Lehmann D (1998) Event-related electric microstates of the brain differ between words with visual and abstract
meaning. Electroencephalogr Clin Neurophysiol 106:535--546.
Kohler E, Keysers C, Umilta MA, Fogassi L, Gallese V, Rizzolatti G (2002)
Hearing sounds, understanding actions: action representation in
mirror neurons. Science 297:846--848.
Kounios J, Holcomb PJ (1994) Concreteness effects in semantic
priming: ERP evidence supporting dual-coding theory. J Exp Psychol
Learn Mem Cogn 20:804--823.
Kourtzi Z, Kanwisher N (2001) Representation of perceived object
shape by the human lateral occipital complex. Science 293:
1506--1509.
Maes F, Collignon A, Vandermeulen D, Marchal G, Suetens P (1997)
Multimodality image registration by maximization of mutual information. IEEE Trans Med Imag 16:187--198.
Martin A, Chao LL (2001) Semantic memory and the brain: structure and
processes. Curr Opin Neurobiol 11:194--201.
Martin A, Haxby JV, Lalonde FM, Wiggs CL, Ungerleider LG (1995)
Discrete cortical regions associated with knowledge of color and
knowledge of action. Science 270:102--105.
Martin A, Wiggs CL, Ungerleider LG, Haxby JV (1996) Neural correlates
of category-specific knowledge. Nature 379:649--652.
McCandliss BD, Cohen L, Dehaene S (2003) The visual word form area:
expertise for reading in the fusiform gyrus. Trends Cogn Sci 7:
293--299.
McClelland JL, Rogers TT (2003) The parallel distributed processing
approach to semantic cognition. Nat Rev Neurosci 4:310--322.
McClelland JL, Rumelhart DE (1985) Distributed memory and the
representation of general and specific information. J Exp Psychol
Gen 114:159--188.
McKeefry DJ, Zeki S (1997) The position and topography of the human
colour centre as revealed by functional magnetic resonance imaging.
Brain 120 (Pt 12):2229--2242.
Miceli G, Fouch E, Capasso R, Shelton JR, Tomaiuolo F, Caramazza A
(2001) The dissociation of color from form and function knowledge.
Nat Neurosci 4:662--667.
Minsky M, Papert S (1969) Perceptrons. Cambridge, MA: MIT Press.
Neville HJ, Mills DL, Lawson DS (1992) Fractionating language: different
neural subsystems with different sensitive periods. Cereb Cortex
2:244--258.
Noppeney U, Price CJ (2004) Retrieval of abstract semantics. Neuroimage 22:164--170.
O’Craven KM, Kanwisher N (2000) Mental imagery of faces and places
activates corresponding stiimulus-specific brain regions. J Cogn
Neurosci 12:1013--1023.
Perani D, Cappa SF, Schnur T, Tettamanti M, Collina S, Rosa MM, Fazio F
(1999) The neural correlates of verb and noun processing. A PET
study. Brain 122:2337--2344.
Posner MI, Pavese A (1998) Anatomy of word and sentence meaning.
Proc Natl Acad Sci USA 95:899--905.
Preissl H, Pulvermüller F, Lutzenberger W, Birbaumer N (1995)
Evoked potentials distinguish nouns from verbs. Neurosci Lett
197:81--83.
Price CJ (2000) The anatomy of language: contributions from functional
neuroimaging. J Anat 197(Pt 3):335--359.
Price CJ, Devlin JT (2003) The myth of the visual word form area.
Neuroimage 19:473--481.
Price CJ, Warburton EA, Moore CJ, Frackowiak RS, Friston KJ (2001)
Dynamic diaschisis: anatomically remote and context-sensitive
human brain lesions. J Cogn Neurosci 13:419--429.
Price CJ, Wise RJS, Frackowiak RSJ (1996) Demonstrating the implicit
processing of visually presented words and pseudowords. Cereb
Cortex 6:62--70.
Pulvermüller F (1999) Words in the brain’s language. Behav Brain Sci
22:253--336.
Pulvermüller F (2001) Brain reflections of words and their meaning.
Trends Cogn Sci 5:517--524.
Pulvermüller F (2005) Brain mechanisms linking language and action.
Nat Rev Neurosci 6:576--582.
Pulvermüller F, Preissl H (1991) A cell assembly model of language.
Network Comput Neural Sys 2:455--468.
Pulvermüller F, Lutzenberger W, Birbaumer N (1995) Electrocortical
distinction of vocabulary types. Electroencephalogr Clin Neurophysiol 94:357--370.
Pulvermüller F, Lutzenberger W, Preissl H (1999) Nouns and verbs in the
intact brain: evidence from event-related potentials and highfrequency cortical responses. Cereb Cortex 9:498--508.
Pulvermüller F, Shtyrov Y, Ilmoniemi RJ (2003) Spatio-temporal patterns
of neural language processing: an MEG study using minimum-norm
current estimates. Neuroimage 20:1020--1025.
Pulvermüller F, Shtyrov Y, Ilmoniemi RJ (2005) Brain signatures of
meaning access in action word recognition. J Cogn Neurosci 17:
884--892.
Rizzolatti G, Craighero L (2004) The mirror-neuron system. Annu Rev
Neurosci 27:169--192.
Rizzolatti G, Fogassi L, Gallese V (2001) Neurophysiological mechanisms
underlying the understanding and imitation of action. Nat Rev
Neurosci 2:661--670.
Rogers TT, Lambon Ralph MA, Garrard P, Bozeat S, McClelland JL,
Hodges JR, Patterson K (2004) Structure and deterioration of
semantic memory: a neuropsychological and computational investigation. Psychol Rev 111:205--235.
Scott SK, Johnsrude IS (2003) The neuroanatomical and functional
organization of speech perception. Trends Neurosci 26:100--107.
Shallice T (1988) From neuropsychology to mental structure. New York:
Cambridge University Press.
Shtyrov Y, Hauk O, Pulvermüller F (2004) Distributed neuronal networks for encoding category-specific semantic information:
the mismatch negativity to action words. Eur J Neurosci 19:
1083--1092.
Skosnik PD, Mirza F, Gitelman DR, Parrish TB, Mesulam MM, Reber PJ
(2002) Neural correlates of artificial grammar learning. Neuroimage
17:1306--1314.
Smith SM (2002) Fast robust automated brain extraction. Hum Brain
Mapp 17:143--155.
Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human
brain. New York: Thieme.
Tyler LK, Stamatakis EA, Bright P, Acres K, Abdallah S, Rodd JM, Moss HE
(2004) Processing objects at different levels of specificity. J Cogn
Neurosci 16:351--362.
Warrington EK, McCarthy RA (1983) Category specific access dysphasia.
Brain 106:859--878.
Warrington EK, Shallice T (1984) Category specific semantic impairments. Brain 107:829--854.
Wernicke C (1874) Der aphasische Symptomencomplex. Eine psychologische Studie auf anatomischer Basis. Breslau: Kohn und Weigert.
Wilson MD (1988) The MRC Psycholinguistic Database: machine readable dictionary, version 2. Behav Res Methods Instrum Comput
20:6--11.
Wilson SM, Saygin AP, Sereno MI, Iacoboni M (2004) Listening to speech
activates motor areas involved in speech production. Nat Neurosci
7:701--702.
Wise RJ, Howard D, Mummery CJ, Fletcher P, Leff A, Buchel C, Scott SK
(2000) Noun imageability and the temporal lobes. Neuropsychologia
38:985--994.
Zeki S, Aglioti S, McKeefry D, Berlucchi G (1999) The neurological basis
of conscious color perception in a blind patient. Proc Natl Acad Sci
USA 96:14124--14129.
Cerebral Cortex August 2006, V 16 N 8 1201