When Elephants Fly: Differential Sensitivity of Right
and Left Inferior Frontal Gyri to Discourse
and World Knowledge
Laura Menenti
1
, Karl Magnus Petersson
1,2
, Rene´ Scheeringa
1
,
and Peter Hagoort
1,2
Abstract
& Both local discourse and world knowledge are known to in-
fluence sentence processing. We investigated how these two
sources of information conspire in language comprehension. Two
types of critical sentences, correct and world knowledge anom-
alies, were preceded by either a neutral or a local context. The
latter made the world knowledge anomalies more acceptable or
plausible. We predicted that the effect of world knowledge anom-
alies would be weaker for the local context. World knowledge
effects have previously been observed in the left inferior frontal
region (Brodmann’s area 45/47). In the current study, an effect of
world knowledge was present in this region in the neutral context.
We also observed an effect in the right inferior frontal gyrus, which
was more sensitive to the discourse manipulation than the left
inferior frontal gyrus. In addition, the left angular gyrus reacted
strongly to the degree of discourse coherence between the con-
text and critical sentence. Overall, both world knowledge and the
discourse context affect the process of meaning unification, but
do so by recruiting partly different sets of brain areas. &
INTRODUCTION
‘‘The elephant flies’’ is a sentence you can immediately
understand, although you know that elephants typically do
not fly. Maybe you thought of a circus traveling by air-
plane or maybe you thought of Dumbo. To comprehend a
sentence, we rapidly make use of the knowledge we have
about the world, and even if what we read or hear does
not fit with what we typically take for granted we usually
comprehend utterances as long as they are well-formed.
Sentence comprehension can be further facilitated if the
reader or hearer is provided an adequate context. If we
first read the sentence, ‘‘Dumbo is a fantasy animal.’’ then
‘‘The elephant flies.’’ becomes a coherent sentence in its
context. The question then is, how understanding of the
sentence ‘‘The elephant flies’’ is modulated depending on
what we just read or heard. When reading texts or listen-
ing to speech, we are constantly integrating the current
word meaning with the preceding information. Grasping
the neural implementation of contextual integration is an
essential part of understanding the neural organization of
language comprehension.
Modulations of sentence comprehension by discourse
have previously been investigated with various techniques.
In an eye-movement study, Duffy and Keir (2004) in-
vestigated the influence of disambiguating discourse on
processing of gender stereotypes. Sentences such as ‘‘The
electrician taught herself...’’ evoke longer reading times
of the word ‘‘herself’’ because electricians are stereo-
typically men and readers therefore take longer time in-
tegrating the incoming word ‘‘herself.’’ However, after a
disambiguating context explaining that the electrician was
a woman, the effect of stereotype anomaly on reading
times at the critical word disappeared. Hald, Steenbeek-
Planting, and Hagoort (2007) investigated modulation of
world knowledge comprehension by discourse context
with ERPs. Hagoort, Hald, Bastiaansen, and Petersson
(2004) had already established that world knowledge
anomalies, just like semantic anomalies, elicit an N400
effect, which indexes ease of semantic integration of con-
tent words. Hald et al. (2007) presented world knowl-
edge sentences (correct or anomalies: ‘‘Dutch trains are
yellow/white and blue.’’) that were preceded by two types
of contexts: (i) neutral contexts introduced the topic
of the world knowledge sentence and were in line with
the world knowledge of the listener/reader (e.g., ‘‘The
Netherlands are famous for their designers. In addition,
the Dutch railways have chosen a very conspicuous color
scheme, which makes them recognizable everywhere.’’);
(ii) local contexts introduced information that made de-
viations from the default world knowledge more accept-
able (e.g., ‘‘The coming world championships are one
bignationalspectacle.TheDutchrailwayshavepainted
the Dutch flag on their trains.’’) They found that the
N400 effect to world knowledge anomalies was weaker
when the sentences were preceded by the local context,
1
Donders Institute for Brain, Cognition, and Behavior, Nijmegen,
the Netherlands,
2
Max Planck Institute for Psycholinguistics,
Nijmegen, the Netherlands
D 2008 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 21:12, pp. 2358–2368
thereby supporting the idea that ongoing discourse can
modulate the integration of world knowledge information
retrieved from long-term memory. Similarly, Nieuwland
and Van Berkum (2006) investigated discourse modula-
tion of animacy anomalies such as, ‘‘The peanut was in
love.’’ Such animacy anomalies presented in isolation elic-
ited a clear N400 effect compared to neutral sentences,
as ‘‘The peanut was salted,’’ but when these sentences
were preceded by a supporting discourse introducing an
amorous peanut, the N400 effect not only disappeared,
but was reversed: ‘‘The peanut was salted’’ now elicited
a larger N400 than ‘‘The peanut was in love.’’ Taken
together, this suggests that local discourse can override
semantic and world knowledge anomalies and that the
anomaly effect is thus inherently context-dependent.
To form a coherent representation of a multiword ut-
terance, the reader must not only retrieve and integrate
lexical information and world knowledge that is stored
in long-term memory. She also has to form a represen-
tation of the ongoing discourse itself. Here it is impor-
tant to make a distinction between three different types
of discourse representation: the surface code, the text
base, and the situation model (van Dijk & Kintsch, 1983;
see also Graesser, Millis, and Zwaan, 1997, for an ex-
tensive and more recent review). The surface code is a
literal representation of the exact wording and syntax of
the text (‘‘The animal tamer gently patted the elephant.
The animal was afraid of entering the plane.’’), the text
base contains explicit text propositions in a stripped-
down format that preserves meaning (e.g., PAT [animal
tamer, elephant], AFRAID [elephant], ENTER [elephant,
plane]), and the situation model is the content or the
conceptual structure of the microworld that the text de-
scribes (Circus traveling by airplane). In the present
article, by discourse representation, we mean the situa-
tion model level of representation, which determines
how additional incoming information is interpreted.
A recurring issue in fMRI research on discourse com-
prehension is the involvement of the right hemisphere
in language processing and more specifically in discourse
processing. Jung-Beeman (2005; and Beeman 1998) pro-
posed a division of labor between the right and left hemi-
spheres in language processing. In this proposal, the right
and left hemispheres perform similar functions in lan-
guage processingbutthey encode information in a different
way, with the right hemisphere performing coarser seman-
tic coding than the left. In other words, it is suggested that
semantic fields are more focused in the left hemisphere,
whereas they are more diffuse in the right hemisphere.
For example, the semantic field for the word foot might
include hand, leg, toe in the left hemisphere, but in
addition, bare, step, ball in the right hemisphere. Reading
foot will then activate a few related words quite strongly in
the left hemisphere, and many words more weakly in the
right. In addition, the right hemisphere has been shown to
be involved in processing jokes (Bartolo, Benuzzi, Nocetti,
Baraldi, & Nichelli, 2006) and metaphors (Stringaris et al.,
2006; but see Stringaris, Medford, Giampietro, Brammer,
& David, 2007; see Mitchell & Crow, 2005, for a review).
This has been taken to suggest that the right hemisphere
is involved in processing nonliteral language. Recent evi-
dence, however, seems to suggest that the division of
labor is different, in that the left hemisphere is more sen-
sitive to salient (dominant) meanings and direct semantic
relationships, whereas the right hemisphere is more sen-
sitive to nonsalient (novel and inferred) meanings and
more remote relationships, irrespective of whether they
are literal or not (Giora, 2007; Mashal, Faust, Hendler, &
Jung-Beeman, 2007; Schmidt, DeBuse, & Seger, 2007).
A few studies indicate that regions in the right hemi-
sphere are sensitive to discourse coherence. Kuperberg,
Lakshmanan, Caplan, and Holcomb (2006) found that
the right inferior frontal gyrus (RIFG) showed stron-
ger responses to sentences unrelated to preceding two-
sentence contexts than to related sentences. In line with
this finding, St George, Kutas, Martinez, and Sereno
(1999) found that untitled (and therefore less coherent)
paragraphs elicited more activation than titled paragraphs
in the right but not in the left hemisphere. Furthermore,
Caplan and Dapretto (2001) found that such coherence
violation effects depend on the precise type of anomaly.
Their subjects read question–answer dialogues where the
answer was on- or off-topic, versus logical or illogical. For
example, for the question, ‘‘Do you believe in angels?’’ the
on-topic answer was, ‘‘Yes, I have my own special angel,’’
whereas the off-topic answer was, ‘‘Yes, I like to go to
camp.’’ For the question, ‘‘Do you like having fun?’’ the
logicalanswerwas,‘‘Yes,becauseitmakesmehappy,’’
whereas the illogical answer was, ‘‘No, because it makes
me happy.’’ They found that the effect of discourse anom-
alies was more left-lateralized for logicality and more right-
lateralized for topicality.
Hagoort (2005) proposes that the left inferior frontal
gyrus (LIFG) is an active workspace for language pro-
cessing. This region is involved in unifying structured
pieces of knowledge that are stored in long-term mem-
ory (Jackendoff, 2007; Vosse & Kempen, 2000). It also
integrates linguistic with nonlinguistic information, in-
cluding, for example, world knowledge (Hagoort et al.,
2004) or gestures (Willems, Ozyurek, & Hagoort, 2007).
Hagoort et al. (2004) compared integration of semantic
and world knowledge. Semantic knowledge is knowl-
edge about the words in our language. World knowl-
edge, on the other hand, refers to our knowledge about
the state of affairs in the world. An example will clarify
the distinction: the sentence, ‘‘Dutch trains are sour,’’
violates our knowledge about the meaning of the word
‘‘sour,’’ which is not applicable to trains. On the other
hand, the sentence, ‘‘Dutch trains are white,’’ is an in-
terpretable sentence, but it just so happens that Dutch
trains are yellow and, therefore, most Dutch people will
know this sentence to be false. Hagoort et al. found that
compared to correct sentences, the LIFG, specifically
BA 45 and 47, showed stronger BOLD responses to both
Menenti et al. 2359
semantic and world knowledge anomalies. They con-
cluded that this result provided evidence for a role of
the LIFG in the integration of world knowledge as well
as semantic knowledge, in line with linguistic accounts
that have argued for the absence of a clear distinction
between semantic and world knowledge regarding lexi-
cal items (Jackendoff, 2002).
The aim of the present fMRI study is to investigate
whether the LIFG unifies information from long-term
memory and discourse. We investigated whether ongo-
ing discourse could modulate the integration of world
knowledge sentences in the LIFG. If a sentence that
departs from our world knowledge (‘‘The elephant
flies’’) is preceded by a discourse context that supports
it (Circus traveling by airplane), unification should be
easier. As described above, there are a few fMRI studies
that shed light on how the brain processes multisen-
tence utterances. Several of these have found that the
right hemisphere is involved in discourse processing (see
Mitchell & Crow, 2005; Bookheimer, 2002 for reviews).
Because we expected right hemisphere involvement to
be stronger in our study with multisentence texts than it
was in Hagoort et al. (2004), where single sentences were
presented, we investigated modulations of world knowl-
edge unification not only in the left hemisphere regions
where they found increased responses to anomalies but
also in their right hemisphere counterparts. To avoid con-
fusion, we do not think a true dichotomy exists between
‘‘correct’’ sentences and ‘‘anomalies.’’ Rather, there is a
continuum from sentences that fit very well with our
world knowledge to sentences that are odd in the light
of what we know. However, for ease of reading, we use
the terms ‘‘correct’’ and ‘‘anomaly’’ as shorthand.
Our paradigm was similar to the one used by Hald et al.
(2007), with either neutral or local contexts preceding
correct world knowledge sentences or anomalies. The
local contexts were designed to make the world knowl-
edge anomalies more plausible. The predictions were as
follows: First, left BA 45 and 47 were expected to show a
stronger response to world knowledge anomalies than
to correct sentences in the neutral context. Second, the
local context should facilitate integration of the anomaly.
The effect of world knowledge should therefore be re-
duced in the local context compared to the neutral con-
text. Third, because the right hemisphere is known to
be involved in discourse processing, we predicted that
the right BA 45 and 47 would also show modulation of
world knowledge processing by discourse context. Fi-
nally, we investigated the effect of both world knowl-
edge and discourse context at the whole-brain level to
see which additional regions might be involved.
METHODS
Subjects
Thirty-two healthy right-handed Dutch native speakers
with normal or corrected-to-normal vision (13 men,
19 women; mean age = 22 ± 3) participated in the ex-
periment. All subjects had attended or were attending
university education in the Netherlands. All subjects gave
written informed consent prior to the experiment and
received a fee for their participation.
Stimuli and Design
One hundred thirty-two sets of Dutch-language stimuli
were created for this experiment. Like Hald et al. (2007),
we used a 2 2 factorial design with the factors discourse
context (neutral/local) and world knowledge (correct/
anomaly). The contexts were either in accordance with
world knowledge (neutral context), or contained a moti-
vation for the world knowledge anomaly in the critical
sentence, making the anomaly more acceptable (local
context). The critical sentences were either in accordance
with world knowledge or departed from world knowledge
(anomaly). There was, however, one important difference
compared to the ERP study by Hald et al. In the present
study, the contexts were much more tightly matched:
The two versions of a particular context had an identical
syntactic structure, were matched on sentence and word
lengthandonwordfrequency,anddifferedinasfew
words as possible. This was necessary due to the lower
temporal resolution of fMRI compared to EEG. In an fMRI
study, contexts differing as widely as they did in the ERP
study could lead to strong but hard-to-interpret effects on
BOLD responses to the critical sentences (see Table 1 for
translated examples of our stimuli).
All contexts consisted of three sentences. The first sen-
tence was equal between the two versions of the context
and introduced the subject of the text. The other two
sentences were matched on syntactic structure, word fre-
quency, and number of words, and differed on as few
words as possible. The three context sentences were fol-
lowed by the critical sentence. This critical sentence had
two versions, which only differed in one word, the critical
word. The critical word never appeared in sentence-final
position, and the contexts did not contain either of the
critical words.
Two hundred twenty-five sets of stimuli were pre-
tested with 75 subjects in total. Nineteen subjects were
given the single critical sentences only, with no prior
context. The sentences were truncated before the crit-
ical word and subjects were asked to complete them
to make a complete, grammatical sentence. The partici-
pants were instructed to fill in the first thing that came
to mind, and to keep completions as short as possible.
Thirty-one subjects were given a list of items consisting
of half neutral and half local contexts in a random or-
der, again followed by the truncated critical sentences.
Stimuli were selected for the experiment if none of the
subjects completed the critical sentence with the world
knowledge anomaly in the single sentence condition.
After the neutral context, not more than two subjects
should fill in the critical word constituting the anomaly,
2360 Journal of Cognitive Neuroscience Volume 21, Number 12
whereas after the local context, at least three subjects
should respond with the anomaly. The difference be-
tween the cloze probabilities of the critical word consti-
tuting the world knowledge anomaly after the local and
neutral contexts was required to be at least 20%. Paired-
sample t tests showed that the two contexts differed
significantly in terms of cloze probability of the correct
critical word [t(133) = 18.3, p < .001] and of the anom-
alies [t(133) = 27.2, p < .001]. The characteristics of
the selected items are reported in Table 2. The cloze
probability of the correct critical word is higher after the
neutral context than in the single sentence, and lower
after the local context. The cloze probability of the
anomaly is higher after the local context than after the
neutral context, or in the single sentence. Local contexts
do not succeed in completely overriding world knowl-
edge, shown by the residual cloze probability of the
correct word in the local context condition (34%). In the
experiment, four different lists each contained one ver-
sion of every item. The items were presented in four dif-
ferent pseudorandom orders. No more than three items
of the same condition were presented in a row.
Procedure
Each participant saw 132 trials (33/condition). The ex-
perimental session was split in four subsequent runs of
15 min. To ensure that the subjects remained atten-
tive, they were given a content question about the pre-
ceding text on 10% of the trials (e.g., ‘‘Who wrote the
Donald Duck stories?’’), and two possible answers from
which to choose with a button press (‘‘Carl Barks/ Walt
Disney’’). After two runs participants underwent the ana-
tomical scan.
A trial consisted of the following elements: The dis-
course contexts were presented sentence-by-sentence.
Each sentence was presented for a total duration of
900 msec + (250 msec times the number of words).
The interstimulus interval (ISI) between sentences was
750 msec and, after the context had been presented, an
ISI between 2500 and 3500 msec occurred in which a
blank screen was presented. Subsequently, the critical
sentence was presented word-by-word, with 500 msec
per word and a 100-msec ISI between words. The in-
tertrial interval (ITI) between the critical sentence and
the next discourse context was jittered between 4000
and 6000 msec. When there was a question, it was pre-
sented 2000 msec after the last word of the critical
Table 2. Results of the Pretest for the Selected Items
Cloze Probability
Condition Correct Anomaly
Neutral context 77% 1%
Local context 34% 43%
Single sentence 59% 0%
Reported are the cloze probabilities of correct completions and anom-
alies after the truncated critical sentence (Measles is a disease that
especially affects_________). The truncated critical sentence was pre-
sented after the neutral context, the local context, or in isolation.
Table 1. Example Stimuli
Examples
Neutral contexts (1) Carl Barks wrote many Donald Duck stories and invented Duckburg. In his early sketches we see
Huey, Dewey and Louie as young well-behaved boys with hats and scarves. They often go out to
help old ladies.
(2) More and more lamp posts are placed in the Netherlands. This way it is easier to see the road.
This is nice for drivers.
(3) There now is a vaccination against measles. The disease is more frequent the lower the age of
patients is. They are more vulnerable to contagion.
Local contexts (1) Carl Barks wrote many Donald Duck stories and invented Duckburg. In his early sketches we see
Huey, Dewey and Louie as young bad boys with striped sweaters and masks. They often go out to
rob old ladies.
(2) More and more lamp posts are placed in the Netherlands. This way it is harder to see the night sky.
This is sad for astronomers.
(3) There now is a vaccination against measles. The disease is more dangerous the higher the age of
patients is. They are more vulnerable to complications.
Critical sentences (1) Donald Duck’s nephews are
boy scouts/thieves and very smart.
(2) With the lights on you can see
more/less at night.
(3) Measles is a disease that especially affects
children/elderly.
Neutral or local contexts were followed by one out of two critical sentences, which only differed on one word (underlined).
Menenti et al. 2361
sentence. The two possible answers were presented
below the sentence 500 msec after its onset and stayed
on screen for 3500 msec. At the end of this question–
answer period, there was a normal ITI of 4000–6000 msec
before the next context was presented.
Scanning Parameters
Subjects were scanned with a Siemens 3-T Tim-Trio
MRI scanner, using a 12-channel surface coil. The TR
was 1.86 sec, each volume contained 28 slices of 3 mm
thickness with a slice gap of 10%. The voxel size was 3
3 3mm
3
, the field of view was 224 mm. We kept the
TR shorter than usual to allow for subsequent dynamic
causal modeling analyses, which require a shorter TR.
The number of slices, therefore, did not allow acquisi-
tion of a full brain volume in most subjects. The exper-
imenter always made sure that the entire temporal and
frontal lobes were scanned, where the activations of in-
terest were expected. However, this implied that in many
subjects data from a part of the parietal lobe were not
acquired. A whole-brain, high-resolution, structural T1-
weighted MP-RAGE sequence was also performed to
characterize the subjects’ anatomy (TR = 2.30 sec, 192
slices with voxel size of 1 mm
3
, FOV = 256 mm).
Data Analysis
The data were preprocessed using SPM5 (Friston et al.,
1995). Images were realigned to correct for movement
artifacts, were slice-timing corrected, and the mean func-
tional image for each subject was coregistered to the
EPI template provided by SPM5 and to the subjects’ ana-
tomical image. Finally, images were anatomically nor-
malized to the MNI space and spatially filtered with an
isotropic 3-D Gaussian kernel (FWHM = 10 mm). Data
were analyzed using the general linear model and sta-
tistical parametric mapping (Friston et al., 1995). In a
2 2 design, with the factors context (neutral/local) and
world knowledge (correct/anomaly), all four regressors
were modeled from the onset of the critical word to the
end of the sentence and were subsequently convolved
with the canonical hemodynamic response function pro-
vided by SPM5. Additional regressors were included for
the discourse context, the first part of the critical sen-
tence, the intertrial and interstimulus intervals, and fi-
nally, six movement parameters. At the single-subject
level, the four conditions of interest were contrasted
separately against the first part of the critical sentences
of all conditions, which formed a high-level baseline.
The four resulting contrast images were included in a
second-level random effects analysis as well as the fac-
tor subject to account for between-subject variability.
For the ROI analysis small-volume correction was used
for two 10-mm spheres centered around the local max-
ima for the world knowledge effect reported by Hagoort
et al. (2004) (MNI coordinates: left BA 47 [48 30 13]
and left BA 45 [44 30 10]) and their right homotopic
regions (see Figure 1 for the location of the ROIs). For
both the ROI and the whole-brain analysis, images were
thresholded at t =3.16(p < .001, uncorrected). The
cluster size was used as the test statistic and only clusters
significant at p < .05, corrected for multiple nonindepen-
dent comparisons, are reported. Local maxima are also
reported for all clusters with their respective family-wise
error (FWE) corrected p values.
RESULTS
ROI Analysis
In a small-volume corrected analysis for both ROIs in
the LIFG, clusters were found that showed a significant
effect of world knowledge in the neutral context. Signif-
icant clusters were also present in both RIFG ROIs. For
the local context, no clusters were found that showed a
significant world knowledge effect in three of the four
regions (left BA 45, right BA 45, and right BA 47). In the
left BA 47, a cluster was present showing a residual effect
of world knowledge in the local context, although it was
smaller than in the neutral context. We predicted that
the effect of world knowledge would be weakened by
the local context because the world knowledge anomaly
would be easier to integrate after such a context. Clus-
ters showing the predicted interaction between world
knowledge and context were found in right BA 47 and
BA 45, but in neither of the left ROIs (see Table 3 for all
cluster coordinates and p values).
For the average beta values in each ROI, the interac-
tion between context and world knowledge was signif-
icant in both right-hemisphere ROIs, but in neither of
the left-hemisphere ROIs, although it showed a trend
Figure 1. ROIs in the current study. Two 10-mm spheres centered
at MNI coordinates [44, 30, 10] (BA 45, top) and [48, 30, 13]
(BA 47, bottom), and their right hemisphere equivalents.
2362 Journal of Cognitive Neuroscience Volume 21, Number 12
![Figure 1. ROIs in the current study. Two 10-mm spheres centered at MNI coordinates [ 44, 30, 10] (BA 45, top) and [ 48, 30, 13] (BA 47, bottom), and their right hemisphere equivalents.](/figures/figure-1-rois-in-the-current-study-two-10-mm-spheres-zz5hn0xp.webp)