Brain (1998), 121, 1133–1142
Distinct time courses of word and context
comprehension in the left temporal cortex
Päivi Helenius,1 Riitta Salmelin,1 Elisabet Service2 and John F. Connolly3
1Brain
Research Unit, Low Temperature Laboratory,
Helsinki University of Technology, Espoo, 2Department of
Psychology, University of Helsinki, Helsinki, Finland and
3Life Sciences Centre, Department of Psychology,
Dalhousie University, Halifax, Canada
Correspondence to: Päivi Helenius, Brain Research Unit,
Low Temperature Laboratory, Helsinki University of
Technology, PO Box 2200, FIN-02015 HUT, Finland
Summary
The time course and cortical basis of reading
comprehension were studied using magnetoencephalography. The cortical structures implicated most
consistently with comprehension were located in the
immediate vicinity of the left auditory cortex, where final
words totally inappropriate to the overall sentence context
evoked enduring activation starting ~250 ms and lasting
up to 600 ms after word onset. Contextually appropriate
but unexpected words produced weaker activation which
terminated earlier. Highly anticipated words totally failed
to activate this area, suggesting that the conceptual
network became involved only if unexpected information
was detected during the primary word identification
process. We propose that the point in time (350 ms
after word onset) where the response to appropriate but
unexpected endings started to diverge from those to
contextually inappropriate endings reflects the boundary
between understanding a single word and the meaning
of a whole sentence.
Keywords: reading; semantic processing; N400; functional brain imaging; magnetoencephalography
Abbreviations: ERP 5 event-related potential; fMRI 5 functional MRI; MEG 5 magnetoencephalography
Introduction
The rich interconnectivity of the cortex makes it an optimal
structure for merging discrete pieces of information into a
perceptual whole (Pandya and Seltzer, 1982; Goldman-Rakic,
1988; Mountcastle, 1997). For reading and understanding of
written language, several hierarchical perceptual/cognitive
processes must be mobilized (McClelland, 1987; Monsell,
1987; Patterson and Coltheart, 1987). The basic visual
features must first be extracted and combined to form an
image of a letter. Several letters must be processed as a
whole to perceive a word. Successful lexical access based
on, or accompanied by, phonological activation then opens
the way for identifying the meaning of the word and, finally,
for evaluating the word meaning in a particular context. On
the basis of experimental psychology and specific deficits
known to result from brain lesions, the analysis of written
words is thought to consist of distinct subprocesses, such as
orthographic/lexical, phonological, syntactic and semantic
analysis.
Evidence for the neuroanatomical correlates of these still
somewhat controversial modular subcomponents of linguistic
processing is scarce and diverse (Frackowiak, 1994; Price
et al., 1994; Poeppel, 1996). Traditionally, based on brain
© Oxford University Press 1998
lesions that compromise linguistic capacities, the role of
Wernicke’s area in the posterior third of the left superior
temporal gyrus has been emphasized in understanding spoken
and written language (Geschwind, 1970; Mesulam, 1990).
Non-invasive functional imaging studies and intraoperative
recordings have modified this view considerably during
the last decade, indicating that several other areas besides
Wernicke’s may be involved in the semantic processing of
language (Petersen et al., 1988; Wise et al., 1991; Démonet,
1992; Nobre et al., 1994; Damasio, 1996; Martin et al., 1996;
Binder et al., 1997). The non-overlapping results may derive
partly from differences in methods—whereas functional
imaging shows activations associated with the full range of
processes involved in a certain behaviour, lesion studies
reveal the structures essential for that behaviour (Steinmetz
and Seitz, 1991).
Although cognitive models often postulate that the semantic
system is multimodal (e.g. Ellis and Young, 1988) and thus
common to the understanding of written and spoken words
and pictures, functional imaging studies have suggested that
the semantic processing of words versus pictures, for example,
does not activate totally overlapping brain areas
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P. Helenius et al.
(Vandenberghe et al., 1996). PET and functional MRI (fMRI)
studies searching for brain areas involved in the semantic
processing of written words have almost exclusively used
isolated words as stimuli—the involvement of the left frontal
areas (Petersen et al., 1988), the left superior temporal areas
(Pugh et al., 1996) or (Vandenberghe et al., 1996) both has
been indicated, depending on the particular task employed.
A recent fMRI study on comprehension of written sentences
(Just et al., 1996) showed activation of both left and right
frontal and temporal areas. Due to the limited time resolution
of haemodynamic measures, it is not possible to follow the
progression of activation from one brain area to another.
Thus, the analysis must rely heavily on the assumption that
even the most complex cognitive operations are composed
of well-defined, distinguishable modules that are extractable
as invariable units through subtractions between specific
tasks (see criticism of Sergent et al., 1992).
The temporal pattern of cortical activation with respect to
a stimulus provides decisive clues to the functions of cortical
areas. A powerful tool for characterizing the temporal aspects
of language comprehension can be found in the EEG
literature. When contextually constrained sentences end with
a semantically inappropriate word, an event-related potential
(ERP) is elicited 300–500 ms after the onset of the final
word (Kutas and Hillyard, 1984). After their seminal finding,
Kutas and Hillyard (1980) further demonstrated that semantic
anomaly is not critical for eliciting this negative ‘N400’
response; it is also observed in response to semantically
possible but unexpected sentence endings. In fact, all words
were followed by an N400 response, but the response
diminished towards the end of the sentence, with increasing
contextual constraint (Kutas et al., 1988). For word pairs,
the response is smaller to a word which is semantically
related to the preceding word than to a totally unrelated
word, and also to a repeated than to a novel word (Rugg,
1985). The N400 response does not seem to be specific to
written words, because spoken words (McCallum et al.,
1984; Holcomb et al., 1992; Connolly and Phillips, 1994)
and pictures (Nigam et al., 1992; Ganis et al., 1996) can
also elicit this response. However, the spatial distributions
of the N400 response to words and pictures do not overlap
perfectly (Ganis et al., 1996), in line with PET results from
word and picture processing (Vandenberghe et al., 1996).
The precise cognitive processes associated with the N400
response remain unknown (Osterhout and Holcomb, 1995).
It has been argued that the response reflects postlexical
processes, either semantic analysis at the level of an isolated
word or integration of the meaning of the whole sentence
(Holcomb, 1993). The N400 response seems to increase with
the amount of unexpected linguistic information the word
(or picture) contains, whether lexical, semantic or syntactic,
and with the difficulty of integrating the word into the context
(Osterhout and Holcomb, 1995).
The N400 response is likely to arise from many generators
that may be functionally (Nobre and McCarthy, 1994) and
spatially (Halgren et al., 1994; McCarthy et al., 1995)
segregated. The electric signal of the conventional scalprecorded ERPs is blurred by conductivity changes at the
skull and the scalp, complicating the interpretation and
localization of the response. Further, the N400 deflection is
normally reported as an average over several subjects.
Magnetoencephalography (MEG) combines the excellent
time resolution of the ERP with superior spatial resolution.
MEG detects the magnetic field associated with synchronous
electric currents in neurons. Since magnetic signals are not
distorted by the structures surrounding the brain tissue,
identification of the source areas, and interpretation of the
signal, are more straightforward than with conventional ERPs.
With MEG, we identified cortical correlates of semantic
processing in individual subjects using the N400 paradigm.
Method
Subjects
We recorded MEG signals from 10 neurologically normal
subjects: five females (age 20–37 years; mean 26 years) and
five males (age 24–31; mean 28 years). All subjects were
right-handed and their native language was Finnish. They
had no history of reading disorders and their reading speed
was found to be normal (see below). Informed consent was
obtained from all subjects. The studies were approved by the
Academy of Finland.
Materials and procedure
We employed four categories of sentence-ending words
(Connolly et al., 1995). One sentence type was constructed
to lead to a very strong expectation for a certain, probable
final word (e.g. ‘The piano was out of... tune’). Sentences
could also have semantically appropriate but unexpected,
rare endings (e.g. ‘When the power went out the house
became... quiet’; ‘dark’ would have been the most likely
ending for this sentence), anomalous endings—totally
inappropriate to the context (e.g. ‘The pizza was too hot to...
sing’), or phonological endings which were semantically
inappropriate but started with the same phonemes as the
most probable word (e.g. ‘The gambler had a streak of bad...
luggage’). Transparency of the Finnish language (practically
one-to-one correspondence between phonemes and
graphemes) means that the two to four letters and the
phonemes forming the first syllable of the phonological final
words were the same as those making up the beginning of
the most probable final word. There were 100 sentences in
each category. To ensure that the attention of the subjects
was maximally engaged in reading the sentences, each
sentence was used only once. The order of the 400 different
sentences was randomized (no sentence type appeared more
than three times in a row) and they were presented visually
one word at a time (duration 330 ms, blank interval between
words 750 ms). Subjects were instructed to concentrate on
Semantic processing in temporal cortex
the meaning of the sentences. In total, the recording session
lasted ~1 h.
The probability of a sentence ending with a particular
word was tested on 30–63 university students instructed to
fill in the best completion for each sentence. The cloze
probability (Taylor, 1953) of the most often suggested ending
was equal (0.73–1.00) for all four sentence categories. The
number of words in the sentences ranged from four to 10
(mean 6.6, SD 1.1) and the length of the final words varied
from five to 13 characters (mean 7.7, SD 1.8). Neither of
these two measures differed among the four different sentence
types. The distribution of different word classes was also the
same for the four types of final word: 74–85% of the endings
were nouns, 8–14% verbs and 7–18% adjectives or adverbs.
The stimuli (yellow words on a black background) were
projected onto a board, placed at a distance of ~1 m from
the subject. The size of the word was on the average 5.3 cm
(visual angle 6°).
The reading speed of the subjects was tested separately
from the MEG measurement in a computerized lexical
decision task. Sitting in front of a computer screen, subjects
indicated with a response key whether they saw a word or
an orthographically legal non-word, as quickly as possible.
The target word or non-word was preceded by a prime
word of short duration (200 ms), which was, or was not,
semantically related to the following word. The word
recognition speed was estimated as the time to correctly
recognize a Finnish word preceded either by an associated
or non-associated prime word (number of averages 45–48).
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modelled as equivalent current dipoles, and the average
strength of the source current and its three-dimensional
location and orientation, representing the centre of gravity
of the activated area and the mean current flow therein, were
determined from the measured field (Hämäläinen et al.,
1993). To estimate the source strengths as a function of time,
the isolated equivalent current dipoles (seven to nine in each
individual subject), localized from subsets of 12–20 sensors,
were introduced simultaneously into a multidipole model,
keeping their locations and orientations fixed while their
strengths were allowed to vary to achieve the optimal
explanation of the data measured with all sensors. The source
area sensitive to the meaning of the words within sentences
was determined either in the anomalous or phonological
condition, showing a clear dipolar field distribution
with minimal interference from simultaneous activation of
other brain regions. The same equivalent current dipoles
adequately explained the activation elicited by all sentence
endings.
Functional landmarks
To identify the auditory and hand somatosensory cortices of
the individual brains, we also recorded responses to 50-ms,
1-kHz tones, delivered alternately to the left and right ears
every 1.2 s (Mäkelä et al., 1994), and to self-paced left and
right index finger lifts, performed approximately every 3 s
(Salmelin et al., 1995).
Statistical analysis
Magnetic measurements
The magnetic activity was measured using a Neuromag122™ device (Neuromag, Helsinki, Finland), which employs
planar gradiometers arranged in a helmet-shaped array to
cover the whole head (Ahonen et al., 1993). Neuromagnetic
fields which are detectable outside the head are typically
generated by the simultaneous activation of ~1 000 000
synapses in the parallel apical dendrites of pyramidal cells.
As MEG is most sensitive to the cortical currents tangential
to the surface of the head, the recorded signals mainly reflect
activity in the fissural cortex (Hämäläinen et al., 1993).
Approximately two-thirds of the entire cortex lies in the
fissures (Zilles, 1990; Armstrong et al., 1995), and even
activation arising from the gyral cortex usually has at least
a small tangential component, rendering essentially all cortical
activations detectable with MEG. The MEG signals were
averaged for each subject with respect to the onset of
the final word (four categories) of each sentence. Epochs
contaminated by eye blinks were discarded.
Source analysis
The whole-head field patterns were scanned for stable dipolar
field distributions, signalling local coherent brain activation,
up to 900 ms after word presentation. The source areas were
A repeated measures analysis of variance (ANOVA; the
within-subjects factor was sentence type) was performed to
reveal statistically significant differences in the strength of
the N400 response. The temporal pattern of the response
was characterized by measuring, in individual subjects, the
latencies at which the source strength had reached 0% (onset/
offset), 25%, 50%, 75% and 100% of the maximum on the
ascending and descending slopes. The temporal patterns were
tested with a repeated-measures ANOVA (the within-subjects
factors were sentence type and latency). A detailed description
of the statistical findings are given in the legend of Fig. 3.
Results
Figure 1A illustrates the whole-head responses of one subject
(S1) to the four different sentence endings. A striking
difference between categories was observed in the left
temporal sensors, where the anomalous and phonological
sentence endings (incongruent with the established context
of the sentence) elicited a strong sustained activity. The
activation was smaller for the rare endings and totally missing
for the probable sentence endings. A smaller and later effect
of word congruity arose in the right hemisphere too. Figure 1B
depicts, for each of the other nine subjects, the channel
displaying the strongest congruity effect in the left
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P. Helenius et al.
Fig. 1 (A) Variation in the cortical magnetic signal as a function of time in one subject (S1), recorded with the 122-channel
neuromagnetometer. Responses are shown from 100 ms before to 800 ms after presentation of the final word. The sensor array is viewed
from above with the nose pointing upwards. Variation in the magnetic field was measured at 61 sites over the head both latitudinally and
longitudinally (see pair of traces), as illustrated on the schematic heads. The Neuromag-122™ detects the strongest signal just above an
active brain area. The sensor displaying the strongest effect of sentence context (over the left temporal area in this subject) is shown
enlarged in the upper left corner. Responses to the four types of final words are displayed in different colours, as demonstrated at the
bottom. The large magnetic deflection in the upper, but not in the lower, sensor of each channel pair indicates that the underlying current
was flowing longitudinally, directed laterally from the vertex; note that the magnetic field changes most in the direction orthogonal to the
electric current. (B) The output of the sensor displaying a distinct effect of sentence context in the other nine subjects. The maximum
was recorded over the left temporal area in subjects S1–S8, and more frontally in subjects S9 and S10.
hemisphere, detected either by temporal or frontotemporal
sensors.
Figure 2 shows the source areas contributing to the
congruity effect in all subjects. Eight of 10 subjects showed
distinct activation in the left superior temporal cortex, which
could be unequivocally localized in seven subjects (S1–S7,
black dots). The origin of this activation within the upper
bank of the superior (four subjects) or middle temporal gyrus
(three subjects) was confirmed by the orientation of the
current flow, perpendicular to the sulci. In two subjects (S9
and S10), no congruity effect was observed in the left middle
temporal region, but it was in the left frontal lobe (grey
triangles). In addition, sources in the temporoparietal area
surrounding the posterior end of the sylvian fissure (grey
squares) were identified in these two subjects and in three
of the seven subjects showing the more anterior temporal
lobe congruity effect. The left middle temporal and the more
posterior temporoparietal sources did not differ from each
Semantic processing in temporal cortex
Fig. 2 Cortical loci displaying a reliable congruity effect
combined from all subjects. Sources located in the left superior
temporal cortex are plotted as black dots; for the one subject with
two sources in this region, the later activation is shown in white.
Two subjects showed a congruity effect in the left frontal lobe
instead (grey triangles), and five subjects had an additional source
around the posterior end of the sylvian fissure (grey squares). In
five subjects the posterior end of the right superior temporal gyrus
also produced signals sensitive to sentence congruity (grey
circles). Dipoles were located on the schematic brain with the
help of individual MRI (available for seven subjects) and/or using
sources of auditory and hand somatosensory responses as
functional landmarks (see Method). For easy visualization, dipoles
were projected to the surface of the schematic brain; the sources
represented by black dots were located on average 16 mm below
the outer surface of the brain. The sources displayed were
required to have a maximum amplitude exceeding 5 nAm and to
show a difference of at least twice the prestimulus noise level
between responses to anomalous (and/or phonological) and
probable sentence endings.
other in peak amplitude or latency. The distinct cluster in
the middle superior temporal lobe was in the immediate
vicinity of the auditory cortex, with the sources, on average,
within 24 mm (range 11–39 mm) of the area activated by
brief tones.
In five subjects the posterior end of the right superior
temporal gyrus also produced signals sensitive to sentence
congruity (Fig. 2, grey circles). The overall number of
context-sensitive sources was, however, significantly higher
in the left than in the right hemisphere (P , 0.03). In every
one of those four subjects who had a localizable source in
both hemispheres, the peak activation (averaged across the
anomalous and phonological endings) was ~25 ms later in
the right (range 388–474 ms) than in the left (range 377–
453 ms) temporal area. All the source areas plotted in
Fig. 2 showed essentially the same behaviour—the strongest
responses were elicited by the anomalous and phonological
final words, peaking ~400 ms after word onset, whereas
practically no response was recorded to the probable ending.
Figure 3A displays the time behaviour of the directly
comparable sources of subjects S1–S7, clustered in the left
superior temporal cortex. To compare the responses elicited
by the different types of final words, the source strengths
were normalized with respect to the maximum activation in
the phonological condition, typically displaying the strongest
absolute amplitude. Time behaviour of these normalized
amplitudes (mean 6 SEM) over seven subjects is shown in
Fig. 3B. The pattern is the same as in the individual
122-channel data and source waveforms—anomalous and
phonological final words were followed by equally strong
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activation, lasting until ~600 ms after word onset, whereas
the rare endings resulted in a significantly weaker (P ,
0.0001) response, in agreement with previous ERP results
(Connolly et al., 1995). The response to rare endings also
terminated earlier (P , 0.002). Interestingly, no activation
exceeding the background noise was observed after the
probable sentence endings in six of these seven subjects.
The activity elicited by the three unexpected endings
always began 250 ms after word onset, with no statistically
significant differences according to the type of incongruency.
The responses to the rare final words culminated, on average,
at 350 ms. The activations elicited by the anomalous and
phonological final words continued to increase after this time
point, but the waveforms started to diverge, the phonological
activation lagging behind the anomalous waveform by ~35 ms
(P , 0.02).
Figure 4 depicts the relationship between the behaviourally
measured word recognition speed and the latency of activation
in the left superior temporal cortex, represented by the time
at which the source strength had reached 50% of the
maximum. A statistically significant correlation between
word recognition speed and latency of the neuromagnetic
response was observed with anomalous (Pearson r 5 0.84,
P , 0.02) and phonological (r 5 0.89, P , 0.007) final
words; in the rare condition the correlation (r , 0.63) failed
to reach significance in this small sample.
Discussion
We employed MEG to track the time course of comprehension
of written sentences using final words which varied in their
semantic appropriateness to the overall sentence context. We
were able to identify, in individual subjects, multiple, widely
distributed cortical areas that were sensitive to the meaning
of the final word in a sentence context. Areas surrounding
the left auditory cortex, in the upper banks of the left superior
and middle temporal gyri, were found to be most consistently
involved in understanding written sentences.
Evidence from behavioural studies indicates that both
primary visual analysis and perception of the global form of
the word have been achieved by 200 ms after word onset
(e.g. Balota and Chumbley, 1985). The fairly late onset
(250 ms) of the left temporal activation thus strongly suggests
that this response is related to the analysis of the meaning
of the word and its role in the context created by the sentence.
The virtually identical onset of activation for the different
final words further suggests that, up to this point, the
basic visual/linguistic processing is largely independent of
semantics, as suggested also by reaction time studies (Taft,
1991). Thereafter, a distinct stage of cognitive processing
begins, with the intensity and duration of the cortical response
heavily dependent on comprehension of the word and
sentence. The interpretation that the left temporal response
reflects purely postlexical processes is also in perfect
concordance with previous ERP studies, indicating that the
N400 effect is not reduced by stimulus degradation thought
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P. Helenius et al.
Fig. 3 (A) The time course of source activation in the left superior temporal cortex in subjects S1–S7. Since the average activity
following the probable sentence endings (5.4 6 1.5 nAm; mean 6 SEM) did not differ from the prestimulus noise level (2.9 6 0.6
nAm), the probable condition was not included in further analysis. The average peak amplitudes differed significantly for the three types
of unexpected endings [F(2,12) 5 23.4, P , 0.0001]. Planned contrasts between the peak amplitudes of anomalous (20.5 6 2.4 nAm)
and phonological (20.7 6 2.4 nAm) endings revealed no difference. Rare sentence endings produced a significantly smaller response
(14.2 6 2.0 nAm) than either anomalous (P , 0.0001) or phonological (P , 0.0001) endings. Colour coding as in Fig. 1. (B) Time
behaviour of normalized waveforms (mean 6 SEM) of the three unexpected sentence endings in the left superior temporal cortex. The
source amplitudes were scaled individually, setting the maximum activation in the phonological condition equal to 1. The latencies and
relative amplitudes were measured at points where the source amplitude reached 0% (onset/offset), 25%, 50%, 75% and 100% of the
maximum source strength in each condition, and averaged over subjects (S1–S7). The dashed line shows the average prestimulus noise
level. The temporal patterns of the responses to three types of unexpected final words differed significantly, both when compared with
respect to their overall shape [F(2,12) 5 20.6, P , 0.0001] and when the ascending [F(2,12) 5 6.0, P , 0.02] and descending
[F(2,12) 5 22.9, P , 0.0001] slopes were considered separately. On the ascending slope, planned contrasts revealed statistically
significant differences between categories only when 75% of the peak activity had been reached; both anomalous (P , 0.03) and rare
endings (P , 0.0009) reached 75% of their maximum strength earlier than phonological endings. The rare sentence endings peaked
earlier than the anomalous (P , 0.02) and phonological (P , 0.0001) endings. In an analysis combining the ascending and descending
slopes, the time behaviour of the anomalous and phonological endings was also different (P , 0.008), the phonological ending tending
to peak later (P , 0.08).
to tap the presemantic processing stages of word recognition
(Holcomb, 1993).
The response waveforms following all incongruent endings
were similar to each other until ~350 ms after word onset,
when the activation elicited by the rare final words started
to fade out. This event coincided with the onset of statistically
significant divergence in the responses to the anomalous and
phonological final words, suggesting a transition between
two separate cognitive processes. As the rare endings are
integrated into the overall sentence context rather effortlessly,
the short-lived response probably reflects analysis of the
word meaning. The continued activation of the left temporal
cortex in the 350–600 ms range could then signal the next
perceptual/cognitive level, which is the extended analysis of
the incongruous word meaning in sentence context. It is
thus likely that the cortical activation reflects two possibly
overlapping semantic processes, the first interval, from 250
to 350 ms, mainly dominated by analysis of word meaning,
and the period from 350 to 600 ms by integration of the
word into the sentence context. The source areas active
during these two processes were, if not the same, at least
indistinguishable from each other.
The recognition speed with the real words was significantly
correlated with the latency of the N400 response. Due to the
fact that the lexical decision time is closely related to the
speed at which the meaning of the word can be activated
Semantic processing in temporal cortex
Fig. 4 Latency of activation of the left superior temporal cortex
as a function of word recognition speed in subjects S1–S7. The
latency of the cortical activation was defined as the time point
where the source amplitude reached 50% of the maximum signal.
(James, 1975), a stage probably reflected in the rising slope
of the left superior temporal activation, this correlation is not
surprising. This kind of correlation should be of particular
interest when disorders of language, e.g. dyslexia, are studied.
The similar onset latencies of the left temporal responses
to the two semantically anomalous endings suggest that fluent
readers perceived a word as a whole, or at least in units
larger than a few letters—the ‘correct’ letters at the beginning
of the phonological final words did not clearly delay the
onset of analysis of word meaning. However, at the later
stage, probably reflecting integration of the word to the entire
sentence, the phonological response showed a systematic 35ms time lag in comparison with the anomalous condition.
Processes based on the analysis of sublexical units as opposed
to whole words (Patterson and Coltheart, 1987) may thus
mainly delay the beginning of the context-sensitive stages of
word analysis. In the auditory domain, where the input is
necessarily serial, a delayed N400 response to final words
beginning with the same phonemes as the most probable
word has been reported in an ERP study (Connolly and
Phillips, 1994).
Although all words in a sentence (Kutas et al., 1988), and
even isolated words (Salmelin et al. 1996), are known to
result in a clear activation peaking 300–500 ms after word
onset, the probable endings totally failed to activate the left
temporal cortex or any other area sensitive to sentence
meaning, or the activation was so minor as not to be detected
with MEG. This observation suggests that the word had
already been recognized as the one expected at the level of
lexical access, at the latest, thus rendering further processing
unnecessary. In this study the sentences were constructed to
lead, with little ambiguity, to the expectation of one particular
terminal word. The relatively slow presentation rate of the
words ensured that the subjects had adequate time to become
aware of the sentence context. The lack of activation with
probable final words is thus likely to be the result of top–
down build-up of anticipation (Neely, 1977, 1991). It would
seem that the only truly efficient and economic way for the
1139
brain to work would be to ignore the fulfilment of the
anticipated scenarios and instead concentrate on new, aberrant
information.
The neural generators of the widespread scalp-recorded
N400 response, with the maximum around the vertex or in
the parietal sensors, have remained unestablished (Nobre
and McCarthy, 1994). Intracortical depth recordings have
provided more information about the neural generators of
language-related processing (Smith et al., 1986; Halgren
et al., 1994; Guillem et al., 1995; McCarthy et al., 1995;
Nobre and McCarthy, 1995). When written words have been
used as stimuli the role of the medial temporal structures
near the hippocampus and amygdala have been emphasized
in the generation of the N400 response (Smith et al., 1986;
Halgren et al., 1994; McCarthy et al., 1995; Nobre and
McCarthy, 1995). However, Halgren et al. (1994) reported
N400-like responses also from more superficial cortical
structures, including the region of the superior temporal
sulcus.
The emphasis on lateral rather than medial temporal
activations in the present MEG data may be associated with
the rapid decay of the magnetic field as a function of distance
from the sensors (Hari, 1993). Also, field patterns arising
from currents, e.g. in the inferior surface of the temporal
pole (McCarthy et al., 1995; Nobre and McCarthy, 1995)
would not be covered adequately by the MEG helmet used,
thus making them even less likely to be identified, especially
in the presence of the dominant lateral neocortical activation.
It also seems that the intracortical recordings, done on
patients, oversample the medial temporal structures compared
with the quite infrequently (if at all) targeted lateral neocortex
(Smith et al., 1986; Halgren et al., 1994; Guillem et al.,
1995; McCarthy et al., 1995; Nobre and McCarthy, 1995).
The lateral temporal origin of the N400 response is further
supported by a recent seven-channel MEG study; in five of
the seven subjects N400-like activation to sentence endings
was localized close to the left superior temporal sulcus
(Simos et al., 1997). An obvious approach for the future is
to combine whole-head MEG and ERP recordings. The
readily identified MEG sources would serve as the initial
estimate for the distribution of activity, and additional sources
(possibly also subcortical) could then be determined based
on the remaining unexplained electrical activity.
Comparison of haemodynamic (PET, fMRI) and
electrophysiological (MEG, ERP) measures is not straightforward. While MEG records the synchronous postsynaptic
currents in neural populations with millisecond time
resolution, PET and fMRI measure the overall level of blood
flow (oxygen consumption) with respect to a certain task
over several seconds or even minutes. Thus the results
cannot be expected to overlap perfectly, even if the stimulus
parameters are essentially the same. It is also worth noting
that even minor changes in stimulus parameters (e.g.
prolonging the duration of a stimulus) can change the
haemodynamic activation patterns radically (Price et al.,
1994). Sentences may well tap semantic processing
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P. Helenius et al.
significantly more efficiently than isolated words, and thus
the results of the present study should be compared primarily
with PET/fMRI studies in which the stimuli have been as
similar as possible to those in the present study.
Just et al. (1996) used three types of sentences designed
to differ in structural complexity. The fMRI signals were
monitored around Wernicke’s and Broca’s areas and their
right-hemisphere homologues. All these areas showed
increased activation with increasing linguistic complexity.
The present results and those reported by Just et al. (1996)
thus differ mainly with respect to the frontal activation.
However, as pointed out in the comment by Rapp and
McCloskey (1997), the syntactic complexity of the sentences
used in the study of Just et al. (1996) covaried with their
semantic complexity, which could account for the inferior
frontal activation. In another recent fMRI study, Bavelier
et al. (1997) contrasted sentence reading with the viewing
of consonant strings. The subtracted activations thus reflected
all aspects of sentence processing from lexical access to
semantic and syntactic processing. Multiple perisylvian
structures were found to be involved in sentence reading,
most consistently in Broca’s area and along the left superior
temporal sulcus, in accordance with the temporal activation
detected in our study. The frontal activation may again reflect
the more general activation associated with reading in the
study of Bavelier et al. (1997) compared with the targeted
semantic processing of the present experiment. Bavelier
et al. (1997) analysed activations elicited by sentence-reading
individually in each subject and found that the activation
pattern was composed of several small patches, variable
across subjects, rather than of large well-circumscribed
centres of activity. The large variation among individuals
may explain some of the inconsistencies found between
methods based on averaging across subjects (e.g. PET) and
on individual analysis [e.g. lesion studies and MEG; see also
Steinmetz and Seitz (1991)].
Although both hemispheres may be involved in the
processing of written language (Price et al., 1994; Just et al.,
1996), an unequivocal left-hemisphere dominance, based on
the number of identified sources, was detected in nine of our
10 right-handed subjects. This is concordant with the findings
of, for example, Just et al. (1996), who found that the overall
level of activation during sentence reading was significantly
higher in the left than in the right hemisphere. More
specifically, we also noted that the responses in the left
hemisphere were systematically ~25 ms earlier than in
the right hemisphere, although the small number of righthemisphere observations prevents us from drawing firm
statistical conclusions about the latency difference.
The magnetic signal probably reflects synchronous
activation of focal nodes within a distributed conceptual
network, which could involve all aspects of language
reception and production (Mesulam, 1990). The balance
within the network undoubtedly depends on the task (Ganis
et al., 1996; Vandenberghe et al., 1996) and shows some
individual variation; in the present study the congruity effect
was detected in the left frontal, rather than the superior,
temporal cortex in two subjects. While many brain areas are
certainly involved in semantic processing (Just et al., 1996;
Vandenberghe et al., 1996; Bavelier et al., 1997), the strong
dominance of the temporal activation may well be related to
the closeness of the auditory cortex, the primary route for
language acquisition.
We propose that it is possible to separate out a specific
context-sensitive stage of word processing from activation
related to lexical semantic analysis. The reliability with which
this activation can be detected, and both spatially and
temporally characterized in individual subjects, holds promise
for further studies of more specific features of the neural
networks subserving the perceptual and cognitive processes
of language.
Acknowledgements
We wish to thank R. Hari for useful comments on the
manuscript and M. Illman for assistance in running the
measurements. This work was supported by the Academy of
Finland, Sigrid Juselius Foundation, Human Frontier Science
Program, Natural Sciences and Engineering Research Council
of Canada, Heart and Stroke Foundation of Nova Scotia and
March of Dimes Birth Defects Research Foundation. The
MRIs were obtained at the Department of Radiology, Helsinki
University Central Hospital.
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Received August 28, 1997. Revised December 31, 1997.
Accepted January 23, 1998