Download Demonstrating the Implicit Processing of Visually Presented Words

Demonstrating the Implicit Processing of
Visually Presented Words and
Pseudowords
This study demonstrates that even when subjects are instructed to
perform a nonlinguistic visual feature detection task, the mere presence of words or pseudowords in the visual field activates a widespread neuronal network that is congruent with classical language
areas. The implication of this result is that subjects will process
words beyond the functional demands of the task. Therefore, contrasting brain activity in a word task that explicitly requires a cognitive
function with a word task in which the function is activated implicitly
will not necessarily isolate the brain area of interest Furthermore, in
most brain regions, we found that pseudowords, which have unfamiliar phonological associations and no associated semantic association,
produce greater activation than words. Greater brain activity associated with pseudowords illustrates that unfamiliar stimuli that are unable to access word associations may activate the neuronal network
more strongly than familiar words for which access occurs with ease.
A number of functional imaging studies have investigated the
brain areas associated with auditory and visual word processing using positron emission tomography (PET; e.g., Petersen
et al., 1988, 1990; Wise et al., 1991; Demonet et al., 1992;
Howard et al., 1992). These studies are usually designed to
identify the anatomical substrates of the individual components of word processing models. Often, stimulus conditions
are chosen on the assumption that successive word tasks will
engage one more component of the word processing model
and that categorical comparisons between tasks will identify
the component of interest. The expectation is that there will
be more neuronal activity in functionally specialized areas
when a task demands the explicit involvement of the pertaining function than when it does not. For instance, in the pioneering study by Petersen et al. (1988), anatomical areas engaged by visual and auditory word processing were investigated by comparing the cerebral blood flow distribution during different word tasks within a three-level subtractive
hierarchy. The first level of the hierarchy was a silent word
viewing condition and comparison of flow in this task with
flow when viewing a fixation point (the baseline task) was
intended to isolate sensory input and involuntary word-form
processing. The second level of the hierarchy was reading
aloud and comparison of flow to that during silent word viewing aimed to isolate speech output processes.The third level
of the hierarchy was a verb generation task (saying an appropriate verb in response to a seen noun) and comparison of
flow in this task to that during reading aloud aimed to isolate
semantic processing.
In a subsequent PET study designed by Petersen et al.
(1990), the areas activated during visual word processing
were investigated further by comparing brain activity during
silent viewing of real words, pseudowords (e.g., FLOOP), consonant letter strings (e.g., JVJFQ, false font
and visual fixation. The brain activity during silent viewing of
each stimulus type was compared to visual fixation. Words
C. J. Price, R. J. S. Wise, and R. S. J. Frackowiak
Wellcome Department of Cognitive Neurology, Institute of
Neurology, London WC1N 3BG, United Kingdom
have legitimate word forms with semantic and phonological
representations; related activity was detected in the left medial extrastriate visual cortex and a left prefrontal area. Pseudowords have legitimate word forms from which phonological but not semantic associations can be computed; related
activity was detected in the left medial extrastriate cortex but
not in the left prefrontal cortex. Consonant letter strings and
false fonts do not have stored word associations and did not
activate either the left medial extrastriate cortex or the left
prefrontal cortex. These results were interpreted as evidence
that the left medial extrastriate cortex was activated by legitimate word forms and the left prefrontal region was activated
by stimuli with semantic associations. No area of activity was
associated with phonological processing.
The assumption behind both Petersen et al.'s studies (1988,
1990), that is, that some word tasks elicit very limited processing responses by the brain, has been challenged by Wise
et al. (1991) and Price et al. (1994). Referring to the Petersen
et al. (1988) article, Wise et al. (1991) suggested that both
word generation and word repetition engage semantic processing and therefore the activity in the left frontal cortex
seen when these conditions were compared primarily related
to processes involved in word generation. The association of
the left frontal region with intrinsic generation is consistent
with the studies by Frith et al. (1991a,b), which showed that
the left dorsolateral prefrontal cortex is activated in generation tasks even when subjects have to produce responses other than words.
There is ample evidence from the psychological literature
that the presentation of familiar words during silent or repeating tasks will automatically activate semantic and phonological representations even when subjects are not instructed to access these processes explicitly (e.g., Van Orden
et al., 1988; Macleod, 1991; Coltheart et al., 1994). Further, the
obligatory activation of these processes affects subsequent or
concurrent language tasks. For instance, when subjects are
required to name the physical color of a word, they respond
faster if the phonological representation of the word is the
same color as the physical color of the word (e.g., the word
RED printed in red ink), and they respond more slowly if the
phonological representation is a different color to the physical color (e.g., the word RED printed in green ink)—the
Stroop effect (see Macleod, 1991, for a review). Consistent
with these theories, Price et al. (1994) showed that when
subjects viewed words silently, activity relative to false font
was detected in a widespread network of language areas involving bilateral posterior temporal cortices, the left inferior
frontal cortex, the left inferior parietal cortex, both sensorimotor cortices, and the supplementary motor area (SMA).
These areas are known to be essential for word processing
from both lesion studies (see Mesulam, 1990, for a review)
and from previous PET studies, which explicitly explored activation of semantic and phonological processing (Wise et al.,
1991; Demonet et al., 1992). Activity during silent viewing in
the sensorimotor cortex and the SMA suggested that there
Cerebral Cortex Jan/Feb 1996;6:62-70; 1047-3211/96/$4.00
was subvocal outflow to the muscles responsible for articulation even though subjects were not instructed to speak.
In order to explain why this network of activity was not
detected in the Petersen et al. (1990) study where the same
conditions were compared, Price et al. (1994) suggested that
the critical differences in the studies were (1) the increased
sensitivity inherent in the introduction of 3-D image acquisition, and (2) the development of newer PET analysis techniques employed in the more recently conducted Price et al.
(1994) study. However, another possibility is that subjects in
the different studies may have been responding to the words
in different ways. In the Petersen et al. (1990) study, subjects
were simply instructed to look at the monitor and fix their
gaze on a central fixation point. In the Price et al. (1994) study,
the subjects were instructed to look directly at the words and
may have sounded out the word internally, although not instructed to do so.
The present article investigates the implicit activation of
language areas by engaging subjects in a nonlinguistic visual
feature detection task with a button-press response while either words or nonwords were presented in the visual field.
The task and the instructions to the subjects remained constant in all conditions and did not involve reading the words.
The only variable was the type of stimulus on which the subject performed the task. The stimuli were chosen to match
those used in the Petersen et al. (1990) study described above,
that is, familiar words, pseudowords, consonant letter strings,
and false font. Any differences detected between conditions
can be attributed to word processing while subjects were
engaged in an irrelevant, nonlinguistic task.
Materials and Methods
During each PET scan, subjects performed one task—"the feature
detection task." For this, subjects were familiarized with the distinction that some letters have ascenders (e.g., b,d,l,t,f) while others do
not (e.g., a,e,g,p) and instructed to press a mouse key with their right
index finger when they detected one or more ascenders within a
stimulus. When no ascender -was detected in a stimulus, they made
no response. An Apple Mac Plus computer running the PSYCHLAB program (Bub and Gum, 1988) controlled the presentation of stimuli to
subjects at a rate of one per 1.5 sec (1.0 sec exposure time, 0.5 sec
interval) and measured reaction times and accuracy of the feature
detection task.
While the task remained constant in all activation conditions the
one variable was the type of stimulus presented. There were four
types of stimulus: (1) real words (single nouns, with access to both
phonological and semantic representations) printed in lowercase—
in half the words one or more letters had an ascender (e.g., toad)
and in the other half there were no ascenders present (e.g., grass);
(2) pseudowords (which have corresponding phonological but not
semantic representations) constructed by rearranging the letters of
the words in condition 1 into pronounceable letter strings (e.g., grass
to sargs, toad to dato), thereby matching the letters in the word and
pseudoword conditions; (3) consonant letter strings (which have neither phonological nor semantic associations) constructed to be as
unword-like as possible (e.g., hlgb) since word-like letter strings (e.g.,
pxnt) might result in high levels of lexical-semantic activation (Rummelhart and McLelland, 1981); (4) false fonts (which contain no linguistic features) constructed by substituting letters in the real words
of condition 1 with 26 nonletters matched for size, ascenders,
and descenders to give them the same overall shape as the words
A fifth baseline condition was also included in the design. This
was a resting condition with eyes closed, during which time the
subjects were instructed to empty their minds. This condition was
included to allow us to measure the activity specifically associated
with the task of feature detection.
The five different conditions were incorporated into three different experiments with three conditions repeated four times within
each experiment. The conditions for experiment 1 were (a) rest, (b)
false font, and (c) words; for experiment 2 were (a) false font, (b)
consonant letter strings, and (c) words; and for experiment 3 were
(a) pseudowords, (b) consonant letter strings, and (c) words.
Incorporating the five different conditions into three separate experiments with'four repetitions of each condition within an experiment allows us to examine the results of individual subjects while a
meta-analysis over the three experiments gives us maximum statistical power for group results. The order of presentation of conditions
for each experiment was ABCCBAABCCBA. There were four subjects
in the first and second experiments and six subjects in the third
experiment. All were English-speaking,right-handedvolunteers, with
no history of neurological disorders, and each gave informed consent
to participate in consecutive measurements of rCBF with an effective
dose equivalent of < 7.2 mSv (approved by the Administration of
Radioactive Substances Advisory Committee of the Department of
Health (UK). The protocol was approved by the research ethics committee of the Hammersmith Hospital.
Data Acquisition
Scans were performed on a Siemens 953B (Erlangen, Germany) dedicated head scanner with retracted septa (Spinks et al., 1992) using
injected radiolabeled water (H2"O) as the tracer of perfusion (rCBF).
For each scan approximately 555 MBq of H2"O in 3 ml of normal
saline were flushed into the subject over 20 sec at a rate of 10 ml/
min by an automatic pump. After a delay of approximately 35 sec,
counts were detected in the head, peaking 30-40 sec later (depending on individual circulation time). The interval between successive
H2"O administrations was 10 min. Data were acquired in one 90 sec
scan frame, beginning 0-5 sec before the rising phase of the head
curve (Silbersweig et al., 1993).
Correction for attenuation was made by performing a transmission scan with an exposed 6sGe/MGa external source at the beginning
of each study. Images were reconstructed in 3-D by filtered back
projection (Harmingfilter,cutoff frequency of 0.5 Hz), giving a transaxial resolution of 8-5 mm full width at half-maximum. The reconstructed images contained 128 X 128 pixels, each 2.05 X 2.05 X
2.00 mm in size.
Image Analysis
Image analysis was performed on a SPARC STATION II (Sun Microsystems Europe Inc., Surrey, UK), using an interactive image display
software package (ANALYZE, Biodynamic Research Unit, Mayo Clinic,
Rochester, MN; Robb and Hanson, 1991) and statistical parametric
mapping (Frackowiak and Friston, 1994; SPM software, MRC Cyclotron
Unit, London, UK). Calculations and image matrix manipulations were
performed in PRO MATLAB (Mathworks Inc., Sherborn, MA).
The distribution of rCBF in the brain was indexed by the accumulated counts over the scanning period, which reliably reflects flow
in the physiological range (Mazziotta et al., 1985; Fox and Mintun,
1989). These data were reoriented parallel to the intercommissural
line (Friston et al., 1989), then standardized for brain size and shape
(Friston et al., 1991b). When stereotactically normalized, one voxel
in the transformed image represented 2 mm in the x and y dimensions and 4 mm in the z dimension, which corresponds to the dimensions of the atlas of Talairach and Tournoux (1988). The standardized images were smoothed with a Gaussian filter 20 mm in
width to account for variation in gyral anatomy and individual variability in structure-function relationships, and to improve signal-tonoise ratio. As a result, each voxel rCBF equivalent value corresponds
to a weighted mean rCBF centered in a spherical domain of about
20 mm in diameter.
Global variance between conditions was removed by a previously
described method (Friston et al., 1990), using analysis of covariance
(ANCOVA). This analysis generated maps of adjusted mean values of
rCBF for each of the experimental conditions with corresponding
associated adjusted error variance maps required for comparison of
these means. The differences between conditions were assessed by
formal comparisons of the condition specific rCBF maps. Adjusted
condition means and variances were compared on a pixel-by-pixel
basis by weighting the condition means by an appropriate contrast
(Friston et al., 1991a). The resulting map of t values constituted the
t statistical parametric map [SPM(0], which indicates the sites of statistically significant change in relative blood flow distribution associated with the differences between the compared conditions. With
so many voxel by voxel comparisons, many t values reach conventional levels of significance by chance. Therefore, the significance
Cerebral Cortex Jan/Feb 1996, V 6 N 1 63
TASK
Ff
4 subjects
R
16 X 16 scam
Exp. 1
^^^^^^H
L
Table 1
Activity associated with feature detection task
W
Ps
j^^^^^^^^^J^^^^^^^^H
| ^ ^ H ^ ^ ^ ^ ^ ^ | ^ ^ ^ | 1 6 X 1 6 scans
Exp. 1
^^H^^H
8 subjects
Cortical
Posterior fusiform gyrus
Ff
|^^^H
N
T
R
O
Exp. 2 ^ ^ ^ H |
^ ^ ^ ^ ^ ^ ^ ^ |
T
L
32 X 32 scans
^ ^ ^ ^ H ^ H 16X16 scans ^ ^ ^ ^ ^ ^ H
Not
compared
6 subjects
Exps. 1 & 2
Middle/inferior temporal
junction
10 subjects
Middle/superior temporal
junction
^^^^^^^^1
^ ^ ^ ^ ^ H 24X24 scam
^^^^^H^^^H
^ ^ ^ ^ H
Exp. 3
4 0 X 4 0 scans
Exps. 2 & 3
L
Ps
^ ^ ^ ^ ^ | ^ H 6 subjects ^ ^ I ^ ^ ^ ^ H 6 subjects
^ ^ ^ ^ ^ H 24X24 scans | ^ H | ^ ^ H 24 X 24 scans
Exp. 3
6.4
8.4
6.4
-28,-82,0
+22,-32.-8
- 8 , -78, - 4
il
83
8.0
-40,-54,-12
+40,-52,-12
19
8J
-42, -54, -12
+40,-46.-16
3£
7J)
-48,-20,-12
5.4
-34, -64, +36
+26.-62,+24
-38, -36, +44
W
19
6J
-36,0,+32
17
-40,-28,+56
US
Left
Right
-28,-88,-12
+24, - 9 2 , - 8
Left
Right
Posterior lingual gyrus'
Middle fusiform gyms
c
o
Words - rest
False font - rest
4 subjects
^^^^^^^^^^^^H
4 subjects
Coordinates of peak and Z score
Location
Left
Right
+56, -44, +8
Posterior parietal-occipital
junction
Left
Right
-26, -64, +36
+26,-64,+24
-36,-36,+48
11
17
5£
8.0
+2,-78,0
Deep inferior parietal lobe
Left
Inferior frorrtal/premotor
junction (44/6)
Left
Primary sensory motor
cortex (3/4|
Left
-38,-30,+56
5J
+2,-16,-8
17
+6,-16,-8
4.1
Left
Right
-26,-26,-4
+16,-24,-4
3.4
11
-24, -24, - 4
+18,-20,-4
18
13
+2.-8,+8
4.0
-2,-10,+8
19
Subcortical
W
8 subjects
10 subjects
6 subjects
32 X 32 scans
4 0 X 4 0 scans
2 4 X 2 4 scans
Exps. 1 & 2
Exps. 2 & 3
Exp. 3
• •
mMMm
jmm
Figure 1. The contrasts between task and control are illustrated with the number of
subjects and scans per contrast and the experiments from which the subjects were
recruited. /?, rest Ff, false font; L, letters; Ps, pseudowords; W, words.
threshold was adjusted to Z = 3.0,/) < O.OO1 to protect from false
positives (Bailey et al., 1991a). The results were displayed in the standard anatomical space of Talairach and Tournoux (1989).
Figure 1 shows the comparisons that were made, with the number of subjects and scans for each comparison. Although subjects
were recruited across experiments for certain comparisons, such
comparisons were only made when each subject had performed both
the activation and control tasks. No intergroup comparisons were
made because of the inherent reduction in sensitivity.
Results
Analyses of the reaction times to the feature detection task
were based on the mean response of each subject for each
condition. Responses to false font stimuli were found to be
significantly faster than to word stimuli, but there were no
significant differences between responses to words, consonant letter strings, or pseudoword stimuli. Eight subjects performed the task on both word and false font stimuli (four
from experiment 1 and four from experiment 2); mean responses were 462 msec for false font and 531 msec for words
rX7) = 8.2,^> < 0.001]. Ten subjects performed the task on
both word and consonant letter strings (four from experiment 2 and six from experiment 3); mean responses were
542 msec for words and 530 msec for letters [/(9) = 1-92,^
= 0.09]- Six subjects performed the task on both word and
pseudowords (experiment 3); mean responses were 557 msec
for words and 569 msec for pseudowords [f(5) = 1.6, p =
0.17].
The faster responses to the false font stimuli may be because the false font ascenders were slightly more distinctive
than those in letters. The implications of this are that there
may be more activity associated with the feature detection
task in the stimuli composed of letters than the stimuli composed of false font. However, since there was no significant
difference in the reaction times to consonant letter stings,
64 Implicit Processing of Words and Pseudowords • Price et al.
Midbrain'
Lateral geniculate nuclei
Thalamus'
Data are the location coordinates and Z scores for the areas of peak activity for the contrasts false
font - rest and words - rest The location coordinates are according to the stereotactjc adas of
Talariach and Tournoux 11388) and reported in the order x ( - is left, + is right), y (— is posterior to
the anterior commissure line, + is anterior to the anterior commissure line), z [ - is inferior to the
intercommissural line (AC-PC line), + is superior to the AC-PC line] and the associated Z score, which
is printed in boldface.
• Peak close to midline—separate left and right peaks not resolved.
pseudowords, and words, contrasts between these conditions
should only reflect activity associated with •word processing.
Activation associated with the feature detection task, letter
processing, word processing, and pseudoword processing will
be presented, in turn, followed by presentation of the deactivation associated with •word processing.
Activation Associated with Explicit Task of
Feature Detection
The areas of the brain that were recruited for the visual feature detection task with the finger-press response were identified by contrasting the conditions when subjects performed
the task with the conditions when subjects were resting with
their eyes closed (see Table 1). Retinal projections to the lateral geniculate nuclei and to midbrain structures were reflected in peaks in these areas. No separate peaks in the striate
cortex were identified, but there was extensive bilateral activity in the extrastriate cortex lateral to the cuneus, which
peaked in the posterior fusiform gyri •with a separate peak in
the posterior lingual gyrus. In both hemispheres, there was
activation of the midfusiform gyri (on the ventral surface of
the temporal and occipital lobes) and the junction of the posterior parietal and occipital lobes (see Fig. 2). The separation
of projections from striate and prestriate cortex into two
streams, ventral and dorsal, which serve different functions,
has recently been reviewed by Goodale and Milner (1992);
feature detection in arrays of letters or letter-like symbols
seems to activate both these streams.
The thalami were activated, possibly in the dorsomedial
nuclei, although the spatial resolution of the technique prohibits precision about the precise region. Thefinger-pressresponse -with the right hand was associated with a left senso-
Feature detection task
False font - Rest
Word processing
Words — False font
Word processing
Words - Letters
Pseudoword processing
Pseudowords — Letters
Word deoctivations
Letters - words
Figure 2. The regions where there were significant changes in cerebral blood flow during feature detection, word processing, and pseudoword processing are illustrated in white
on green models of the left and right hemispheres of the brain.
rimotor signal that merged with a left anterior parietal lobe
signal, but became apparent at about 56 mm above the intercommissural line.
Areas that were only activated in the word condition were
located in the ventral part of the left middle temporal gyrus
and the junction of the left inferior frontal and precentral gyri
(Brodmann's area 44/6). For false font, there was activity in
the dorsal part of the right middle temporal gyrus that was
not present for words.
Activation Associated with Implicit Letter Processing
The areas of the brain recruited during presentation of letters
were identified by contrasting the conditions when subjects
performed the feature detection task on consonant letter
Cerebral Cortex Jan/Feb 1996, V 6 N 1
Table 2
Activity associated with letter processing
Table 3
Activity associated with word processing
Coordinates of peak and Z score:
Letters - false font
Location
Location
Inferior/middle frontal junction
Middle frontal gyrus
Words - false font
Words - letters
Cortical
Cortical
Posterior fusiform gyrus
Middle fusiform gyms
Extrastriate cortex
Deep inferior parietal lobe
Coordinates of peak and Z score
Left
Left
Left
Left
Right
Right
Right
-30,-76.-12
-34, -50, - 1 2
-28, -30, + 4
-36, -34, +28
+32, -56, +36
+38,+46,0
+36, +34, +32
U
11
17
13
10
18
10
Data are the location coordinates and Z scores for the areas of peak activity for the contrasts letters
- falsefont. For details see Table 1 note.
strings (which have no semantic or phonological associations) with the conditions when the same subjects performed
the feature detection task on false font. The results are shown
in Table 2. Three areas became active for letters that were
not active for the false font — rest comparison (Table 1); these
were located in the right prefrontal cortex (two peaks) and
the right parieto-occipital junction. However, letters also resulted in significantly greater activity than false font in the left
posterior fusiform gyrus, the left lateral extrastriate cortex
throughout the inferior occipital gyrus, the left anterior fusiform gyrus, and deep in the left anterior parietal lobe.
Activation Associated with Implicit Word Processing
Direct comparison of words with false font and consonant
letter strings were made to reveal whether words that have
both phonological and semantic associations produced activation of language areas even when subjects were engaged
in a nonlinguistic task. Data for the contrast words — false
font were from the eight subjects in experiments 1 and 2;
data for the contrast •words — consonant letter strings were
from the 10 subjects in experiments 2 and 3- These comparisons will be more sensitive than the results of the words —
rest and false font — rest contrasts shown in Table 1 because
(1) there were at least twice as many scans involved (see Fig.
1), and (2) analysis of the data did not include the rest condition during which intersubject variability may be high, as
subjects are free to attend to random thoughts. The results
are detailed and illustrated in Table 3 and Figure 2. They demonstrate involvement of the cuneus (extrastriate cortex), the
left posterior temporal lobe, the left inferior parietal lobe, and
the left inferior frontal gyrus, which strongly suggests implicit
word processing.
There were also mesial frontal activations. The cingulate
gyral loci were quite widely separated in the two contrasts,
possibly because of the different demands of the feature detection task in the two control states (reaction times to the
ascenders in false font were faster than to the ascenders in
all the other stimuli; see above). A small mesial premotor activation was just apparent in words — false font. This was
associated with the activation in the left primary sensorimotor cortex close to the insula (where the muscles of articulation are represented) and more dorsally, close to the motor
representation for muscles of expiration (Ramsay et al.,
1993)—voluntary control of expiration is important in articulation. In the comparison of words with letters, there was
also primary sensorimotor activation, which was bilateral and
close to the representation for muscles of expiration. During
die scans the subjects were not asked to articulate the word
stimuli, but the primary sensorimotor activations would suggest subvocal articulation during visual presentation of word
stimuli (Price et al., 1994).
66 Implicit Processing of Words and Pscudowords • Price et al.
Cuneus'
Middle/inferior temporal
junction
Middle/superior temporal
junction
Superior temporal/inferior
parietal junction
Posterior parietal/
occipital junction
Primary sensorimotor cortex
Inferior frontal gyrus
Inferior frontal premotor
junction (44/6)
Middle frontal gyrus (91
Anterior cingulate gyrus'
Premotor cortex (6)
Subcortical
Thalamus*
Subthalamus
Lentiform nucleus
Left
Left
Right
Left
Left
Right
Left
Left
Right
Left
Left
Right
-10,-96,0
4J)
- 2 , - 9 0 , +8
-48,-42.-12
-48,-18,-4
+44,-28,0
15
U
16
-46,-36,-8
-34, -56, +36
+44.-56, +40
-50, - 8 , +8
-52, - 8 , +32
U
14
16
11
-38.+20,+12
6J
-48, +8, +32
+36, +32, +32
5J
4.1
4i
11
0,-10,+28
+2,+12,+6
Right
Left
-8, -8, +16
+24,-14,-4
-14,-30,0
17
-34. - 4 2 , +20
18
-46,-10,+48
+44,-16,+48
-42, +28, +20
11
tO
a
-40, +4, +28
4J
+12.+16.+40
14
IS
4.4
4J
Data are the location coordinates and Z scores for the areas of peak activity for the contrasts letters
- falsefont and words - letters. For details see Table 1 note.
• Peak close to midline—separate left and right peaks not resolved.
The contrast of words with false font also revealed activity
in thalamic and subthalamic regions and in areas of the right
temporal lobe, the right parieto-occipital junction, and the
right middle frontal gyrus diat •were not identified when
words were contrasted with consonant letter strings. Activity
in the right middle frontal gyrus and the right parietal-occipital junction was also identified when consonant letter strings
were contrasted with false font, consistent with these areas
being equally activated by words and letters.
The precise location of peak activity within each region,
in particular, activity in the parietal lobes, does not correspond exactly between die different groups of subjects. We
believe this discrepancy is most likely to be due to individual
differences in subject anatomy, which could not be accommodated by the stereotactic normalization procedure (see
Steinmetz and Seitz, 1991, for a review of die problem of
individual variability in neuroimaging of language processes).
This hypothesis is currendy being investigated in a further
study in which each subject is treated as an individual, widi
coregistration of functional activity detected by PET with die
individual's MRI. It is also possible that since we are measuring differences in word processing while subjects are involved in an explicit task, diere will be variability in die extent to which implicit word processing proceeds.
The areas associated widi word processing in die present
study correspond to diose associated with word processing
in the Price et al. (1994) study when subjects "passively"
viewed words presented for 981 or 150 msec. The Price et
al. (1994) study demonstrated diat activity in die frontal and
temporal cortices was more extensive during 150 msec exposure durations than during 981 msec. In the present study,
subjects were engaged in die feature detection task for less
than 600 msec, leaving approximately 400 msec for "passive"
word viewing; die increased activity associated widi words in
die left frontal and temporal cortices under these conditions
was more extensive dian during silent viewing with 981 msec
Table 4
Table 5
Activity associated with pseudowords
Deactivations associated with words
Coordinates of peak and / score
Coordinates of peak and I score
Location
Cortical
Posterior fusiform/lingual junction
Pseudowords - letters Pseudowords - words Words - pseudowords
Middle occipital gyrus
Right
Posterior lingual gyrus
Right
+42, -70, +4
4.1
+12,-52.+4
12
+30,-38,+16
+38,-38,+28
18
14
+40, -54, +28
+38,-16,+24
+38, +2, +16
+28, +48, +24
+16,+38,-12
15
4.8
17
16
14
+ 10,+56,+24
+ 14,+26,+56
13
14
-12, -54, +24
14
+6.+2.+12
+2,-16,-4
3.7
13
Inferior/middle temporal juncRight
Medial temporal lobe Left
Inferior temporal gy- Left
Right
ms
Middle temporal gy- Left
Right
rus
Superior
temporal/
inferior
parietal
junction
Left
Anterior inferior insula Right
Orbital frontal cortex
Letters - words
Cortical
Cuneus-
+28,-88,-12
3.7
- 4 , -96, +8
+2, -86, +28
12
19
-18,-16,-12
15
+24, -94, - 4
+32, -78, - 4
4.6
17
tion
Right
+52,-56,-4
17
Superior temporal/inferior parietal junction
Deep inferior parietal lobe
Right
Right
Posterior parietal/occipital
-20,-16,-12
10
junction
Anterior parietal operculum
-46,-52,-12
+48, -62, - 8
6.4
18
-44, -26, - 8
+56,-46,0
14
11
+48, -62. - 4
+50,-50,-12
14
11
Posterior frontal operculum
Middle/superior frontal cortex
Medial superior frontal gyrus
+54, -44, +4
16
Right
Right
Right
Right
Right
Right
Right
Right
Anterior cingulate gyrus
Posterior cingulate gyrus
Precuneus
-30, -40, +24
6.0
+26,+10,-12
12
-24, -42, +28
+ 14,+44, +32
+12,+54,+24
4.1
+4, +38, +8
-12,-64,+16
-2.-62,+40
13
4.0
19
a
5.6
Subcortical
Caudate nucleus
Midbrain
Left
-22, +24, - 8
3.4
Mi(4,J|a | _ . _
Miouie trontal gyrus
False font - words
Location
Right
+16,+2,+16
13
Data are the location coordinates and Z scores for the areas of significant decreases for the contrasts
words versus false font and words versus letters. For details see Table
Left
-42. +34, +24
U
-26, +46, +28
1 note.
4.1
Data are the location coordinates and Z scores for the areas of peak activity for the contrasts pseudowords - letters, pseudowords - words, and words - pseudowords. For details see Table 1 note.
• Peak close to midline—separate left and right peaks not resolved.
exposure durations in the Price et al.(1994) study. The greater
activity in the left frontal and temporal regions in association
with word processing with the feature detection task may
relate to the reduction in time available to view the words
"passively" (see Price et al., 1994). The feature detection task
may also help the subjects to attend to the stimuli.
Activation Associated with Presentation of
Pseudowords
The areas of the brain recruited during presentation of pseudowords in contrast to consonant letter strings (experiment
3) are detailed in Table 4 (Pseudowords - letters). Although
pseudowords (e.g., floop, peesh, rennid, ryfer) are pronounceable, they have no associated meaning. Nevertheless, in this
contrast, the anterior and posterior regions associated •with
word processing were found to be active. Furthermore, in
many areas, there was more activity associated with pseudowords than with real words evident from direct comparisons
between pseudowords and words (Table 4, Pseudowords —
words). For pseudowords compared to words there was additional activity in posterior regions with peaks in the extrastriate cortex, left and right temporal regions, and the left inferior parietal lobe. For words compared with pseudowords,
there was some additional activity in anterior regions, which
peaked in the left inferior and middle frontal gyri (Table 4,
Words — pseudowords).
Deactivations Associated with Word Processing
Table 5 shows the reversed comparisons to Table 3 in order
to show the areas of the brain where there were decreases
in activity during word presentation in contrast to false font
and consonant letter strings. These deactivations are particularly interesting because they are largely confined to the right
hemisphere. In particular, the right middle temporal, inferior
parietal, and middle frontal regions, which increased in the
word — false font contrast but not in the words - letters
contrast (see Table 3), are shown to be less active for words
than for consonant letter strings (see also Fig. 2). We also
know that the right middle frontal gyrus and the right inferior
parietal lobe are significantly more active for letter strings
than for false font (see Table 2), and that pseudowords activated the right extrastriate and temporal cortices more than
words (Table 4). Over experiments, these results demonstrate
that regions in the right hemisphere are more active for letters than words, and false font, more active for pseudowords
than for words and more active for words than false font.
Discussion
Several new results have emerged from this study. First, we
have demonstrated that even when subjects are engaged in a
nonlinguistic task, the mere presence of words in the visual
field can activate a widespread network of language areas in
the left hemisphere. Second, this network of language areas
is also activated by die presence of pseudowords, suggesting
that even though pseudowords have no stored semantic representation, they engage much the same brain areas as real
words. Third, the results show that while a network of language areas in the left hemisphere are activated, a corresponding network in the right hemisphere is deactivated by -word
stimuli in contrast to nonword letter strings. The implications
of each of these results will be discussed in turn.
Activation of the Left Hemisphere Language Network
In this study, subjects were instructed to perform a simple
visual feature detection task on word and nonword stimuli.
The only variable between scans was the type of stimulus on
which they performed the task. We are therefore measuring
differences in processing functions that are unrelated to the
explicit task. The results have shown highly significant differences in the distribution of blood flow when subjects were
performing the explicit task on words and pseudowords relative to consonant letter strings and false fonts.
Cerebral Cortex Jan/Feb 1996, V 6 N 1 67
Words and pseudowords activated the medial extrastriate
cortex, the left posterior temporal cortex, the left inferior parietal cortex, and the left prefrontal cortex. These areas are
known to be related to visual and auditory word processing
from (1) previous PET studies that explicitly activated semantic and phonological processes (e.g., Petersen et al., 1988,
1990; Wise et al., 1991; Demonet et al., 1992; Howard et al.,
1992; Price et al., 1994), and (2) lesion studies on patients
with specific language deficits (for reviews on this subject,
see Ellis and Young, 1988; Shallice, 1988; MacCarthy and Warrington, 1989; Mesulam, 1990).
The activation of the language network even when subjects are engaged in a nonlinguistic task is consistent with
psychological studies that have demonstrated that visual
word processing is obligatory to the extent that it can interfere with the explicit task a subject is asked to perform (e.g.,
Lupker, 1985; Van Orden et al., 1988;Macleod, 1991;Coltheart
et al., 1994). The classic demonstration of obligatory word
processing is the Stroop effect, but many "priming" studies
have shown that even when subjects are unaware of a visually
presented word the occurrence of the word influences explicit semantic and phonological processing of subsequendy
presented words (e.g., Marcel, 1983; Humphreys et al., 1987;
Neely, 1991). We cannot confirm from the present experimental design whether some subjects deliberately read the
words while performing the feature detection task or whether the observed activity we detected •when words •were presented was entirely a consequence of obligatory word processing. Although the different degrees of regional activation
across experiments suggests that the subjects may have responded in different ways, the overall results show that language areas are engaged even when the task does not necessitate their involvement. Such implicit word processing means
that the subcomponents of language will not necessarily be
revealed by contrasting word tasks that selectively engage a
component to tasks where the component is activated implicitly. This applies particularly to a contrast such as reading
aloud versus reading silently, in which it might be assumed
that reading aloud requires retrieval of phonological representations but reading silently does not; if subjects retrieve
phonological representations even when viewing words silendy, comparison of the conditions will not isolate areas related to phonological retrieval. To some degree, this problem
can be overcome by selecting tasks that weight processing
heavily to a particular component (e.g., Demonet et al., 1992;
Zatorre et al., 1992). However, these complex monitoring
tasks encounter a different problem in that the tasks, instructions, attentional demands, and strategies employed by the
subjects cannot necessarily be kept constant across conditions and therefore the additional variables will influence differences in brain activity between conditions.
Interpretation of Differences in Activity Related to
Processing Real Words and Pseudowords
The network of language areas activated by real words was
also activated by pseudowords in comparison to consonant
letter strings and in all regions except the left prefrontal cortex, activity was greater during presentation of pseudowords
than during presentation of words—in other words, pseudowords activate the language network more strongly than
words. In particular, presentation of pseudowords generated
significantly more activity than words deep in the left inferior
parietal cortex, a finding that is consistent with several studies
that have shown that activity in the left inferior parietal cortex is associated with phonological tasks. For instance, Law et
al. (1991) found significantly greater activity in the left inferior
parietal cortex when Japanese subjects were reading Kana
words than when they were reading Kanji words. This result
68 Implicit Processing of Words and Pseudowords • Price et al.
indicated that regions within the left inferior parietal cortex
were dedicated to phonological recoding because Kana
words—like pseudowords—rely on translation of their characters into the corresponding phonological code. The coordinates of this region are similar to the region that Paulesu et
al. (1993) associated with the phonological store in a visualverbal short-term memory task.
Although most areas of the language network detected in
die present study were activated more by pseudowords than
real words, two areas within the left prefrontal cortex were
more active for words than for pseudowords. Petersen et al.
(1990) also found an active inferior frontal region during "passive" viewing of words but not during "passive" viewing of
pseudowords. They associated diis area with semantic processing of real words, and supportive evidence from neuropsychological studies was given, which suggested that semantic priming tasks are preferentially affected by frontal lesions
(Milberg et al., 1987; Sartori et al., 1987).
We have attempted to identify the functions of brain
regions that are differentially activated by the different stimuli
according to the hypothesis that a direct comparison of
words and pseudowords should reveal the area of the brain
associated with semantic processing because real words have
specific semantic associations but pseudowords do not (Petersen et al., 1990). However,diis hypothesis does not explain
why we found that most brain areas were more active in die
presence of pseudowords than words. A possibility is that
pseudowords activate semantic representations more strongly
than real words because a more prolonged search for the
"missing" representations occurs. Similarly, pseudowords may
activate phonological processes more strongly than real
words because the phonological associations are unfamiliar
and therefore less readily retrieved. The dilemma is whether
we are measuring activity associated with accessing stored
representations or activity associated with a search for missing representations. Connectionist models of word processing, for example, the interactive activation model of word processing proposed by McClelland and Rumelhart (1981),
would predict that passive presentation of pseudowords will
create more activity in the word recognition network than
familiar words. McClelland and Rumelhart (1981) argued diat
activation of feature, letter, and •word representations does not
occur in a discrete fashion within the hierarchy. As features
are extracted activation accumulates simultaneously for letters and words consistent with the input. Active word and
letter representations inhibit competing responses at all levels
of the hierarchy until the system converges on a single interpretation. For pseudowords, the system will take longer to
converge on an interpretation because there are no connections to specific representations; dierefore, there "will be more
activity in the network due to less inhibition of competing
responses.
Right Hemisphere Activity
Activity in regions of the right hemisphere that are homologous to those associated with die left hemisphere language
network was detected when words and consonant letter
strings were contrasted to false font (see Tables 2, 3). However, when words were contrasted to letters and pseudowords, right hemisphere regions were significandy more active for letters and pseudowords dian real words (Tables 4,
5). Overall, right hemisphere regions were most active for
letters, widi progressively decreasing activity for pseudowords, followed by words and least activity for false font. One
possible explanation for diese results is tihat die degree of
right hemisphere activity is inversely related to the ease with
which word associations are accessed. Another possibility is
that a right hemisphere language network is initially activated
by the presence of letters but inhibited by the computation
of word associations. Further studies that investigate these
hypotheses directly are required.
Conclusions
Our results have shown that when subjects are asked to perform a simple task on word stimuli processing of the word
beyond that required for the task occurs. A consequence of
this finding is that the anatomical region associated with a
function of interest will not necessarily be revealed by contrasting brain activity in tasks that explicitly activate a specified function with tasks where the function is not required
explicitly but activated implicitly. The second difficulty we
face when interpreting blood flow differences between passive presentation of words and pseudowords is whether relative increases in activity are related to the ability of words
to access their stored representations or the inability of pseudowords to find stored representations. These issues can be
resolved to some extent by using paradigms that actively engage subjects in attention-demanding tasks. However, as the
task becomes more demanding, subjects may adopt internal
strategies that have little to do with normal everyday processing of language stimuli. Ultimately, our knowledge of the
functions of different language areas will depend on acquiring
and collating data from several different approaches.
Notes
Cathy Price was funded by the McDonnell Pew Program, Grant 9123, and the Stroke Association. Our thanks to Chris Frith, Karalyn
Patterson, David Howard, Elizabeth Warburton, and Eraldo Paulesu for
their helpful contributions to this article, to Graham Lewington and
the radiochemists at the MRC Cyclotron Unit for their help in performing the studies, and to Ruth Ellis and Brian Wharton for their
help in recruiting normal volunteers.
Address correspondence to Dr. Cathy Price, Wellcome Department of Cognitive Neurology, Institute of Neurology, Queen Square,
London WC1N 3BG, UK.
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