Electrophysiological Measures of Language Processing in Bilinguals
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Electrophysiological Measures of Language Processing
in Bilinguals
Alice Mado Proverbio1, Barbara Čok2, and Alberto Zani3
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Abstract
& The aim of the present study was to investigate how activation of the same areas for Italian words, which was also
multiple languages are represented in the human brain. Event- displayed by topographical mapping. In monolinguals, seman-
related brain potentials (ERPs) were recorded from right- tic error produced a long-lasting negative response (N2 and N4)
handed polyglots and monolinguals during a task involving that was greater over the right hemisphere, whereas syntactic
silent reading. The participants in the experiment were nine error activated mostly the left hemisphere. Conversely, in the
Italian monolinguals and nine Italian/Slovenian bilinguals of a bilinguals, semantic incongruence resulted in greater response
Slovenian minority in Trieste; the bilinguals, highly fluent in over the left hemisphere than over the right. In this group, the
both languages, had spoken both languages since birth. The P615 syntactical error responses were of equal amplitude on
stimuli were terminal words that would correctly complete a both hemispheres for Italian words and greater on the right
short, meaningful, previously shown sentence, or else were side for Slovenian words.
semantically or syntactically incorrect. The task consisted in The present findings support the view that there are inter-
deciding whether the sentences were well formed or not, giving and intrahemispheric brain activation asymmetries when
the response by pressing a button. Both groups read the same monolingual and bilingual speakers comprehend written
set of 200 Italian sentences to compare the linguistic process- language. The fact that the bilingual speakers in the present
ing, while the bilinguals also received a set of 200 Slovenian study were highly fluent and had acquired both languages in
sentences, comparable in complexity and length, to compare early infancy suggests that the brain activation patterns do not
the processing of the two languages within the group. For the depend on the age of acquisition or the fluency level, as in the
bilinguals, the ERP results revealed a strong, left-sided case of late, not-so-proficient L2 language learners, but on the
activation, reflected by the N1 component, of the occipito- functional organization of the bilinguals’ brain due to poly-
temporal regions dedicated to orthographic processing, with a glotism and based on brain plasticity. &
latency of about 150 msec for Slovenian words, but bilateral
INTRODUCTION
unilateralized electroconvulsive therapy. The authors
The study examines the neurofunctional mechanisms of described a lateralization of semantic functions to the
linguistic comprehension in monolingual and bilingual right hemisphere for L1 and to the left hemisphere for
speakers engaged in the processing of well-formed or L2, while syntactic functions were lateralized to the left
incongruent sentences in Italian and Slovenian. More hemisphere for both languages. A differential lateraliza-
specifically, the aim of the study was to investigate tion of multiple languages has also been reported for
whether the two cerebral hemispheres of monolingual professional interpreters (Fabbro, Gran, Basso, & Bava,
and polyglot people process orthographic, semantic, 1990; Fabbro & Daró, 1995; Fabbro, Gran, & Gran,
and syntactic aspects of written language differentially. 1991). However, the pattern of lateralization in these
In fact, while it is generally acknowledged that the right individuals is complicated by an asymmetric use of the
hemisphere has limited capabilities in syntactic process- ears for listening to the linguistic material to be translated
ing and a higher involvement in semantic processing in during their professional commitments. In fact, they have
monolinguals, there is evidence that hemispheric later- the habit of listening to the source language with the left
alization of linguistic functions is different in polyglots. ear (right hemisphere), taking off the right earphone in
Chernigovskaya, Balonov, and Deglin (1983) showed order to leave the right ear (left hemisphere) free to
a different lateralization of semantic and syntactic monitor their own verbal performance (Gran, 1989).
structures for the first language (L1) and the second Indeed, in a behavioral study (Fabbro et al., 1991)
(L2) in a bilingual psychiatric patient treated with involving a dichotic listening task simulating a simulta-
neous interpretation performance, professional simulta-
1
University of Milano-Bicocca, 2University of Trieste, 3National neous interpreters showed a significant right-ear
Research Council (CNR), Italy superiority in recognizing semantic errors in L1, and
D 2002 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 14:7, pp. 994 – 1017
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syntactic errors in L2, while they showed left-ear superi- development (in adulthood), the areas of activation of
ority in recognizing semantic errors in L2 and syntactic the two languages appear to be distributed slightly
errors in L1. Based on these studies, the conclusion differently. Perani et al. (1996) used positron emission
might be drawn that linguistic functions tend to be tomography (PET) to study brain activity in adults
more differentially lateralized in polyglot brains than in listening to stories in their native language (L1), in a
monolingual. second language acquired after the age of 7 (L2), and in
Clinical cases of polyglot aphasia have also suggested an unknown third language (L3). They found that
that the linguistic representation of L1 and L2 in poly- several areas, similar to those already observed in mono-
glots might involve separate neurofunctional circuits, linguals, were activated by L1 but not by L2. These
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and/or be caused by a dysfunction of a putative switch- results demonstrated the great importance of early
ing mechanism between the languages. This assumption exposure to the maternal language in shaping linguistic
is based on evidence that after the insult polyglot areas of the brain. However, in a later study (Perani
patients may selectively recover one language while et al., 1998), the same authors demonstrated another
showing severe aphasic symptoms for the other lan- important dimension in determining cortical represen-
guage. However, lesion data have provided a rather tation of languages in polyglots to be the proficiency
complex pattern of results, including a selective recovery level of a given language, regardless of acquisition age.
of the language learned earlier in life or the one spoken They evaluated the effect of early and late acquisition of
most frequently (Paradis, 1989), as well as a pathological L2 in highly proficient bilinguals testing a group of
mixing of the languages (Abutalebi, Miozzo, & Cappa, Italian/English bilinguals who had acquired L2 after the
2000; Aglioti, Beltramello, Girardi, & Fabbro, 1996; age of 10 years (high proficiency, late acquisition bilin-
Aglioti & Fabbro, 1993). guals) and a group of Spanish/Catalan bilinguals who
In general, although the role of the right hemisphere had acquired L2 before the age of 4 years (high profi-
in bilinguals’ language processing remains controversial, ciency, early acquisition bilinguals). Failing to find any
there is a great deal of evidence supporting a differential difference in the cortical response of volunteers listening
intrahemispheric representation for monolingual and to stories in L1 and L2, Perani et al. (1998) ascribed the
bilingual speakers. For example, Dehaene et al. (1997) difference between the data of that study and those of
used fMRI to assess intersubject variability in the cortical their earlier study (Perani et al., 1996) to the low
representation of language comprehension in moder- proficiency level attained by the late acquisition bilin-
ately fluent French/English bilinguals while they listened guals in the previous PET study. On the basis of these
to stories in the two languages. They found that while data, they also concluded that attained proficiency is
the first language (L1) activated a similar set of areas in more important than age of acquisition as a determinant
the left temporal lobe in all subjects, the second lan- of the cortical representation of L2.
guage (L2) activated a highly variable network of the left Linguistic processing in bilinguals has also been inves-
and right temporal and frontal areas, with individual tigated by event-related potentials (ERPs) of the brain.
subjects varying from a standard left lateralization to Indeed, ERPs are very useful tools to study the neural
a complete right hemispheric lateralization. However, basis of language comprehension, as they provide
another fMRI study (Illes et al., 1999) described a differ- information on the temporal course of information
ent pattern of results with fluent English/Spanish bilin- processing neural flow in different semantic and mor-
guals who acquired their second language years after phosyntactic tasks. In fact, ERP studies on language (see
acquiring their first language. In this study, no differ- Federmeier, Kluender, & Kutas, 2002, for a recent review;
ences in brain activation were found across groups for Kutas & Van Petten, 1994; Kutas & Hillyard, 1980) have
semantic analysis of the two languages. shown that semantic integration is reflected by the N400
A further important dimension related to bilingualism component, a centro-parietal negativity with a latency of
and polyglotism is the age of acquisition of a given around 400 msec very sensitive to word cloze probability.
language, this leading to considerable variation in the On the other hand, phrase structure assignment and
pattern of brain activation for native and second lan- syntactic integration are assumed to be reflected by an
guages. The fMRI findings of Kim, Relkin, Lee, and early left anterior negativity (ELAN) with a latency of
Hirsch (1997) indicate that while the language-sensitive about 100 – 300 msec, a left anterior negativity (LAN) with
regions of the temporal lobe (Wernicke’s area) show a latency of about 300 –500 msec, and a late centro-
little or no difference in activity based on the age of parietal positivity (P600), also called syntactic positive
language acquisition, those of the frontal lobe (Broca’s shift (Friederici, Steinhauer, & Frisch, 1999; Hahne &
area) show a differential activation as a function of the Friederici, 1999; Münte, Heinze, Matzke, Wieringa, &
age of acquisition of the second language. When the Johannes, 1998; Osterhout & Holcomb, 1992, 1993).
second language is acquired during early language The ELAN is reported to reflect a first-pass parsing
development, the native and second languages tend to process and to be very sensitive to word category, being
be represented in common frontal cortical areas, where- guided by phrase structure rules. The later negativity
as when they are acquired at a later stage of linguistic (LAN), overlapping in time with semantic N400, reflects
Proverbio, Čok, and Zani 995
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morphosyntactic analysis while the late positivity reflects and bilingual groups could be ascribed solely to poly-
relatively controlled language-related processes (Hahne glotism, and not to acquisition age or proficiency level.
& Friederici, 1999) sensitive to inflectional information The aim of the present investigation was manifold.
(Gunter & Friederici, 1999) and is associated with sec- First of all, we wanted to study the neurolinguistic
ondary syntactic processes such as sentence reanalysis organization of brain structures by comparing the ERP
and repair (Friederici, 1997) and processes inhibiting response of ‘‘early’’ (or ‘‘infant’’) bilinguals with that
incorrect representation due to difficulty with syntactic of monolinguals, both tested in the same language
integration (Kaan, Harris, Gibson, & Holcomb, 2000). (Italian). Secondly, our aim was to compare the spatio-
Few ERP studies have investigated the neurofunc- temporal activation of brain areas in bilinguals during
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tional differences in linguistic semantic and syntactic the reading and comprehension of two different
processing in bilinguals. The ERP study by Fischler, languages, both acquired precociously (Italian and
Boaz, McGovern, and Ransdell (1987), where the N400 Slovenian) and of a high proficiency level. Thirdly, we
component was measured in English/Spanish bilinguals investigated possible inter- and intrahemispheric differ-
during a semantic decision task, failed to find any cross- ences in brain activation during word processing as a
linguistic effect of semantic priming. The study revealed function of the specific word (violation) type, namely
a reduction in N400 amplitude for within-language ‘‘correct,’’ ‘‘semantically incorrect,’’ and ‘‘semantically
repetitions, but no effect for the cross-language repeti- and syntactically incorrect.’’ On the basis of previous
tions. In other words, the prior repetition of a word in a literature data, we hypothesized a difference in the
given language (for instance, English) failed to influence specific role of the two cerebral hemispheres and of
the processing of its Spanish translation, thus support- the anterior and posterior language-sensitive brain areas
ing the view of two independent lexical stores. This in the processing of first and second languages. As the
result fits in neatly with the differential pattern of primary aim of the study was to compare how a bilingual
bilingual brain activation in semantic violation studies brain processes words belonging to two different lan-
on the N400 component. Meuter, Donald, and Ardal guages, also comparing it with a monolingual brain
(1987) found that N400 was greater over the left parietal subjected to an identical stimulus, we did not adopt
sites than over the right for the second language (L2) of the classical paradigm of the presentation of sentences
French/English speakers, while it was bilaterally sym- known as rapid serial visual presentation (RSVP), which
metrical for their first language (L1). Ardal, Donald, would have allowed a more specific study to be made of
Meuter, Muldrew, and Luce (1990) examined different the semantic and syntactic aspects of linguistic process-
groups of bilinguals of different native languages— ing (of noncritical words also). Given our different aim,
French, English, Chinese, Spanish, and Korean—finding the study called for a paradigm that would satisfy, as far
N400 to be greater over the right parietal side in as possible, the need to control, and balance perfectly
monolinguals and over the left side in bilinguals. In a within groups and conditions, a series of linguistic
more recent study, Weber-Fox and Neville (1996) inves- factors related only to terminal words on which the
tigated the influence of bilingual proficiency on hemi- electroencephalogram (EEG) was time-locked for the
spheric lateralization of linguistic brain areas, testing a purposes of ERP averaging.
large sample of Chinese/English bilinguals who had been The present study set out to achieve an insight into the
exposed to English at different stages of their develop- spatio-temporal activation, indexed by ERP components,
ment. The test involved only the English language, not of the two cerebral hemispheres in bilinguals and mono-
Chinese. The authors found a delay in N400 latency for linguals during the processing of Italian and Slovenian.
bilinguals exposed to English after the age of 10, but no Both languages are phonologically transparent, Slove-
differences in the amplitude or topography of N400 on nian being more complex than Italian at the morphosyn-
comparing bi- and monolinguals. tactic level due to its being a highly inflected language.
In the present experiment, ERPs and reaction times
(RTs) were recorded in two groups of young monolin-
guals and Italian/Slovenian bilinguals. The subjects had RESULTS
to decide on the correctness of visually presented short
sentences. All the participants in the study were highly Behavioral Results
fluent in Italian, and the bilinguals were also very fluent Overall, the RTs were much faster for the monolingual
in Slovenian, being for the most part university students group (675 msec) than the bilingual (Italian 759 msec,
belonging to the Slovenian minority living near the Slovenian 726 msec).
Italian/Slovenian border, having Italian nationality, and
attending the Italian University in Trieste. Some taught
Reaction Times
Italian in Slovenian schools. Thus, all the bilinguals had
an excellent command of both languages and a high Monolinguals/Bilinguals—Italian. The analysis of var-
proficiency level. Because of this, we hypothesized that iance (ANOVA) on mean RTs to Italian terminal words
any difference in the brain activation of the monolingual confirmed the difference in response speed between the
996 Journal of Cognitive Neuroscience Volume 14, Number 7
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Table 1. ANOVA Significance for Each Statistical Comparison In addition, the interaction of Word type Language and
Performed on Behavioral Data post hoc comparisons indicated that the RTs to correct
and syntactically incorrect words were faster ( p < .01) in
Data Factors df F p
the Slovenian condition (correct = 704 msec, syntacti-
Monolinguals/bilinguals—Italian cally incorrect = 702 msec) than the Italian condition
RTs Group 1,12 5.58
indicated a lower percentage of correct recognition of Electrophysiological Results
semantic error than of syntactic error and correct words.
For each subject, electrode, and hemispheric sites, distinct
The double interaction of Word type Language proved
ERP averages were computed as a function of the linguistic
that the bilinguals recognized a higher percentage of
group (monolinguals and bilinguals), the language (Italian
semantic errors in the Italian language, and a higher
and Slovenian), and the word type (correct, semantically
percentage of syntactic errors in the Slovenian language,
incorrect, or syntactically incorrect). Moreover, ANOVA
whereas there was no difference between the two
was applied to each ERP component, with the factors and
languages for correct words (see Figure 2). The ANOVA
levels being described in the Methods section.
also yielded a significance of Word type Language
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Hand. The bilinguals in the Italian language produced
the highest percentage of correct categorization for
N1 Component
syntactic error using the right hand while the worst
performance produced with the same hand was for Monolinguals/Bilinguals—Italian. The ANOVA, per-
semantic error ( p < .05). In the Slovenian language, formed on the N1 mean area values (recorded at F34,
they produced the highest percentage of correct cate- C34, P34, T56, and O12 sites between 140 and 200 msec),
gorization for syntactic error using the left hand, while revealed an electrode effect indicating greater N1 ampli-
the worst performance produced with the same hand tudes at the posterior temporal and occipital sites for
was for semantic error ( p < .01). both linguistic groups (see Table 2 for statistical signifi-
An analysis of correct response showed a preference cance). The Electrode Hemisphere significant interac-
for the left hand by the monolingual group in Italian tion showed greater N1 response at the left hemispheric
and by the bilingual group for Slovenian, the bilingual posterior temporal and occipital sites. Although there was
showing, instead, preference for the right hand in the a tendency in that direction (monolinguals: left hemi-
Italian language. Consistent with this was the RT anal- sphere = 2.63, right hemisphere = 0.39; bilinguals:
ysis for the bilingual group: It showed a left-hand left hemisphere = 2.19, right hemisphere = 1.79), no
preference for the Slovenian language and no hand significant effect of group per se or in interaction with the
preference for Italian. These data could be interpreted hemisphere was found at this latency level.
in the light of the so-called interference hypothesis that
hypothesizes that if the hemisphere controlling the Bilinguals—Slovenian/Italian. The ANOVA performed
two-choice (index/medium finger) motor response is on the bilingual group revealed a significant effect of
also involved in linguistic processes, the performance is language due to the greater N1 response to Italian words
worse than if there is no involvement (e.g., Waldie & ( 2 AV) than to Slovenian ( 0.97 AV). The ANOVA also
Mosley, 2000). Thus, favoring the left-hand would reveal showed an effect of electrode. As in the preceding
a left hemisphere involvement in linguistic processing, analysis, the post hoc comparisons indicated greater
whereas favoring the right would reveal right hemi- N1 amplitude at the posterior temporal and occipital
sphere involvement. sites. This amplitude proved to be greater over the left
BILINGUALS MONOLINGUALS
100 100
COR
SEM
SYN
95 95
90 90
HITs (%)
85
HITs (%)
85
80 80
75 75
70 70
ITALIAN SLOVENIAN ITALIAN
R Hand L Hand R Hand L Hand R Hand L Hand
Figure 2. Percentages of correct categorizations obtained for the two linguistic groups to Italian and Slovenian terminal words as a function of
word type and response hand.
998 Journal of Cognitive Neuroscience Volume 14, Number 7
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Table 2. ANOVA Significance for Each Statistical Comparison Performed on ERP Data
ERP Component Factors df F p value
Monolinguals/bilinguals—Italian
N1 Electrode 4,48 21.4
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Figure 3. Topographical maps of brain activation recorded in bilinguals during processing of Slovenian (left) and Italian (right) material at N1
latency level. Worth noting is the statistically significant greater involvement of the right occipital site for the Italian than Slovenian language,
pointed out by the red circle.
C34, P34, T56, and O12 sites between 200 and 340 msec) incorrect terminal words than for correct ones. Indeed,
revealed a significant effect for the Electrode factor. N2 to syntactic error ( 0.67 AV) was significantly bigger
Both groups had a negative peak that reached its than N2 to semantic error ( 0.49 AV, p < .05) or correct
maximum amplitude at the posterior temporal and words (+0.36 AV, p < .01). Between-groups ANOVA also
occipital sites. At this latency, the first effect of word showed an interaction of Word type Hemisphere
type appeared, such effect being greater negativity for Group. Relative post hoc comparisons (N2 in Table 3)
Table 3. N2 Mean Amplitude Values (with Standard Errors) Recorded at Left and Right Hemispheric Sites as a Function of
Linguistic Group and Word Type
Language Correct Semantic Syntactic
Group Left Right Left Right Left Right
Monolingual 0.41 (0.63) 0.97 (0.67) 0.09 (0.64) 0.1 (0.64) 0.66 (0.56) 0.38 (0.53)
Bilingual 0.09 (0.55) 0.14 (0.54) 1.12 (0.61) 0.81 (0.60) 0.75 (0.50) 0.86 (0.50)
1000 Journal of Cognitive Neuroscience Volume 14, Number 7
Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/089892902320474463 by guest on 19 September 2021indicated that, in monolinguals, semantic error pro- in the bilinguals, the pattern is almost inverted for the
duced a greater negative response over the right hemi- Slovenian language (Figure 4d); no other response was
sphere than over the left (Figure 4a), whereas syntactic evident in the latter group for Italian. Post hoc compar-
error mostly activated the left hemisphere (Figure 4b). isons also showed that the bilingual N2 response to
The difference maps (Figure 5) show the topographical semantic incongruence was of greater amplitude in the
distribution of the enhanced negativity to semantic and left hemisphere than in the right (Figure 4c and e).
semantic + syntactic error within this latency range. The
syntactic – semantic difference map series (Figure 5, Bilinguals—Slovenian/Italian. The within-group
right) shows the topography of the additional negativity ANOVA on bilinguals also revealed a significant electrode
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in response to terminal words that are also syntactically effect, indicating greater N2 amplitudes at the posterior
incongruous. This negativity is distributed more over the temporal and occipital sites. The interaction of Language
left temporal area than the right in monolinguals, while Hemisphere showed that, as for the N1 component,
Figure 4. Grand-averaged ERP
waveforms recorded at the left
and right side of the frontal,
lateral frontal, central, posterior
temporal, and occipital areas
of monolingual and bilingual
individuals as a function of
language presented. ERPs to
correct (solid line) and
semantically (A, C, and E) or
syntactically (B, D, and F)
incongruent (dashed line)
terminal words are overlapping.
The shaded areas illustrate the
response of linguistic brain
regions to semantic and/or
syntactic violations in the
N2 (light gray) and N400
(dark gray) latency range.
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Figure 4. (continued )
N2 to Slovenian terminal words was much greater at the at F34, C34, P34, T56, and O12 sites between 340 and
left recording sites ( 0.27 AV) than the right (+0.47 AV) 540 msec) revealed an electrode effect, with N4 being
( p < .05), no significant asymmetry emerging for greater at the posterior temporal and occipital sites. The
response to Italian words (left hemisphere = 0.71, ANOVA also revealed an effect of hemisphere, with the
right hemisphere = 0.57 AV). In addition, the post N4 component being much greater over the right hemi-
hoc tests indicated greater N2 response to Italian sphere ( 0.56 AV) than over the left (+0.49 AV). Elec-
words than to Slovenian words over the right hemi- trode Hemisphere interaction also proved significant.
sphere ( p < .01). Post hoc comparisons indicated greater amplitudes of
the N4 component at the right posterior temporal and
occipital sites. The significant factor word type indicated
N4 Component
much higher N4 values to semantic error ( 1.11 AV)
Monolinguals/bilinguals—Italian. Between-groups than to syntactic ( 0.79 AV) and to both error types
ANOVA performed on N4 mean area values (measured than to correct words (1.79 AV).
1002 Journal of Cognitive Neuroscience Volume 14, Number 7
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Figure 4. (continued )
Bilinguals—Slovenian/Italian. The ANOVA performed greater for semantic error than for syntactic, while in
on the N4 values of the bilingual group for Italian and Italian there was no difference in N4 for these errors
Slovenian revealed the significance of the electrode (Figure 6). Furthermore, for both semantic and syntactic
effect, showing almost the same pattern of results as errors, the N4 response differed significantly as a func-
for the homologous split-plot ANOVA. tion of language, being more negative for Italian terminal
The significant effect of word type indicated greater N4 words than for Slovenian (see maps in Figure 7). The
response to semantic error ( 1.78 AV) than to syntactic difference maps (Figure 7) show the topographical dis-
( 0.85 AV) and to both error types than to correct words tribution of the N400 response to semantic error, dis-
( 0.69 AV). The interaction of Word type Language, playing a mainly centro-parietal distribution as described
F(2,12) = 4.49, p < .035, also proved significant. Post hoc in the literature, but with hemispheric asymmetries
comparisons showed that in Slovenian N4 was much involving the temporal and frontal areas.
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Figure 5. Temporal series of difference maps of brain activation obtained by subtracting ERP responses to congruent words from ERP responses
to syntactically incongruent words (on the left) and subtracting ERP responses to semantically incongruent words from ERPs to syntactically
incongruent words (on the right). The goal was to somehow isolate the semantic component from the syntactic one in the combined
syntactic + semantic violation condition. The blue areas indicate the scalp distribution of N2 response to the incongruence of the terminal
word recorded in the monolingual and bilingual people examined.
P600 Component than at the anterior, this being supported also by the
significant Electrode factor. In addition, the P600 values
Monolinguals/bilinguals—Italian. The between-groups
were greater for syntactic error (4.54 AV) than for
ANOVA performed on the P600 values recorded at the
semantic error (3.33 AV, p < .01) and correct words
lateral frontal (F78) and posterior temporal electrodes
(3.98 AV, p < .05), as indicated by the word type factor.
(T56), between 540 and 680 msec poststimulus, indi-
cated a much greater component at the posterior sites
Bilinguals—Slovenian/Italian. ANOVA performed for
the bilingual group as a function of language showed
the electrode effect with P600 as being much greater at
1
the lateral frontal site than at the posterior temporal.
0.5
Again, word type turned out to be significant, with P600
N400 to syntactic error (3.76 AV) being much greater than
0 the responses to other word types (semantic error =
Amplitude(µV)
Correct 1.79 AV; correct = 2.86 AV). The interaction of Word
-0.5 Sem err Type Hemisphere, F(2,6) = 3.555, p = .06, almost
Synt err reached significance as, overall, the greater amplitude of
-1
P600 to syntactic errors, rather than to other stimulus
-1.5
types, was much more pronounced in the left hemi-
spheric sites. However, the significant interaction of
-2 Language Electrode Word Type in the bilinguals
revealed this positive deflection to be observed only at
-2.5 the posterior temporal sites for Slovenian syntactically
ITALIAN SLOVENIAN incorrect words, not for Italian syntactically incorrect
words (see waveforms in Figure 4d and maps in Figure 8).
Figure 6. N400 mean amplitude values recorded at left and right
hemispheric sites in response to Italian and Slovenian words in the
bilingual group, as a function of word type. Note the differential DISCUSSION
response to syntactically, as opposed to semantically, incongruent
Slovenian words, a response that was absent for Italian terminal The study investigated whether linguistic comprehen-
words. sion activates the same brain areas at different stages of
1004 Journal of Cognitive Neuroscience Volume 14, Number 7
Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/089892902320474463 by guest on 19 September 2021Figure 7. Temporal series
of difference maps of brain
activation obtained by
subtracting ERP responses to
correct words from those to
semantically incongruent
words. The blue areas indicate
the scalp distribution of N400
response to semantic
incongruence recorded in the
monolingual and bilingual
people examined.
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word processing in monolinguals and bilinguals; this was monolinguals were presented with a set of 200 Italian
done by recording ERPs to correct or incorrect terminal sentences; the bilinguals were presented the same set of
words while the participants were engaged in deciding Italian sentences together with a different set of 200
word appropriateness for the whole sentence. The Slovenian sentences of comparable difficulty.
Figure 8. Temporal series
of difference maps of brain
activation obtained by
subtracting ERP responses to
correct words from those to
syntactically incongruent words.
The red areas indicate the scalp
distribution of P600 response
to syntactical incongruence
recorded in the monolingual
and bilingual people examined.
Proverbio, Čok, and Zani 1005
Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/089892902320474463 by guest on 19 September 2021In general, the bilinguals turned out to be slower than occipital and occipito-temporal cortices during ortho-
the monolinguals in responding to linguistic stimuli, graphic processing of single words, the so-called word
regardless of the language. Such a finding has already form system (Petersen, Fox, Posner, Mintun, & Raichle,
been described in the literature (Green, 1986) and was 1988), that is specifically sensitive to real fonts as
interpreted in relation to a possibly different neurofunc- opposed to false fonts. In the present study, and con-
tional organization of linguistic functions in polyglots. sistent with the above findings, the occipito-temporal
scalp sites, which might reflect the activation of brain
areas underneath, showed a bilateral response in the N1
Between-Groups Differences in Hemispheric
latency range (about 160– 180 msec poststimulus) dur-
Lateralization: Hand Preference
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ing the processing of Italian words and a left-sided
Analyses of correct response revealed a left-hand prefer- response during Slovenian word processing in the bilin-
ence in the monolinguals in responding to Italian words guals. In our view, this indicates that the word form
and in the bilinguals responding to Slovenian words, system might be able to discriminate between different
plus, for the bilinguals, a preference for the right hand in languages on the basis of orthographical analysis at very
responding to Italian words. These findings might be early stages of visual processing. In polyglots, this early
explained in the light of the so-called interference detection would enable the reader to address the
hypothesis advanced on the basis of behavioral studies. specific knowledge proper to a given language (i.e.,
According to it, the percentage of correct responses and graphemic/phonemic conversion rules, lexicon, etc.) in
the speed of response are higher when the hemisphere order to comprehend the material.
mainly involved in a given task is not also engaged in
controlling contralateral motor response. Therefore, a
Semantic and Syntactic Processing in
left-hand advantage in performing a motor response to
Monolinguals
lateralized stimuli would reveal left-hemisphere predom-
inance in linguistic processing, whereas a right-hand Analyses of later ERP potentials revealed the onset of
advantage would reveal right hemisphere involvement. negative responses (N2 and N400) to incongruent
According to this hypothesis, our data indicate a greater words as early as 200 msec, followed by a later positivity
involvement of the left hemisphere in monolingual (P600), such responses being differentially sensitive to
linguistic processing, whereas in the bilinguals, the left the semantic and syntactic aspects of the word process-
hemisphere would be dominant for Slovenian material ing as it progressed over time. The responses were also
and the right hemisphere for Italian. In line with this differentially distributed over the frontal and occipito-
interpretation, the bilingual group showed faster RTs to temporal electrode sites of the two hemispheres as a
Slovenian words for the left hand, whereas in respond- function of the linguistic group and languages (see
ing to Italian words, no hand preference was found. waveforms in Figure 9 for a comparison of conditions).
Overall, the behavioral data suggest a greater involve- In monolinguals, the N2 at the posterior temporal and
ment of the right hemisphere in the linguistic processing occipital electrode sites was greater for incorrect termi-
of Italian (compared to Slovenian) in apparently highly nal words than for correct terminal words and especially
fluent Slovenian/Italian bilinguals, suggesting a possible so for words with syntactic error rather than semantic
‘‘preference’’ for Slovenian (L1) as the mother tongue. It error. It is worth noting that this increased negativity
is very important to note that this preference did not was right-sided for semantic error and left-sided for
produce overall faster RTs for L1 than for L2, but was syntactic error. In the following temporal window, the
subtly revealed in the electrophysiological responses, for negativity became strongly lateralized to the right hemi-
example, by very small or absent N400 or P600 to sphere, and greater for semantic error than for syntactic
syntactically incongruent Italian words. and for both types of error than for correct words.
Difference maps obtained by subtracting the area of
brain activation to semantically incongruent words from
Orthographic Analysis
that of correct words showed that the effect had a
As a whole, the ERP data also indicate the presence of centro-parietal source, with an important involvement
strong inter- and intrahemispheric differences in the of the right temporal and frontal sites (see maps in
timing and topography of brain responses as a function Figure 7). These findings are consistent with electro-
of linguistic group and language (L1 and L2). Among the physiological literature that reports, for monolingual
differences, there appears in the bilinguals an involve- speakers, an involvement of the right hemisphere in
ment of the right lateral occipital area in the ortho- semantic processing and, possibly, in N400 generation
graphic analysis of Italian words, as reflected at the scalp (Kiefer, Weisbrod, Kern, Maier, & Spitzer, 1998; Hagoort,
by the topographical distribution of the early-latency N1 Brown, & Swaab, 1996; Kutas, Hillyard, & Gazzaniga,
component. In this regard, neuroimaging studies (see 1988; Kutas, Van Patten, & Besson, 1988; Kutas & Hill-
the review by Fiez and Petersen, 1998, on monolinguals; yard, 1982). Other studies have provided evidence of
Polk et al., 2002) have described a left-sided activation of N400 bilateral generation in the anterior temporal lobe
1006 Journal of Cognitive Neuroscience Volume 14, Number 7
Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/089892902320474463 by guest on 19 September 2021Figure 9. Grand-averaged ERP
waveforms recorded at left
and right posterior temporal
electrode sites in the two groups
of people and for the two
languages, as a function of
terminal word correctness. The
shaded areas illustrate the brain
response to semantic and
syntactic violations at the N2/N4
and P600 levels.
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(McCarthy, Nobre, Bentin, & Spencer, 1995; Nobre & words from that to syntactically incongruent words
McCarthy, 1995). In these studies, intracranial electrodes between 200 and 340 msec poststimulus showed that
were used to record field potentials while the subjects the effect involved the left temporal and occipital areas in
viewed sentences that could end either normally or monolinguals, whereas it was more anteriorly distributed
with a semantically anomalous word. The anomalous and right-sided in bilinguals (see maps in Figure 5). The
sentence-ending words elicited a large negative field present results are quite consistent with recent neuro-
potential with a peak latency, near 400 msec, focally imaging findings in the literature (Dehaene et al., 1997).
distributed bilaterally in the anterior medial temporal In our view, this lends support to the robustness of our
lobe, anterior to the hippocampus, and near the amyg- topographical inferences, despite the ERP limitations in
dala. The authors advanced the hypothesis that the neural source localization. This pattern of almost in-
most likely neural generator of this field potential might verted hemispheric lateralization is also supported by
be in the region of the collateral sulcus and anterior the significant hand preference factor, as emerges from
fusiform gyrus. The data are in good agreement with the the RT data. The findings suggest that the overall pattern
distribution of negativity to semantically incongruent of brain activation and hand preference shown by the
words that we found in our ERP study, the maximum bilinguals for Slovenian is very similar to that of the
amplitude being at the lateral occipital/temporal scalp monolingual Italian group.
sites. However, the subtraction of the ERP to congruent In general, both linguistic groups were slower in
words from the ERP to semantically incongruent words responding to semantic error than to syntactic error.
resulted in a centro-parietal distribution, with some right This could be interpreted as a sign that the semantic
frontal and right temporal involvement in monolinguals. incongruence was more difficult to detect than the
Unfortunately, because of ERP limitations in source syntactic one, the latter being more redundant in a
localization, it is difficult to ascertain whether this way as it includes also a word type error. Interestingly,
scalp-recorded neural activity reflects the activation of although the bilinguals were much slower in responding
underlying cortical areas. to semantic error (in Italian) with the left hand (right
hemisphere), they were much faster with the same hand
in responding to syntactic error. Such data might be
Semantic and Syntactic Processing in Bilinguals
interpreted as a sign that the semantic system for L2,
Significantly, the bilinguals showed a left-sided lateraliza- whose activity was reflected at the scalp by negativity to
tion of negativity between 200 and 340 msec poststimu- semantic error, was not actually strictly right-sided, just
lus for semantic error. In addition, the N2 component to as syntactic ability was not left-sided. This assumption is
Slovenian terminal words in this group was, on the supported by other electrophysiological studies that
whole, much larger at the left sites, while there was no provide evidence of a differential lateralization for
significant asymmetry for the response to Italian words. N400 in monolinguals versus bilinguals (Ardal et al.,
In the N4 latency range, negative response to word 1990; Fischler et al., 1987; Meuter et al., 1987).
incongruence became much greater over the right hemi- Still, one reason for doubting this assumption is due to
spheric sites. It is worth noting that in the bilinguals N4 the ERP findings of the study by Weber-Fox and Neville
was sensitive to syntactic violations in Slovenian, but not (1996) who took bilingual proficiency into account, such
in Italian. Consistently, P600 was almost absent for Italian proficiency being strongly influenced by the age of
syntactic violation. The difference maps obtained by acquisition of L2 and able to modify the functional
subtracting brain activation to semantically incongruent organization and the possible hemispheric lateralization
Proverbio, Čok, and Zani 1007
Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/089892902320474463 by guest on 19 September 2021of linguistic brain areas. They, as already noted above, In agreement with behavioral data, the ERPs provided
examined a large sample of Chinese/English bilinguals evidence of a differential processing of the two lan-
exposed to English at different stages of their develop- guages, apart from the marked differences in topo-
ment and found no difference in the amplitude or top- graphic distribution and hemispheric lateralization.
ography of N400 in bilinguals compared to monolinguals, Indeed, the differences were mainly related to the
although they did find that the latency of N400 was syntactic violation responses. In the range of N400, this
delayed for bilinguals exposed to English after the age component for Slovenian was greater for syntactic vio-
of 10. However, in our opinion, these findings alone lations than for semantic ones, while it was of the same
are not sufficient to discard the aforementioned assump- amplitude for Italian. In the latency range of P600 for
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tion as being untrue. Indeed, a possible explanation for Italian, there was no syntactic violation response at the
this lack of difference could be that the individuals posterior temporal site, while there was response at the
exposed to English very early in life (especially at 1– 3 lateral frontal sites. These findings might imply that
and 4– 6 years) were not very fluent in Chinese, having despite our efforts to balance the two groups of speak-
used this language very little, both at school and at home. ers with regard to fluency, proficiency, age and modality
In these individuals, the learning of Chinese, although of acquisition, and daily exposure to the two languages,
from an early age, was modest and approximate and, as there might still be some very subtle, hard-wired, differ-
such, did not justify functional bilingualism. Conversely, ences in the linguistic proficiency of the two groups.
their knowledge of English was excellent, especially in Alternatively, one could advance the intriguing hypoth-
reading and writing, as was evidenced in the N400 to esis that some of the between-groups discrepancies
English sentences, their N400 results differing very little discussed above could be ascribed to differences in
from those of native English speakers. the structural properties of the two languages, these
Unlike Weber-Fox and Neville’s (1996) study, the having totally different syntactic constructions. Indeed
bilinguals in our study had a profound knowledge of Slovenian is a richly inflected language, unlike Italian
both Slovenian and Italian, having learned them con- and, even more so, English. There are no articles and
temporarily and at a very early age in the same social– nouns, adjectives and pronouns are inflected for three
emotional context. Thus, we can conclude that our data numbers, three genders, and six cases. Verbs are also
indicate that the knowledge and fluent use of more than inflected for number, gender, and case, and differ by
one language is reflected in a differential activation of means of affixes, suffixes, and a particle placed between
distinct brain regions devoted to linguistic processing in the verb root and the end. Thus, it cannot be excluded a
polyglots, there being no such differentiation in mono- priori that these features, which make the syntactic
linguals. The specific pattern of cerebral activation con- analysis of Slovenian somehow qualitatively different
cerns all stages of the processing of single words from that of Italian, might be partly responsible for
(orthographic, semantic, and syntactic stages). The the bilinguals’ different brain responses to syntactic
present results are from early, highly proficient, fluent violations in Italian and Slovenian.
bilinguals, and thus indicate that the specific pattern of
brain activation observed in this study is not the result of
a late defective neurofunctional organization (as in the METHODS
case of late, low proficiency learners).
Participants
Nine Italian monolinguals (four men and five women,
Bilingual Proficiency
mean age 27 years) and nine Italian/Slovenian bilinguals
As for possible differences in the bilinguals’ proficiency (four men and five women, mean age 29 years) parti-
in Italian and Slovenian, the RTs did not show any cipated in this experiment as volunteers. They had
significant difference in response times to semantically normal or corrected-to-normal vision and were right-
anomalous words. Still, in this group there was evidence handed with a right-eye dominance. The participants in
of a significant advantage of Slovenian over Italian in the two groups were of comparable educational level
responding to correct words (46 msec faster) or syntac- and social status. The bilinguals had all acquired Italian
tic violations (50 msec faster). On the other hand, the and Slovenian in early infancy (since birth) and were
accuracy analysis showed a mixed pattern of results: no very fluent in both languages. All the participants in the
difference between the two languages in the correct study lived in Italian territory (on the outskirts of
response percentages, faster and more accurate report- Trieste) right at the border with Slovenia and either
ing of semantic violations in Italian and syntactic viola- the mother or father of the bilinguals belonged to the
tions in Slovenian. All in all, our findings seem to suggest Italian or Slovenian linguistic cultures. According to
that, although very tiny, there might have been a certain neurolinguistic literature, the bilinguals tested in the
‘‘preference’’ in the bilinguals for the Slovenian language present investigation can be classified as ‘‘early com-
(L1) especially as far as the responses to syntactic pound’’ bilinguals as they grew up in bilingual families
violations were concerned. and acquired both languages before the age of 5 in the
1008 Journal of Cognitive Neuroscience Volume 14, Number 7
Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/089892902320474463 by guest on 19 September 2021of the sentence and terminal word. Both the monolin-
gual group and the bilingual one were shown 200
sentences in the Italian language. The bilingual group
was shown a further 200 sentences in the Slovenian
language, the sentences having been carefully balanced
with the Italian sentences for sentence length (see
Figure 10) and syntactic complexity. Terminal words
were accurately balanced for length, number of syllables,
frequency of use, and concreteness/abstractness. For the
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Italian language, word frequency of use was controlled
by evaluating the scores reported in Bortolini, Tagliavini,
& Zampolli (1971) and De Mauro, Mancini, Vedovelli, &
Voghera (1993). The overall linguistic complexity of the
sentences was balanced by presenting a larger initial set
of stimuli to a sample of 20 Italian and Slovenian speak-
ers, asking them to evaluate the difficulty encountered
in assessing the correctness of each phrase on a seven-
point scale. The results of this preliminary test allowed
Figure 10. Number of words/sentences in the two languages.
Sentences and terminal word length was balanced across languages
us to select Italian and Slovenian sentences of compara-
and word types. ble difficulty (see Figure 11). Each set of stimuli included
100 correct, 50 semantically incorrect, and 50 syntacti-
cally and semantically incorrect sentences. They were
same social– emotional context (Genesee et al., 1978). randomly presented in short sequences of 3-min dura-
To test bilingual proficiency, we engaged the partici- tion, preceded by three 500-msec warning stimuli
pants in a standard preliminary conversation in front of (‘‘ready,’’ ‘‘set,’’ ‘‘go’’). After the ‘‘go’’ stimuli, an inter-
a native Italian and a native Slovenian experimenter who stimulus interval of 1500 msec allowed the observer to
found no significant difference in oral production in carefully adjust his/her gaze on the fixation point, wait-
either Italian or Slovenian for these individuals. Further- ing for the first sentence to be presented. Each sentence
more, all the bilinguals were asked to self-rate their stayed on the screen for 1500 msec and was followed by
comfort in reading, comprehending, and writing both an interstimulus interval that varied randomly between
languages. In addition, for reading and written produc- 350 and 500 msec during which the screen was dark with
tion, no significant differences emerged for the two the exception of the fixation point. This was followed
languages in the examined bilingual sample (N = 9). immediately by the terminal word, which stayed on the
Because of problems related to EEG techniques (exces-
sive muscular and/or ocular artifacts), two bilingual and
two monolingual individuals were excluded from the
initial sample, and their EEG traces were rejected before
ERP averaging.
Materials and Procedure
The target stimuli were terminal words that could
correctly complete a previously shown short meaningful
sentence, or else words that were semantically and/or
syntactically incorrect. The syntactical incongruence
consisted of a phrase structure violation achieved by a
word type error (see Appendices 1 and 2 for a complete
list of stimuli).
The sentences, presented visually on a high-resolution
PC monitor, were white on a black background and were
displayed in easily readable large-size capital letters,
appearing in one or two short lines centered on the
foveal region. The longest sentence subtended a visual
angle of about 128 and 30 in. in length and 28 and 30 in.
Figure 11. Distribution of the frequency with which the various
in height. A small yellow cross (4 mm in size) was located sentences in the two languages were judged as relatively difficult
at the center of the screen and served as a fixation point (i.e., relative difficulty in assessing their correctness) from a preliminary
in order to minimize eye movement during the reading sample of 20 Italian and Slovenian mother-tongue subjects.
Proverbio, Čok, and Zani 1009
Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/089892902320474463 by guest on 19 September 2021screen for 250 msec. The intertrial interval was of associated with incorrect behavioral response was also
1500-msec duration. The order of experimental sessions excluded from further analysis. For each subject, distinct
(Italian or Slovenian) for bilingual participants was coun- ERP averages were obtained as a function of group and
terbalanced across subjects. Except for a few cases, the stimulus category. More specifically, ERP averages were
two sessions took place on different days, so that session computed in response to correct, semantically incorrect,
duration was similar to that of the monolingual subjects. and syntactically incorrect Italian words for monolinguals
The participants sat in a dimly lit, acoustically shielded and to correct, semantically incorrect, and syntactically
cubicle facing a window that looked out on a high- incorrect words both in Italian and Slovenian for Bilin-
resolution VGA computer screen 114 cm from their guals. The major ERP components were identified and
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eyes. The participants were instructed to fixate the measured automatically by a computer program with
center of the screen and avoid any eye or body move- reference to baseline voltage averages lying in the range
ment during the recording session. The task consisted in of 100 to 0 msec. The ERP components were quantified
deciding the correctness of terminal words in relation to by measuring peak latency and mean area amplitude
the previously read incomplete sentence, and in press- values within a specific latency range centered approx-
ing a button (alternatively with the left or right hand) imately on the peak latency of the deflection observed in
with the index finger in response to words judged the grand average waveforms. The N1, N2, and N4
correct and the medium finger to words judged incor- negative deflections were all larger at occipito-temporal
rect. This allowed the recording and measuring of the sites and peaked at about 160, 245, and 425 msec,
speed and accuracy of response, respectively, RTs and respectively. They were quantified by computing the
percentage of correct responses. The order of hands to mean area in the time windows between 140 and 200,
be used and of trials (different sets of sentences) was 200 and 340, and 340 and 540 msec at both posterior
randomized within and across subjects. (O1, O2, T5, T6, P3, and P4) and anterior (F3, F4, C3, and
C4) electrode sites. While the N400 per se was greater at
the posterior sites, the brain response to semantic
Electrophysiological Recording
violation (the difference between semantic violation
The EEG was recorded continuously from 28 scalp sites and correct word) had a more central and anterior
using tin electrodes mounted on an elastic cap (Electro- distribution. The P600 component, peaking at about
cap). The electrodes were located at frontal (Fp1, Fp2, 605 msec, was greater at the central and frontal midline
FZ, F3, F4, F7, and F8), central (CZ, C3, and C4), sites, but showed considerable functional differences in
temporal (T3 and T4), posterior temporal (T5 and T6), hemispheric distribution. It was therefore quantified in
parietal (PZ, P3, and P4), and occipital scalp sites (O1 and the time window between 540 and 680 msec at posterior
O2) of the International 10 –20 System. Additional elec- temporal (T56) and lateral frontal (F78) sites.
trodes were placed halfway between homologous ante-
rior temporal and central sites (FTC1 and FTC2), central
Data Analysis
and parietal sites (CP1 and CP2), anterior temporal and
parietal sites (TCP1 and TCP2), posterior temporal and For each subject, RTs faster than 140 msec and exceed-
occipital sites (OL and OR), and left and right occipital ing the mean ± 2 standard deviations were excluded
sites (OZ). To ensure that fixation was maintained, the from the statistical analysis. Both RTs and error percen-
horizontal and vertical oculograms (EOG) were also tages were computed for the various stimulus categories
recorded. Vertical eye movements were recorded by (correct, semantically incorrect, or syntactically incorrect
means of two electrodes placed below and above the in Italian and Slovenian).
right eye, whereas horizontal movements were recorded Two main types of statistical comparisons were per-
using electrodes placed at the outer canthi of the eyes. formed on ERP and RT measures, allowing direct com-
Linked earlobes served as the reference lead. The EOG parison of the monolinguals and bilinguals in processing
and the EEG were amplified with a half-amplitude band Italian sentences (monolinguals/bilinguals—Italian) and
pass of 0.1 –70 and 0.01 –70 Hz, respectively. Electrode between the processing of Italian and Slovenian senten-
impedance was kept below 5 k . Continuous EEG and ces in the bilingual individuals (bilinguals—Slovenian/
EOG were digitized at a rate of 512 samples/sec. Italian).
Any trial contaminated by eye or body movement was
rejected. Computerized artifact rejection was performed
Monolinguals/Bilinguals—Italian
before averaging to discard epochs in which eye move-
ment, blinking, excessive muscle potentials, or amplifier Behavioral response (i.e., mean RTs and percentages of
blocking occurred. The artifact rejection criterion con- correct responses) recorded to Italian words was ana-
sisted of peak-to-peak amplitude exceeding ±50 AV. The lyzed by three-way ANOVAs whose factors of variability
artifact rejection rate was about 5%. The ERPs were were 1 between groups (monolingual or bilingual) and 2
averaged offline from 100 msec before to 1000 msec within groups (word type: correct, semantically incor-
after presentation of terminal words; any ERP trial rect, and syntactically; response hand: left and right).
1010 Journal of Cognitive Neuroscience Volume 14, Number 7
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