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International Journal of Multilingualism, 2014

Vol. 11, No. 2, 182201, http://dx.doi.org/10.1080/14790718.2013.791298

Multilingual processing in the brain


Maurits van den Noorta,b*, Esli Struysa, Kayoung Kimc,d, Peggy Bosche,
Katrien Mondta, Rosalinde van Kralingenf, Mikyoung Leeg and Piet van de Craena
a
Department of Linguistics, Vrije Universiteit Brussel, Brussels, Belgium; bResearch Group of
Pain and Neuroscience, Kyung Hee University, Seoul, Republic of Korea; cDepartment of
Psychology, Texas A&M University, College Station, TX, USA; dHarvard Graduate School of
Education, Harvard University, Cambridge, MA, USA; eDonders Centre for Cognition, Radboud
University Nijmegen, Nijmegen, The Netherlands; fDanone, Wageningen, The Netherlands;
g
Munich Center of the Learning Sciences, University of Munich, Munich, Germany
(Received 31 May 2010; final version received 22 March 2013)

In this paper, in contrast to previous neuroimaging literature reviews on first


language (L1) and second language (L2), the focus was only on neuroimaging
studies that were directly conducted on multilingual participants. In total, 14
neuroimaging studies were included in our study such as 10 functional magnetic
resonance imaging, 1 positron emission tomography, 2 magneto encephalography
and 1 electroencephalography. Surprisingly, not many neuroimaging studies have
been conducted on multilingual participants to date. As a result, most
conclusions that are drawn about multilingual processing are in fact solely based
on bilingual processing. Moreover, the few multilingual studies that were
conducted frequently showed serious methodological flaws, often due to the
practical limitations in terms of accessing a large homogeneous multilingual
group. In future research, more multilingual neuroimaging studies are needed, in
which factors such as language proficiency, age and manner of acquisition,
language exposure and linguistic distance between the spoken languages, are
better controlled for. Currently, these factors can explain away a large part of the
differences that are found in brain activation between L1, L2 and L3. Finally,
there is a need for more sophisticated neuroimaging techniques in order to
capture non-invasive activity.
Keywords: multilingualism; fMRI; PET; MEG; EEG

Introduction
The ability of the human brain to acquire, process and use more than one language is
a biologically based ability (Bosch & Sebastián-Gallés, 2001). It is, among other
things, important for education purposes to better understand how the human brain
processes and acquires multiple languages, since this knowledge can be used in the
development of better multilingual education programmes.
In this paper, the interest lies in the question as to what insights neurolinguistic
research on multilingualism has given us so far. The main part of this paper will focus
on multilingual studies that were conducted with neuroimaging techniques. Surpris-
ingly, many claims about third language (L3) processing/acquisition are not directly

*Corresponding author. Email: info@mauritsvandennoort.com

# 2013 Taylor & Francis


International Journal of Multilingualism 183

based upon neurolinguistic studies on multilingual participants, but are indirect


claims based on monolingual and bilingual (neuroimaging) studies.
Therefore, in this paper, in contrast to previous neuroimaging literature reviews,
we will not focus on first language (L1) and second language (L2) neuroimaging
studies (for neuroimaging reviews on L2, see Abutalebi, 2008; Indefrey, 2006; Perani
& Abutalebi, 2005), but will only concentrate on the studies that were directly
conducted on multilingual participants.
One of the most investigated issues in neurolinguistic research on multilingualism
is the so called: ‘language representation’ issue (Fabbro, 2001). This research focuses
on the question of whether different languages are represented in the same brain
areas or are localised in different brain areas (please see clarification Boxes 1 and 2
for a summary of the basic brain anatomy and the localisation of linguistic functions
in the brain; moreover, we refer to an introduction book about neuroanatomy (Nolte,
2008). Before presenting and discussing the most important findings from
neuroimaging studies on multilingual participants, we will first briefly discuss what
has been discovered in neurosurgery, aphasia and cortical stimulation studies
(Giussani, Roux, Lubrano, Gaini, & Bello, 2007).

Box 1. Basic brain anatomy.

The cortex is built up of four major regions: the frontal, temporal, parietal and
occipital lobes. As indicated by its name, the cortex is a folded structure made up
of gyri (sing. gyrus) or ridges, surrounded by sulci (sing. sulcus) or fissures. The
frontal, temporal and parietal lobes are further divided (from bottom to top) into
inferior, middle and superior gyri or sulci. The sides of the cortex are called lateral
parts, closer to the mid-point the medial parts can be found. Sometimes anterior
and posterior are used as synonyms for ‘the front’ and ‘the back’, respectively, of
the brain. The occipital lobe, for example, is the most posterior lobe of the cortex.
Other important regions for language processing such as the basal ganglia and the
cerebellum lie below the cortex lie.

Box 2. Localisation of linguistic functions.

Most essential for understanding the localisation of linguistic functions is the


language centres of Broca and Wernicke. The region of Broca is mainly
responsible for language production, but is also shown to be active during
language comprehension (Caplan, 2006) and grammatical processing (Skipper,
Goldin-Meadow, Nusbaum, & Small, 2007). It is localised in the lower or
inferior part of the frontal lobe in the left hemisphere. Broca’s area can be
found close to the Sylvian sulcus, which separates the frontal lobe from the
temporal lobe. Wernicke’s area can be found in the upper or superior parts of
the temporal lobe and is one of the many cortical regions involved in language
processing (Poeppel, Idsardi, & van Wassenhove, 2008). As both regions border
the Sylvian sulcus, these traditional language regions are often referred to as
the perisylvian language zones.
184 M. van den Noort et al.

Localisation of these two language centres has been established in the nineteenth
centuries by studies on aphasiacs. Modern neuroimaging techniques have further
broadened the view on language localisation in the brain. Activity in the frontal
or temporal lobes is shown not to be restricted to Broca’s or Wernicke’s area,
other zones of these lobes may be involved as well (Jeong et al., 2007; Vingerhoets
et al., 2003). Neuroimaging has shown that other parts of the cortex such as the
parietal and occipital lobes (Pihko, Mäkinen, Nikouline, Mäkelä, & Ilmoniemi,
2001; Pihko, Nikulin, & Ilmoniemi, 2002), subcortical regions such as the basal
ganglia (Booth, Wood, Lu, Houk, & Bitan, 2007; Ullman, 2006) and the
cerebellum (Booth et al., 2007; Mariën, Verhoeven, Engelborghs, Rooker, Pickut,
& De Deyn, 2006) are involved in speech processing. The occipital lobe is located
in the back of the brain and is engaged in all activities involving visual processing,
including reading. The parietal lobe contains the angular and supramarginal
gyrus, which are most relevant to language processing. As these regions lie near
the junction of occipital, parietal and temporal lobes, they combine visual and
auditory information necessary for reading and writing.

Clinical neurolinguistic research


Neurosurgery and cortical stimulation
One of the first methods used to investigate language representation is electro-
cortico-stimulation during brain surgery (Ojemann & Whitaker, 1978; Rapport, Tan,
& Whitaker, 1983). Although most electro-cortico-stimulation studies are on
monolingual and bilingual patients, Bello et al. (2006) conducted a study on seven
late, highly proficient multilingual patients with a left frontal glioma (tumour arising
from glia cells). All patients preoperatively conducted several tests in order to
evaluate oral language production, comprehension and repetition. Language
mapping was conducted during craniotomies on persons who were awake and
participating in a counting and oral naming task. To map activities related to
language processing, an Ojemann cortical stimulator (a device designed to map
cortical stimulation in awake or anaesthetised patients) was used. Furthermore,
subcortical stimulation was conducted with the same experimental tasks and the
same current threshold during tumour resection, in a back and forth fashion, with
the same experimental tasks. Bello et al. (2006) found that the cortical sites that are
known to be related to oral naming were activated in 87.5% of patients whereas the
cortical sites for different languages were distinct and separate. The number and
location of the sites were widely distributed in the cortex around, or in some cases
over, the tumour area. In addition, the subcortical stimulation results showed tracts
for the native language in four patients, and for the later acquired languages in three
patients. Moreover, it was found that in three of these patients their native language
fluency decreased immediately after surgery, fully recovered in two patients and
partially recovered in one patient. The results of the electro-cortico-stimulation by
Bello et al. (2006) are in line with the hypothesis that different languages may be
partially processed in different brain regions.

Aphasia
Other insights with respect to the language representation issue came from the
different recovery patterns observed in multilingual aphasics (e.g. Paradis, 1993,
International Journal of Multilingualism 185

1998, 2001). In these patients, stroke may alter the function of the mother and
foreign languages differently, suggesting that different languages may be processed in
different brain regions.
Neuroimaging research has shown that other regions than the classical language
areas like the prefrontal cortex are active during L2 processing (Miller & Cohen,
2001). The prefrontal cortex is the most anterior part of the frontal lobe, located in
front of Broca’s area. This finding seems to corroborate the idea that different
recovery patterns in aphasia patients may be caused by the fact that L2 processing
requires different brain regions than native tongue processing. More recent research,
however, has laid more emphasis on the role of language control mechanisms in the
selective recovery of language skills in multilingual aphasics (Green & Abutalebi,
2008). According to this interpretation, intriguing patterns of selective recovery do
not necessarily have to refer to distinct neural representations of the different
languages, but could be due to damage in control mechanisms located in the
prefrontal cortex that activate the target language and inhibit the non-target
language (Abutalebi, 2008). This explanation is also more in harmony with the
neuroimaging evidence given in the next paragraph.

Neuroimaging techniques
Over the last three decades, besides patient studies and cortical stimulations studies,
neuroimaging techniques such as functional magnetic resonance imaging (fMRI),
positron emission tomography (PET), magneto encephalography (MEG) and
electroencephalography (EEG) are available for the study of multiple languages in
the brain. With respect to the present paper, it is particularly important to note that
there is no perfect neuroimaging technique. Every technique has its specific
advantages and disadvantages (Halchenko, Hanson, & Pearlmutter, 2005). Two
particularly important factors are the so called ‘temporal resolution’, referring to the
precision of a measurement with respect to time and ‘spatial resolution’ of a
technique, referring to the precision of a measurement with respect to space. Ideally,
researchers want to get information about both ‘when’ and ‘where’ in the brain
language processes are occurring, but presently, no neuroimaging technique exists
with both an excellent temporal and spatial resolution. More specifically, the
temporal resolution of EEG and MEG is good, but the spatial resolution is not,
whereas the spatial resolution of PET and fMRI is good, but the temporal resolution
is not (Andreassi, 2000).
Besides the temporal and spatial resolution, other factors play an important role
for the language researcher in deciding in favour of or against a specific technique.
For instance, there are important differences in the kind of brain responses that a
neuroimaging technique can detect (e.g. MEG yields more superior (cortical)
localisation information compared to EEG, as the magnetic field is unaffected by
tissue conductivity (Helenius, Salmelin, Service, & Connolly, 1999). The haemody-
namic methods, such as PET and fMRI, in contrast to EEG and MEG, measure
indirect neural activity (Tagamets & Horwitz, 2001), where PET can be considered as
a more direct measure of local neural activity than fMRI. Moreover, the invasiveness
of the technique is often considered as a disadvantage of PET compared to non-
invasive techniques such as EEG, MEG and fMRI (Halchenko et al., 2005).
Therefore, for a multilingual researcher the choice of the neuroimaging technique
generally depends on the primary focus of the research question at hand. For
186 M. van den Noort et al.

example, if the research question concerns the timing of language processes in the
brain, EEG or MEG would be appropriate techniques, but if the research question
concerns the location of language processes in the brain (relevant to the language
representation issue), PET and fMRI would be more suitable techniques (van den
Noort et al., 2010). However, in recent years, neuroimaging researchers have tried to
further improve the weaknesses of each neuroimaging technique as well as
developing combinations of techniques such as EEG and fMRI (Eichele et al.,
2005). A more detailed description of the different neuroimaging techniques can be
found in Andreassi (2000).
Previous neuroimaging studies on bilingualism showed inconsistent findings with
respect to the language representation issue. For instance, although in some studies
at least partially separate representations for the L1 and L2 were detected (e.g.
Dehaene et al., 1997; Kim, Relkin, Lee, & Hirsch, 1997; Mondt, 2007; Perani et al.,
1996), other investigations found no support for the hypothesis that the native
language and the second language are organised in distinct brain regions (e.g.
Hasegawa, Carpenter, & Just, 2002; Hernandez, Dapretto, Mazziotta, & Book-
heimer, 2001; Illes et al., 1999; Klein, Milner, Zatorre, Meyer, & Evans, 1995).
Importantly, bilingual neuroimaging studies have found that age of L2 acquisition
(e.g. Kim et al., 1997) and L2 proficiency (e.g. Perani et al., 1998) are major
determinants of L2 cortical representation (see Indefrey, 2006; Perani & Abutalebi,
2005 for recent reviews).
Thus, in the next part of the paper, we question the generalisability of results from
bilingual speakers to those of multilingual speakers. Many claims on multilingual
processing are based on bilingual neuroimaging studies, but are the findings of L2
and L3, especially with regard to language representation in the brain, indeed the
same?

Overview of the neuroimaging findings


This section presents neuroimaging results from 14 studies concerning multi-
lingualism. The results are grouped according to the type of neuroimaging technique,
with 10 fMRI, 1 PET, 2 MEG and 1 EEG studies. The main inclusion criteria were
that the neuroimaging study was a direct study on multilingual participants and was
published in a peer-reviewed scientific journal.

fMRI
As can be seen in Table 1, Yetkin, Yetkin, Haughton, and Cox (1996) were the first to
publish an fMRI study on multilingualism. In their study, five right-handed male
multilingual participants performed a verbal fluency task in three languages. All
participants were fluent in two languages and had studied a third language for 24
years, but the participants did not speak their L3 on a regular basis. The participants
were not comparable with respect to the languages that they spoke: three participants
were native speakers of English, whereas the other two participants were native
speakers of Turkish and Chinese. The foreign languages of investigation in this study
were: English, German, Norwegian, Russian, Japanese, French and Spanish. The
experimental task was a verbal fluency task that was first conducted in the L1, then
in the L2 and finally in the L3. The participant was cued by the investigator with a
letter randomly selected from the alphabet and the participant’s task was to silently
Table 1. Overview of 10 fMRI studies conducted on multilingual participants, with information concerning the study, language of investigation, language
proficiency of the participants, experimental task of investigation, results of the study and critiques regarding the study.

Study/number of Experimental
participants/languagesa Proficiency taskb,c Baseline comparison task Results Critiques

Yetkin et al. (1996)/N = 5/ L1 high, L2 high, Verbal fluency task Rest (1) Left frontal lobe activation (1) There were only
languages: English, L3 fair was found. five participants in
German, Turkish, (2) The largest activation was the study.
Norwegian, Chinese, found for the language in (2) The participants
Russian, Japanese, which the participant was were not
French, Spanish least fluent. comparable with
respect to the
languages spoken.
Pihko et al. (2001)/N = 2/ L1 high, L2 high, Silently counting No control task (1) In all three languages, There were only two
languages: L1 Finnish, L3 poor to fair words in a target activation in the left occipito- participants in the

International Journal of Multilingualism


L2 was either Swedish, language parietal cortex was found. study.
English or Italian, L3 (2) Greater activation in the left
was Italian or Swedishd occipito-parietal cortex was
found for the two foreign
languages.
Wattendorf et al. No information Verbal fluency task Motor task (1) Different coactivation There was no
(2001)/N = 8/languages: about language patterns in Broca’s area for information about
German, Frenche proficiency the three languages were language proficiency.
found.
Vingerhoets et al. L1 high, L2 poor Picture naming Looking at scrambled (1) In all three languages, Note the large range
(2003)/N = 12/languages: to high, L3 poor line drawings without overlapping regions of in foreign language
L1 Dutch, L2 French, L3 to high trying to recognise or activation were found. proficiency.
English search for meaningful (2) Foreign languages recruited
objects additional inferior lateral
and medial frontal regions
predominantly on the left.
(3) More posterior right
hemispheric activation in the
L1.

187
Table 1 (Continued )

188
Study/number of Experimental
participants/languagesa Proficiency taskb,c Baseline comparison task Results Critiques

M. van den Noort et al.


Vingerhoets et al. L1 high, L2 poor Verbal fluency task Silently counting from a (1) In all three languages, Note the large range
(2003)/N = 12/languages: to high, L3 poor given number overlapping regions of in foreign language
L1 Dutch, L2 French, L3 to high activation were found. proficiency.
English (2) Foreign languages elicited
additional bilateral inferior
frontal activation, including
Broca’s area and left middle
temporal gyrus activation.
(3) In the L1, additional
postcentral activation was
found.
Vingerhoets et al. L1 high, L2 poor Comprehension Reading of nonsense (1) In all three languages, Note the large range
(2003)/N = 12/languages: to high, L3 poor reading task texts overlapping regions of in foreign language
L1 Dutch, L2 French, L3 to high activation were found. proficiency.
English (2) In the L1, more activation in
medial posterior regions was
found.
Briellmann et al. L1 high, L2 high, Verbal fluency task Fixating on a cross-hair (1) In all four languages, There are only six
(2004)/N = 6/languages: L3 fair to high, L4 activation was found in participants in the
English, German, poor to fair overlapping brain areas. study.
Italian, French, and (2) The activated volume
Spanish increased for languages in
which a participant had
poorer proficiency.
Jeong et al. (2007)/ N = 30/ L1 high, L2 Auditory sentence Button press after (1) In all three languages, (1) In general,
languages: L1 Korean, intermediate to comprehension listening to a white noise bilateral superior temporal participants
L2 English, L3 Japanese high, L3 stimulus cortex activation was found. learned English
intermediate to (2) For Japanese, the left inferior before they
high frontal gyrus (IFG) was learned Japanese.
additionally activated. (2) Participants spent
(3) For English, additional significantly more
activation was found in the time learning
right cerebellum, the left IFG English.
and the superior frontal gyrus.
Table 1 (Continued )
Study/number of Experimental
participants/languagesa Proficiency taskb,c Baseline comparison task Results Critiques
Bloch et al. (2009)/ N = 44/ L1 high, L2 Language Attention task: joining (1) Participants with early 18 different languages
languages: In total, 18 intermediate to production task together thumb and exposure to L2 showed low were used
different languages were high, L3 forefinger of the variability in brain activation
investigated as L1, L2, intermediate to dominant (right) hand in all three languages, in the
and L3 high when scanning sound was two early as well as the late
perceived learned language
(2) However, for the late
multilinguals higher
variability was found
Videsott et al. L1 high, L2 high, Picture naming Fixating a cross (1) In all three languages, a Only fluency of word
(2010)/N = 20/languages: L3 intermediate common set of brain areas production was tested

International Journal of Multilingualism


L1 Ladin, L2 Italian, L3 dedicated to known which is just one
English subcomponents of picture aspect of language
naming were found proficiency
(2) In L1 and L2, enhanced right
prefrontal activity was found
a
Note that Jeong et al. (2007) is the only study that has been conducted on languages that have a large linguistic distance (Korean vs. English).
b
Note that there are only two language reception studies, whereas most studies focus on verbal fluency tasks.
c
Note that all experimental tasks were conducted covertly in the MR scanner.
d
Pihko et al. (2001) do not mention exactly what second and third languages the two participants in the fMRI study spoke.
e
Wattendorf et al. (2001) do not give any information about the third language involved in the study.

189
190 M. van den Noort et al.

generate words in the language under investigation that began with the letter until
the investigator instructed them to stop.
The results of the study showed activation from the language tasks primarily in
the lateral sections in the left prefrontal cortex. Most activation was found in the
inferior frontal, middle frontal and precentral gyri. In addition, for all five
participants, the largest activation was found for the L3, in which the participant
was least fluent. Finally, activation was also found in more medial sections in the
frontoparietal cortex and in supplementary motor areas.
Yetkin et al. (1996) conclude from their fMRI results that, in multilingual
participants, more activation is found in languages in which a participant is not
fluent compared with languages in which the participant is fluent. The results suggest
that activation decreases as proficiency in a language increases. Additional activity
was found in prefrontal areas, which corresponds to the idea that language control
regions are active in less fluent languages in order to avoid interference from the
more dominant languages. One major limitation of this study is that the control task
consisted of a rest period in which the participants were asked not to think of words,
an assignment which is, of course, impossible to control.
Pihko et al. (2001) investigated visual attention to words in L1 versus later
acquired languages with fMRI. The participants in their study were two healthy
right-handed volunteers who were native speakers of Finnish, were fluent in their L2
and were poor to fair speakers of L3. The participant’s task was to count how many
words were written in a target language out of the majority of words presented in
another language or non-target deviants in L3.
In both the native and the foreign languages, activation in the left occipito-
parietal cortex was found. In addition, greater activation in the left occipito-parietal
cortex was found for the two foreign languages in comparison with the native
language.
Pihko et al. (2001) conclude that the difference in neuroimaging results between
L1 and L2/L3 (acquired on or after school age) is likely to stem from the difference in
proficiency levels of each language, with lower proficiency being associated with
higher activation.
Wattendorf et al. (2001) conducted an fMRI study on eight right-handed healthy
multilingual participants. All participants were between 25 and 35 years and were
subdivided into ‘early’ bilinguals and ‘late’ bilinguals according to the acquisition
time of their languages. A verbal fluency task was conducted in all three languages.
The participant’s task was to formulate covertly the daily routine of the previous day.
The results showed activation in the language areas and in the premotor area,
supplementary motor area, anterior cingulate gyrus and middle temporal gyrus. The
additional activity of motor regions may be caused by the nature of the control
motor task and could thus be unrelated to language processing itself. Interestingly,
within the participants, different co-activation patterns were found in Broca’s area
for the three languages.
The authors conclude that the finding, that distinct response patterns exist for
each language in a multilingual person, supports the idea that different languages
may have different demands on specific brain areas involved in language processing
(Wattendorf et al., 2001).
In a study by Vingerhoets et al. (2003), the hypothesis was tested that in
multilingual speakers different languages are represented in distinct brain regions.
Twelve multilingual healthy male volunteers entered the study. All participants were
International Journal of Multilingualism 191

right-handed and were native speakers of Dutch (Flemish) and had learned French
(L2) and English (L3) as a foreign language at school. The different experimental
tasks were conducted; a word fluency task, a picture naming task and a
comprehension reading task.
The results of the picture naming task in general showed predominantly
overlapping regions of activation across all three languages. However, picture
naming in foreign languages recruited additional inferior lateral and medial frontal
regions predominantly on the left, and more posterior right hemispheric activation in
the L1.
The results of the word fluency task in general also showed overlapping regions
of activation across different languages. Word generation in the L2 and L3 elicited
additional bilateral inferior frontal activation, including Broca’s area and left middle
temporal gyrus activation whereas in the L1 additional postcentral gyrus activation
was found. Activity in regions that are not part of the classical language areas was
related to increased lexical retrieval effort during foreign language production
(Binder & Price, 2001; Fletcher & Henson, 2001).
In addition, the results of the comprehension reading task again revealed
overlapping regions of activation for native versus foreign languages; however, more
activation in medial posterior regions in the L1 was found. More specifically, the
lingual gyrus of the occipital lobe was involved, a region supposedly contributing to
the successful mapping of orthographic mental images to visual word form
representations (Fiebach, Friederici, Müller, von Cramon, & Hernandez 2003).
Hence, the authors concluded that the increased orthographic familiarity (as in L1)
could lead to more intense activity in occipital regions.
Finally, Vingerhoets et al. (2003) conclude that the performance of language
tasks in the native versus the foreign languages activates largely the same cerebral
areas. However, in order to perform at a comparable proficiency level, the brain
engages more neural substrates for the later acquired languages.
The study by Briellmann, Saling, Connell, Waites, Abbott, and Jackson (2004)
was one of a kind. In their study, six multilingual participants were assessed by fMRI
using a noun verb generation task in four languages. The languages of investigation
were English, German, Italian, French and Spanish. For four participants the native
language was German, the L2 was English, the L3 French and the L4 Italian. For
one participant the native language was English, the L2 was Italian, the L3 German
and the L4 Spanish, and finally for one participant the native language was French,
the L2 was English, the L3 German and the L4 Italian.
The results of the noun verb generation task showed task-related activity in the
left inferior frontal region, left posterior temporal region and left angular gyrus. In
addition, activation was found in the middle frontal gyrus and in the anterior
cingulate cortex, and finally a negative response in the posterior cingulate cortex was
observed. In other words, the Blood Oxygen Level-Dependent (BOLD) response
during the control condition (rest) was higher in the posterior cingulate cortex than
during the experimental (noun verb generation) task. Such a negative response in the
posterior cingulate cortex is not an unusual finding. It has, for instance, been found
in response to several cognitive paradigms (Mazoyer et al., 2001) and seems to be not
specifically related to linguistic processes.
Briellmann et al. (2004) conclude that their results support the hypothesis that
multiple languages are subserved by a common left hemispheric network. It should
be noted, however, that the choice for a low-level control task as in this design
192 M. van den Noort et al.

(fixating on a cross-hair) could yield more activity than is strictly required for the
linguistic processing one is interested in. Responses in the middle frontal region are
more likely to be associated with working memory aspects of word retrieval than
with speech processing per se (Wood et al., 2001). Also anterior cingulate activity can
be linked to extralinguistic attentional processing. Moreover, the authors state that
variations in language proficiency modulate the extent of activation with lower levels
of proficiency which leads to more intense activation in all parts of the network
mentioned.
Jeong et al. (2007) conducted an fMRI study on 30 healthy, right-handed native
Korean multilingual participants who were foreign language speakers of English and
Japanese. Their language proficiency in the two foreign languages did not differ. In
the study, all participants performed an auditory sentence comprehension task
in Korean, English and Japanese. Jeong and colleagues were particularly interested in
the question of whether linguistic similarity between the L1 (here Korean) and the
foreign languages (English vs. Japanese) would affect the cortical processing of a
foreign language.
Their results showed bilateral superior temporal cortex (Wernicke’s area)
activation during the comprehension of three languages. For Japanese, additional
activation was found in the pars triangularis of the left IFG (which is one of the two
subparts of Broca’s area). For English, the right cerebellum, the pars opercularis of
the left IFG (which is the other part of Broca’s area) and the posteromedial part of
the superior frontal gyrus were found to be additionally activated.
Jeong et al. (2007) conclude that the differential activation between the two
foreign languages seems to reflect an elaborate syntactic processing for English, as a
result of the different linear word order of English relative to Japanese (and Korean).
Broca’s area seems to play an important role in processing syntactically demanding
utterances (Stowe, Paans, Wijers, & Zwarts, 2004) and is shown to be connected to
the right cerebellum (Paulesu, Frith, & Frackowiak, 1993). The authors, therefore,
claim that their results support the hypothesis that linguistic similarity between the
native language and the foreign language indeed affects the cortical processing of the
foreign language.
In another neuroimaging multilingualism study, Bloch et al. (2009) tested the
hypothesis that the age of foreign language acquisition determines the variability in
activation in three languages in Broca’s and Wernicke’s area. In total, 44 multilingual
speakers, all of whom were fluent in a late learned L3, participated in the study. It
should be noted that the multilingual participants had a different age of exposure to
a second language (simultaneous or covert simultaneous exposure to L1 and L2,
sequential acquisition of L1 and L2 between 1 and 5 years and late learning of L2
after 9 years of age). The participant’s experimental task was a language production
task (silent free narration task).
It was found that the multilingual participants with early exposure to L2 showed
low variability in activation in Broca’s and Wernicke’s area across three languages, in
the two early as well as the late learned languages. However, in late multilingual
participants higher variability was found.
Bloch et al. (2009) conclude that there is a relation between cerebral representa-
tion of languages and the age of L2 acquisition. With increasing age of L2 exposure,
access to the classical language processing areas (Broca’s and Wernicke’s area) is
gradually decreasing, leading to more variable activation.
International Journal of Multilingualism 193

Finally, a very recent fMRI study was conducted by Videsott et al. (2010). In this
study, the neural correlates of language proficiency were investigated in a
homogeneous sample of 20 healthy right-handed multilingual native Ladin speakers,
who are highly proficient speakers of Italian (L2) and intermediate proficient
speakers of English (L3). Note that Ladin is spoken in a mountain valley in South
Tyrol in Italy. The participant’s experimental task was to name pictures of objects in
all three languages.
The results of the constrained word production task showed that word
production in all three languages activated a familiar group of brain areas that are
known to be subcomponents of picture naming. In comparison with the L3, the
fluently spoken native and second languages were associated with enhanced right
prefrontal activation. The investigators also found that the magnetic resonance (MR)
signal in the right prefrontal cortex showed a positive correlation with naming
accuracy as a measure of language proficiency. Since this was found to be
functionally related to inter-individual differences in language proficiency within
languages the authors conclude that it is unlikely that this finding can be explained
by intrinsic linguistic aspects of the languages or by the age of language acquisition.
Videsott et al. (2010) conclude that their results demonstrate the importance of
right prefrontal areas for language proficiency. The right prefrontal cortex seems to
support language proficiency by effectively supervising word retrieval.

PET
Halsband, Krause, Sipilä, Teräs, and Laihinen (2002) investigated the memory
processing of word pairs in multilingual participants with PET. Ten multilingual
speakers participated in the study. All participants were native speakers of Finnish
and had learnt 34 languages at school. For all multilingual participants, English
was their L2. The experimental task was to either encode or retrieve word pairs in
their native language or in a foreign language (English). More precise, the
experimental material consisted of four sets of 12 visually presented paired word
associates and the participants were instructed to read them aloud and to learn the
paired associations. The word pairs were difficult to associate, since they were
semantically unrelated. The duration of stimulus presentation was 4 seconds with a 1
second interval.
It was found that during memory retrieval, the precuneus which is part of the
superior parietal lobule (alternatively described as the medial area of the superior
parietal cortex) showed a consistent activation in both Finnish and English. This was
the case for both abstract and highly imageable words. The precuneus region thus
seems to underlie verbal memory and retrieval independent of the language used.
Moreover, although the brain mechanisms of the native and the foreign language
share common components, differential activations were found in the cerebellum, in
Broca’s area, and in the angular/supramarginal gyri (in the parietal lobe) according
to the language used. As the cerebellum was only active in native language trials,
activation of this region may refer to more automatic motor patterns associated with
the mother tongue. The additional activation in the parietal cortex when foreign
words are processed emphasises the role of this region in cognitive control of
language processes.
194 M. van den Noort et al.

Halsband et al. (2002) conclude that their results support the hypothesis for
largely overlapping cortical areas to be activated during retrieval of native and
foreign language word pairs (Halsband, 2006; Halsband et al., 2002).

MEG
Pihko et al. (2001) investigated the visual attention to words in L1 versus later
acquired languages with MEG. The participants in their study were nine healthy
right-handed volunteers, native speakers of Finnish, fluent in their L2 (Swedish,
English or Italian), and had poor to fair fluency in their L3 (Italian or Swedish). In
the MEG study as well, a collection of words was visually presented in three different
languages. The participant’s task was to count how many words were in a target
language when the majority of the words were in another language and there were
also non-target deviants in a third language.
The results showed that responses evoked by words in different languages began
to differ from each other at around 200 ms after stimulus presentation. With native
words as target, a selection response was found after 300600 ms. However, when
participants had to count foreign words among native standards, in addition to the
targets, the non-target foreign words as well evoked the selection process. Pihko et al.
(2001) conclude that their results of the MEG study reflect differences in the
selection process for native versus non-native words that can be explained by the
different proficiency levels of the L1, L2 and L3.
Pihko et al. (2002) conducted a second MEG study on 13 healthy participants.
All participants were early foreign language learners with the two foreign languages
learned well in early childhood before school age. Some of the participants even
spoke more than three languages. The participants differed from each other with
respect to their L1, L2 and L3, and the languages of investigation were Finnish,
English, Swedish, Italian and Croatian. Again the task was to count words in a target
language when most of the words were in another language and there were also non-
target deviants in L3.
The results showed an evoked pattern of magnetic responses in parieto-occipital
areas. Moreover, in the majority of the participants, the visual presentation of words
also evoked activation in the left temporal area. A negativity was found at a range of
400 ms after stimulus presentation (the so-called N400 component).
Pihko et al. (2002) conclude that their results support the hypothesis that in
multilingual visual surroundings there is a different need for attention to a non-target
language depending on whether the participant is attending to words in their native
or L2 even if the participant is a highly proficient L2 speaker, as in early foreign
language learners. In sharp contrast to L1, when words in L2 are being attended to,
participants are also paying attention to words in the non-target language to be able
to tell one from the other even though the non-target language is a language that the
foreign language speaker does not know. Finally, this different need for attention is
independent of the age of foreign language acquisition.

EEG
In their study on visual attention to words in the L1 versus later acquired languages
using MEG, Pihko et al. (2001) conducted simultaneous EEG recordings in two
International Journal of Multilingualism 195

healthy right-handed volunteers who were native speakers of Finnish, fluent in their
L2 and who were poor to fair speakers of L3.
When selecting words in the native language, the response resembles ‘selection
negativity’ with enhanced response amplitude in comparison with the response of
words in non-selected languages. However, in contrast to the L1, when selecting
words in a non-native L2, words in non-target L3 evoked a similar response as well.
Pihko et al. (2001) conclude that their results of the EEG study reflect differences
in the selection process for native versus non-native words that can be explained by
the different proficiency levels of the three languages.

Discussion
This review showed that, compared to bilingual studies, only few neuroimaging
studies have been conducted on multilingual participants. As a result, most
conclusions about L3 acquisition/processing in the brain are in fact based on L2
studies. Although we agree that these L2 studies can certainly give insights in L3
acquisition/processing we argue that studies based on bilingualism certainly cannot
replace these studies entirely. Clearly there are similarities between L2 and L3
acquisition/processing, but there are also important differences. Like in L2 (for a
review see Indefrey, 2006), overlapping areas of activation are often found with more
increased, larger and additional activations in the L3 (Jeong et al., 2007).
Moreover, the general results showed that in multilingual processing in the brain,
age of foreign language acquisition and foreign language proficiency are major
determinants of foreign language cortical representation (see Indefrey, 2006; Perani
& Abutalebi, 2005 for recent L2 reviews). In their multilingual neuroimaging study,
Bloch et al. (2009), for instance, showed that cerebral representation of languages is
linked to the age of L2 acquisition. With increasing age of exposure to a second
language, access to a common network for language processing is gradually
decreasing, resulting in a more variable activation.
However, L3 processing is not simply just another L2 processing. For instance, if
a participant knows three languages instead of two, different transfer effects than
only from L1 to L2 and/or from L2 to L1 as in bilinguals (Verhoeven, 2007) are
ongoing (for instance also from L2 to L3) (Heidrick, 2006). Moreover, there is
general consensus among researchers that language transfer is more likely to occur at
lower levels of proficiency (Odlin, 1989; Poulisse & Bongaerts, 1994) and often
people are indeed less proficient in their L3 compared to the L2. However, it is
important to note that this does not mean that language transfer cannot occur at
high proficiency levels (Verhoeven, 2007).
With respect to language switching (Hernandez et al., 2001) and language control
(Crinion et al., 2006), bilingual participants only have to control the language switch
and the use of two different languages, whereas multilingual participants have to
switch and control three different languages. It is assumed that this implicit practice
in language control also affects non-linguistic cognitive control in bilinguals. Costa,
Hernández, and Sebastián-Gallés (2008) have shown that bilingualism aids conflict
resolution in an attentional network task that taps into different non-verbal executive
functions such as orienting and alerting. Behavioural data showed faster reaction
times overall for bilinguals, which may suggest that they enjoy a more efficient
executive control network. Neurocognitive data as well have demonstrated that
bilinguals process conflict tasks differently from monolinguals (Bialystok et al.,
196 M. van den Noort et al.

2005). Given that multilinguals need to control even more than two languages, it
would be highly interesting to see if these advantages are enhanced when compared
to speakers of just two languages.
There are several important methodological remarks to make with respect to the
multilingual neuroimaging studies that were conducted so far. First, this study
showed that the selection of multilingual participants in multilingual neuroimaging
studies often causes difficulties. There are three main problems in the selection of
multilingual participants. First, most of the L3 neuroimaging studies are conducted
with very few participants (e.g. Pihko et al., 2001; Wattendorf et al., 2001; Yetkin
et al., 1996). Second, there often is a large difference and variability in foreign
language proficiency among the multilingual participants (Vingerhoets et al., 2003)
and thus the results may not be comparable. Finally, the foreign languages of the
multilingual participants are sometimes not kept constant (Yetkin et al., 1996). For
instance, in the Bloch et al. (2009) study, in total 18 different languages were
investigated as L1, L2 and L3. From a methodological point of view, this is not
desirable since it makes it nearly impossible to draw any firm conclusions about the
general L3 acquisition/processing. For instance, the results of the Jeong et al. (2007)
study clearly showed that linguistic distance is an important factor to control for. The
reason for the problems with the selection of multilingual participants often is a
practical one and has to do with the fact that it is often not possible to get access to a
large homogeneous multilingual group. On the one hand, a homogeneous multi-
lingual group is needed in order to obtain reliable and replicable results. On the other
hand, although the highly controlled studies are necessary for testing competing
theories, it is important to keep in mind that the selection of subgroups of participants
could in itself introduce generalisation problems. The simplest solution to this
problem is increasing the sample sizes. The inclusion of many more participants in the
multilingual neuroimaging studies should, in principle, allow studies to identify
subgroups of participants while still maintaining adequate statistical power. This
seems to be an adequate solution. In practice, however, the high expenses of the
neuroimaging techniques make these large-scale studies unrealistic. Therefore, a more
cost-effective and realistic solution seems to be to first identify the subgroups based
on a battery of behavioural measures, and then sample representative participants
from the subgroups based on those measures. Although this alternative will
undoubtedly lead to discussions like; which behavioural measures need to be used
in the battery and how exactly can subgroups of participants be identified?
Nevertheless, this seems to be the most promising direction to go in order to further
improve the selection of participants of future multilingual neuroimaging studies.
The second methodological issue is that all of the different multilingual
neuroimaging studies conducted so far have used different experimental tasks,
investigated different languages and used different kinds of multilingual participants,
making it impossible to compare and generalise results. Therefore, there is a need for
replication studies. Moreover, the very diffuse nature of some of the experimental
tasks in the multilingualism studies, like for instance the silent free narration task in
the Bloch et al. (2009) study is a huge limitation. Multilingualism is a very complex
topic to investigate and many factors need to be taken into account. Therefore, it is
particularly important to use clear experimental tasks where the experimenter can be
sure which factors play a role in performing the tasks, and that the multilingual
participants are actually conducting the task as was planned (which is impossible to
control in case of a silent free narration task). In addition, it is important to conduct
International Journal of Multilingualism 197

experimental tasks with different neuroimaging techniques like Pihko et al. (2001) did
because most experimental techniques require covert responses, and it may be hard
for researchers to ensure that participants are responding in the correct language.
This given could of course distort the collected data and explain some of the
confusing results that have been reported. Moreover, it would be important and
interesting to integrate them in order to combine the high spatial resolution of fMRI
or PET with the high temporal resolution of EEG and MEG (Halsband, 2006).
Finally, it is common in the neuroimaging field to use the term ‘activation’ in the
presentation of neuroimaging results (see for instance, Bloch et al., 2009; Jeong et al.,
2007); however, it is important to keep in mind that the relationship between the
activation of excitatory/inhibitory neurons and measures of BOLD signal change or
MEG source strength is actually a more complex one (see Editorial, 2009).
Therefore, in future research, researchers should take this point more into account
and should be more precise in the presentation of their results.

Conclusion
This review showed that in sharp contrast to L1 and L2, not many neuroimaging
studies have been conducted on multilingual participants so far. Most conclusions
that are drawn about multilingual processing are in fact solely based on bilingual
processing. Moreover, the few multilingual studies that were conducted contain
many serious methodological flaws, often as a result of the practical limitations to get
access to a large homogeneous multilingual group. In future research, more
multilingual neuroimaging studies need to be done, given that they can shed more
light onto how multiple languages are processed and represented in the brain. In
these future studies, multilingual researchers should better control for factors such as
language proficiency, age and manner of acquisition, language exposure and
linguistic distance between languages spoken. Moreover, replication studies are
needed, showing which results are consistent, reliable and unique for neuroimaging
research on multilingual participants in comparison with bilingual participants.
Here, the behavioural evidence for non-selective lexical access in bilinguals (e.g. de
Groot, 2010; de Groot, Delmaar, & Lupker, 2000) that presumably affect bi- and
multilinguals alike, for instance, might have important consequences for the
interpretation of certain functional brain imaging findings and seems to be a
promising future direction to go. Another way to make progress in future
neuroimaging research on multilingualism might be to look more specifically into
the interactions between language domains (input vs. output, grammar vs. lexicon)
and proficiency as well as age of acquisition as has been done in neuroimaging
research on bilingualism (e.g. Mechelli et al., 2004). Finally, it would be an
improvement when in future multilingual neuroimaging research different techniques
are used in the same study in order to acquire both temporal and spatial information
about multilingual processing in the brain or better still, more sophisticated
neuroimaging techniques to capture non-invasive activity are developed.

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