Bilingual and multilingual language processing · Bilingual and multilingual language processing...

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Journal of Physiology - Paris 99 (2006) 355–369

Bilingual and multilingual language processing

Ulrike Halsband *

Neuropsychology, Department of Psychology, University of Freiburg, Engelbergerstr. 41, 79089 Freiburg, Germany

Abstract

This chapter addresses the interesting question on the neurolinguistics of bilingualism and the representation of language in the brainin bilingual and multilingual subjects. A fundamental issue is whether the cerebral representation of language in bi- and multilingualsdiffers from that of monolinguals, and if so, in which specific way. This is an interdisciplinary question which needs to identify and dif-ferentiate different levels involved in the neural representation of languages, such as neuroanatomical, neurofunctional, biochemical, psy-chological and linguistic levels. Furthermore, specific factors such as age, manner of acquisition and environmental factors seem to affectthe neural representation.

We examined the question whether verbal memory processing in two unrelated languages is mediated by a common neural system orby distinct cortical areas. Subjects were Finnish–English adult multilinguals who had acquired the second language after the age of ten.They were PET-scanned whilst either encoding or retrieving word pairs in their mother tongue (Finnish) or in a foreign language (Eng-lish). Within each language, subjects had to encode and retrieve four sets of 12 visually presented paired word associates which were notsemantically related. Two sets consisted of highly imaginable words and the other two sets of abstract words. Presentation of pseudo-words served as a reference condition. An emission scan was recorded after each intravenous administration of O-15 water. Encodingwas associated with prefrontal and hippocampal activation. During memory retrieval, precuneus showed a consistent activation in bothlanguages and for both highly imaginable and abstract words. Differential activations were found in Broca’s area and in the cerebellumas well as in the angular/supramarginal gyri according to the language used. The findings advance our understanding of the neural rep-resentation that underlies multiple language functions. Further studies are needed to elucidate the neuronal mechanisms of bi/multilin-gual language processing. A promising perspective for future bi/multilingual research is an integrative approach using brain imagingstudies with a high spatial resolution such as fMRI, combined with techniques with a high temporal resolution, such as magnetoenceph-alography (MEG).� 2006 Elsevier Ltd. All rights reserved.

Keywords: Bilingualism; Brain imaging techniques; Indo-European and non-Indo-European languages; Brain development; Aging; Associative learning

1. Introduction: Languages and different forms of

bilingualism

There is no evidence of any human groups who do notspeak at least one language. At present, more than 6000spoken languages are used in the world. Moreover, man-kind has a unique ability to learn more than one language.This is thought to be mediated by functional changes in thebrain.

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Fabbro (1999) pointed out that all languages show twomain characteristics (i) they make use of the vocal-auditorychannel to produce and perceive sounds and (ii) they areorganised according to the principle of double articulationor duality of patterning. The latter refers to a level of wordswhich bear meaning and a level of phonemes limited innumber.

Language use consists of the socially and cognitivelydetermined selection of behaviours according to the goalsof the speaker and the context of the situation. Since itexists in the form of several different languages, it is notsurprising that some nations are officially bi- or multilin-gual. Well-known examples are Canada and India. Most

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356 U. Halsband / Journal of Physiology - Paris 99 (2006) 355–369

citizens of these countries are bilingual. Out of the Euro-pean nations that are officially bi- or multilingual, Belgium,Switzerland and Finland are well-known examples. OtherEuropean countries have at least one linguistic minoritywhose members are, usually, bilingual. One might askhow much semantic overlap there might be between thetwo languages. Obviously, closely related languages (e.g.Spanish and Italian) share much semantic overlap; in con-trast, unrelated languages (e.g. Finnish and English) do nothave much in common. There are different forms of bilin-gualism. Simultaneous bilingualism refers to the learningof two languages as ‘‘first languages’’. Infants who areexposed to two languages from birth will become simulta-neous bilinguals. In other words, a person who is a simul-taneous bilingual advanced from speaking no languagesat all directly to speaking two languages. In contrast, con-

secutive or successive bilingualism refers to the learning ofone language after already knowing another. This is the sit-uation for all those who become bilingual as adults, as wellas for many who became bilingual earlier in life. In addi-tion, receptive bilingualism implies that a person is able tounderstand two languages but expresses oneself in onlyone language. However, this is generally not consideredto fall under the category of ‘‘true’’ bilingualism but is afairly common situation worth to mention.

2. Where are the roots of the Indo-European and

Non-Indo-European languages?

There is no consensus on where the Indo-European lan-guages originally came from. The origin of the Indo-Euro-pean language family is ‘‘the most intensively studied, yetstill most recalcitrant problem of historical linguistics’’(Diamond and Bellwood, 2003).

It has been suggested that a family tree of Indo-Euro-pean languages spread and split about 9000 years ago. Itwas argued that Kurgan (Siberian) horsemen carried themout of central Asia around 6000 years ago. However, thisview was recently challenged by the work of Gray andAtkinson (2003). They analysed lists of 200 commonly usedwords in 87 different languages, such as ‘‘I’’ and ‘‘sky’’.Their resulting tree matches many existing ideas about lan-guage development. For instance, Spanish and Portuguesecame out as sisters and German as their cousin. Hindi wasjudged as a common source to all three of them but to havea more distant relationship. All other Indo-European lan-guages split off from Hittite, the oldest recorded memberof the language groups. According to Gray and Atkinson(2003) this happened between 8000 and 9500 years BP(before present).

But Gray and Atkinson (2003) make a further point.Taken archaeological evidence into account they argue thatfarming techniques began to spread out of Anatolia (cur-rently Turkey). Along these lines the farmers themselvesmight have moved and/or natives adopted words alongwith agricultural technology. Radiocarbon analysis of theearliest Neolithic sites across Europe suggests that agricul-

ture arrived in Greece at some time during the ninth millen-nium BP and had reached as far as Scotland by 5500 yearsBP. The Hittite lineage is thought to have been divergingfrom Proto-Indo-European around 8700 years BP, perhapsreflecting the initial migration out of Anatolia. Tocharianand the Greco-Armenian lineages are shown as distinctby 7000 years BP, with all other major groups formed by5000 years BP. This hypothesis is consistent with recentgenetic studies supporting a Neolithic, Near Eastern contri-bution to the European gene pool (Chikhi et al., 2002;Richards et al., 2000).

Non-Indo-European languages are classified together asthose languages that do not figure as members of thisstock. Written evidence of, e.g., the Turkic languagesbegins with the Orkhon inscriptions of the 8th centuryAD, found near the river Selenga in Mongoli.

Genetic relations among Non-Indo-European languageswere reported, e.g. for Finno-Ugric languages such asFinnish, Hungarian, and Estonian, Kartvelian languagessuch as Georgian, Abkhaz and Armenian, and Altaic lan-guages such as Turkic and Manchu-Tungus. However,typological similarities were also observed among the lin-guistic structures of genetically unrelated languages suchas Japanese and Turkish. Studies of geographical cultureareas such as the Ancient Near East further show that cul-turally-linked regions share non-genetic similarities.

Casad and Palmer (2003) tried to outline the dimensionof Cognitive Linguistics with respect to Non-Indo-Euro-pean languages. The authors argued that ‘‘The world ofnon-Western languages offers a breathtaking opportunityto delve into a wide spectrum of empirical and theoreticalissues, some of which are new (. . .) and others that havehitherto resisted satisfactory explanations constructed inother linguistics theories’’.

3. Language education and bilingualism

One of the central questions concerns when and howchildren ought to start learning a second language. It is wellknown that the earlier the exposure to both languages, theeasier and more complete their acquisition. In the best pos-sible way already toddlers are confronted with two differentlanguages during their daily life activities. Foreign lan-guage education should already start at pre-school and/or early primary school; young children display a remark-able capacity to adjust to the features of different accents.Thus, young children show a great ability to acquire newlanguages with ease in that they can quickly become profi-cient in the accent of the new language.

A controversially discussed question is whether bilingualchildren turn out to be cleverer than monolinguals. Pealand Lambert (1962) examined monolinguals and French/English bilinguals in Montreal. They tested the childrenon both verbal and non-verbal measures of intelligenceand found that bilinguals had more ‘diversified structureof intelligence’ and more ‘flexibility in thought’. Bilingualchildren showed ‘greater cognitive flexibility’ and they

U. Halsband / Journal of Physiology - Paris 99 (2006) 355–369 357

recognised the arbitrariness of words and their referents. Incontrast, the recent study by Albert et al. (2002) failed toprovide sufficient evidence to support the existence of arelationship between either bilingualism and critical think-ing ability or between critical thinking disposition and crit-ical thinking ability. However, the authors reported thatthere was sufficient evidence to support the existence of acurvilinear relationship between bilingualism and criticalthinking disposition.

Bialystok (2001) showed that bilingual children developcontrol processes more readily than monolingual childrenbut that the two groups progress at the same rate in thedevelopment of representational processes.

4. Speech disorders in bilinguals and the effect of aging

There is no evidence that bilinguals are more vulnerableto speech disorders, like stuttering, as compared to monol-inguals. Jankelowitz and Bortz (1996) examined the rela-tion between bilingualism and stuttering in a bilingualadult (English and Afrikaans) who stuttered. Results indi-cated that language ability influenced frequency, distribu-tion and nature of disfluencies. The subject was moreproficient and stuttered less in his predominant language.The difficulty stutterers might have with individual soundswas investigated by Jayaram (1983) (19 with respect to twomodes of speaking (oral reading versus spontaneousspeech) and two languages (English versus Kannada).Ten monolingual and ten bilingual stutterers read 16 listsof words (eight in each language). Analysis of stutteringwas made with respect to a three-way classification ofsounds (vowels, voiceless consonants, and voiced conso-nants) as well as an eight-way classification (short vowels,long vowels, voiceless stops, voiceless fricatives, voicedstops, voiced fricatives, nasals, and semivowels). Word-initial and total stuttering was analysed. Results indicatedthat both monolingual and bilingual stutterers were moredysfluent on voiceless consonants and especially on voice-less fricatives, when total stuttering was considered. Find-ings of the analysis of word-initial stuttering showed thatbilingual subjects stuttered more on the nasal sounds.The results of the bilingual comparison indicated the possi-bility that the phonetic influences on stuttering might bedependent on the number of languages spoken by the sub-jects as well as the specific language in which the effectswere observed.

As yet little is known about the effects of normal agingon the bilingual condition. A decline in bilingual profi-ciency with age has been reported. There are examples ofelderly multilinguals who have maintained only certainlanguages. MacWhinney and Bates (1989) concluded ‘‘Alife-time of multilingualism is not sufficient to guaranteemaintenance of more than one language across the courseof normal aging’’. Balota and Duchek (1988) reported thatelderly adults can compensate for a loss in processing effi-ciency under normal conditions with context-based strate-gies (‘top-down’). However, this may require attentional

resources that are hard to maintain over time. Thereforethere is a tendency to retreat towards a monolingual condi-tion as a strategy for coping with the hypothetical loss inprocessing efficiency.

Recently Bialystok et al. (2004) investigated whether abilingual advantage persists for adults. The authors com-pared the performance of monolingual and bilingual mid-dle-aged and older adults on the Simon task. This task isbased on stimulus–response compatibility and evaluatesthe extent to which the prepotent association to irrelevantspatial information affects the participants’ response totask-relevant non-spatial information. Results indicate thatbilingual subjects showed smaller Simon effect costs forboth age groups; bilingual subjects also responded fasterto conditions that placed greater demands on workingmemory. Interestingly, the bilingual advantage was morepronounced for older participants. It was concluded thatexecutive functioning is carried out more effectively by bil-inguals and that bilingualism helps to offset age-relatedlosses.

5. What are the neural bases of language processing inone’s mother tongue as compared to a foreign language?

5.1. Lateralisation in spoken and signed languages

For more than a century it is known that the dominantleft hemisphere of the human brain is critical for producingand comprehending spoken language. Damage to perisyl-vian areas within the left hemisphere produces varioustypes of aphasia, whereas damage to homologous areaswithin the right hemisphere does not generally produceaphasic symptoms. Furthermore, brain imaging studiesconfirmed that speech activation mainly occurred in theof language dominant hemisphere. For instance, Borbelyet al. (2003) tested the prediction that single photonemission computed tomography (SPECT) of the bloodflow distribution in speech-activated brain identifies thelanguage-dominant hemisphere. The authors comparedthe results of speech activation to the results of functionaltranscranial Doppler (fTCD) monitoring in the same sub-jects. Highest changes of rCBF from baseline to activationwere found in the left posterior inferior frontal cortex andin the contralateral cerebellum. The evaluation of hemi-spheric language dominance based on SPECT showed anagreement with the evaluation based on fTCD.

Similarly, research has indicated that the left cerebralhemisphere is also critical to processing signed languages.It was found that damage to the left perisylvian areas butnot to the right hemisphere lead to sign language aphasias(Bellugi et al., 1989; Corina, 1999; Hickok et al., 2001). Bel-lugi et al. (1989) reported that the left cerebral hemispherein man is specialised for signed as well as spoken languages,and thus may have an innate predisposition for language,independent of language modality.

Sign languages have many structural features in com-mon with spoken languages, though they do not use the


vocal-auditory channel (Bellugi et al., 1989). Studies of thesigned languages of deaf people have shown that fullyexpressive languages can arise, outside of the mainstreamof spoken languages that exhibit the complexities of lin-guistic organisation found in all spoken languages (Bellugiet al., 1989). Multi-layering of linguistic elements and theuse of space in the service of syntax appear to be modal-ity-determined aspects of signed languages. In other words,the human capacity for language is not linked to some priv-ileged cognitive-auditory connection. The formal proper-ties of languages (spoken or signed) appear to be highlyconditioned by the modalities involved in their perceptionand production. Analyses of patterns of breakdown ofsigned languages provide new perspectives on the natureof cerebral organisation for language.

Most interestingly, recent evidence suggests a criticalrole of the right hemisphere in signed language production.Using PET, Emmorey et al. (2002) tested deaf native sign-ers who viewed line drawings depicting a spatial relationbetween two objects (e.g., a cup on a table). Subjects wereasked either to produce a classifier construction or anAmerican Sign Language (ASL) preposition that describedthe spatial relation or to name the figure object. Resultsindicate that describing spatial relationships with classifierconstructions engaged the supramarginal gyrus (SMG)within both hemispheres. Compared to naming objects,naming spatial relations with ASL prepositions engagedonly the right SMG. In contrast, naming concrete objectsin either ASL or English resulted in activation in the left

inferior temporal (IT) cortex. In summary, the study makestwo major points:

(1) The results suggest more right hemisphere involve-ment when expressing spatial relations in ASL. Thus,when expressing spatial relationships, the visuo-spa-tial modality of signed languages has an impact onthe neural systems that underlie language production.

(2) Findings indicate that the neural systems involved inthe retrieval of ASL signs denoting concrete entitieswithin distinct conceptual categories are remarkablysimilar to those underlying the retrieval of spokenwords denoting the same types of entities. Thus, whennaming concrete entities, the neural structures thatmediate language output are the same regardless ofthe mode of output, either speech or sign.

The nature of spatial language differs quite dramaticallyfrom spatial language in spoken languages where singleclosed class elements (i.e., prepositions or locative affixes)denote spatial relations. Therefore it is not surprising tofind within this domain variation between the neural sys-tems underlying speech and sign production.

Most recently, Sakai et al. (2005) systematically ana-lysed comprehension of sentences and sentential non-worddetection in different groups of Japanese subjects and stim-ulus conditions. Under the sign condition with sentencestimuli in the Japanese Sign Language (JSL) the authors

tested two groups of volunteers: deaf signers of JSL, andhearing bilinguals, competent of JSL and Japanese. Inthe speech condition, hearing monolinguals of Japanesewere tested using auditory Japanese stimuli alone or anaudio-visual presentation of Japanese and JSL stimuli.Results indicated across all experimental conditions a con-sistent left-dominant activation involving frontal andtemporo-parietal regions. Activations selective to the com-prehension of sentences were also found primarily in theleft hemisphere. The authors reported that the opercularand triangular parts of the left inferior frontal gyrus, theleft lateral premotor cortex (Brodmann area 6), the frontaleye fields (Brodmann area 8), and the prefrontal cortex(Brodmann area 9) are specifically involved in grammaticalprocessing. The function of such a grammar centre for signas well as spoken language was further discussed in a recentarticle by Sakai (2005).

5.2. Brain imaging of bilingual processing using functional

brain imaging and neurophysiological techniques

5.2.1. State of the artThe cerebral localisation of multiple languages is a topic

of active research. Recent studies have shown variation inthe cerebral activation in the context of processing nativeand foreign languages (Dehaene et al., 1997; Kim et al.,1997; Klein et al., 1994; Perani et al., 1996, 1998). It hasbeen suggested that there are differences in the cerebralorganisation of language depending on the age of acquisi-tion and learning strategies (Neville et al., 1992, 1997;Weber-Fox and Neville, 1996). However, it remained to alarge extent unsettled how multilingual processing takesplace in the brain.

Clinical studies on aphasic disturbances in bilingualpatients have provided information about the recovery ofthe respective languages spoken by these subjects, e.g. pref-erential recovery of the old as contrasted with the new lan-guage or preferential recovery of the most familiarlanguage (Fabbro, 1999; Paradis, 1994; Roberts and LeDorze, 1998). These findings suggest that there are multi-lingual patients, who after brain lesions may become apha-sic in only one of the languages they originally mastered.This dissociation is supported by the results obtained withelectrical cortical stimulation: Ojemann and his associates(Ojemann, 1991; Ojemann and Whitaker, 1978) stimulatedelectrically the cortical areas of neurosurgical patients inorder to identify the speech-relevant centres. In the studyby Ojemann and Whitaker (1978) the localisation of twolanguages in the lateral cortex of the dominant cerebralhemisphere was determined by the technique of mappingsites where electrical stimulation altered naming in twobilingual patients’ languages (patient one Dutch–English,patient two Spanish–English). The patients had to name45 common objects which were presented visually throughslides. It was found that sites in the centre of the languagearea of each patient were involved in both languages. How-ever, peripheral to this, in both frontal and parietal cortex,


were sites involved in only one of the languages. It was con-cluded that in each patient, each language in part used dif-ferent areas of the brain.

Language mapping in bilingual patients undergoing cor-tical resection of an epileptic focus has major restrictions:The cortical organisation of language may have beenaffected by the effects of having a seizure focus establishedearly in life. In contrast, adults presenting with a primarybrain tumour offer a different opportunity to study bilin-gual cortical representation of language sites, because pre-sumably the brain has been unaffected by epilepsy duringthe first decade of life. Recently, Walker et al. (2004) pre-sented the results for 17 bilingual patients who underwentspeech mapping as part of the surgical procedure toundergo tumor resection. Stimulation mapping was per-formed in each language by use of an object-naming task.A site was classified to be essential for naming in either lan-guage if interruption of naming occurred in at least two-thirds of the stimulations at that site. A site essential fornaming was identified in the exposed cortex only for 5 of17 patients. Two out of five patients displayed anomia inboth languages, two others had anomia in only one lan-guage, and one showed anomia in one language but onlyhesitation of naming in the other language. The authorsconcluded that although no site was identified in the major-ity of the patients, those individuals in whom a site wasidentified demonstrate that bilingual patients undergoingtumour resection should be mapped for ALL languagesbefore it is decided which cortical and subcortical areasare safe to remove. A recent study with optical imagingpreceding a neurosurgical procedure (Pouratian et al.,2000) confirms that cortical language representations inbilingual persons may consist of both overlapping and dis-tinct components.

Using functional magnetic resonance imaging (fMRI),Kim et al. (1997) reported that the mother tongue is local-ised in Broca’s area and each newly acquired language inanterior portions of Broca’s area. The second languagetended to have a more diffuse representation in the lefthemisphere than did the mother tongue (Dehaene et al.,1997). Furthermore, it has been proposed that the leftsupramarginal gyrus in the parietal lobe controls switchingfrom one language to another (Price et al., 1999).

Pillai et al. (2003) studied differences in regional fMRIactivation topography and lateralisation between semanticand phonological tasks performed in English and Spanishin bilingual individuals. Eight bilingual Spanish-Englishindividuals had to perform noun-verb association andrhyming tasks in their mother tongue (Spanish) and in aforeign language (English). The authors reported signifi-cantly higher laterality indices in the semantic tasks ascompared with the phonological tasks in the anteriorregions of interest comprising the frontal and superior tem-poral lobes. A task subtraction analysis demonstrated righthemispheric (inferior frontal gyrus and supramarginalgyrus) foci of significantly increased activation in thecombined language phonological tasks compared to the

combined language semantic tasks. Pronounced righthemispheric activation was also seen in the English phono-logical-English semantic subtraction, but the analogousSpanish task subtraction revealed no task-related differ-ences. This divergence in activation topography observedin the foreign language condition suggests that neuralnetworks utilised for phonological and semantic languageprocessing in the non-native language may not be as similaras those in the mother tongue.

Using fMRI Mahendra et al. (2003) examined whetherpartial overlap of active voxels reflects differential languagelocalisation, or simply the variability known to occur withmultiple runs of the same task. They studied two groups ofbilingual subjects (early and later learners of L2) when thesubjects had to perform word fluency and sentence genera-tion tasks in both languages. They found that early biling-uals showed greater total numbers of active voxels than latebilinguals for both tasks. This effect occurred despite a lackof a behavioural performance differences by the twogroups.

Sinai and Pratt (2003) recorded event related brainpotentials to assess stages of linguistic processing of first(L1), second (L2) language and of pseudo words when sub-jects were engaged in a different task and did not attend tothe words. Young adults (n = 15) were presented with pairsof auditory stimuli consisting of words and pseudowords inL1 and L2 with different voice onset times (VOT), whichserved as distracters in a short-term memory task. ERPswere recorded from 11 scalp electrodes. Behavioural resultsshowed that attention was drawn to the primary task andaway from the words; yet significant, including semantic,processing was evident in the ERPs to the words, with sig-nificant effects of language, meaning and priming. It wasconcluded that even with barely any awareness of the stim-uli, the brain processes words distinguishing between L1and L2 and relating to the stimuli’s context.

Nakamura and Kouider (2003) reviewed lesion andfunctional imaging studies of Japanese writing to discussthe possible differences in neural correlates that have beenassumed for its two orthographic systems, kanji (logogram)and kana (syllabogram). The author concluded that fronto-parietal cortical circuit linking the premotor with posteriorparietal areas in the left hemisphere constitutes a basic neu-ral substrate for the motor act of writing. It was arguedthat writing of kana utilises these structures in conjunctionwith the left perisylvian area for spoken language. In con-trast, writing of kanji shares this network for motor execu-tion, but recruits the left basal temporal area as anadditional device for the generation of motor output. Find-ings suggest that writing of kanji needs the retrieval of vis-uospatial information of characters as an additionalcognitive demand.

A most interesting question is to analyse how one’smother tongue affects the acquisition of second languages.Tan et al. (2003) studied with fMRI the neural mechanismsof reading in a second language (L2) in Chinese-Englishbilinguals. Chinese and English are two written languages


with a sharp contrast in phonology and orthography.Chinese language (L1) consists of logograms, i.e., singlewritten characters which represent a complete grammaticalword as compared to alphabetic English (L2). The authorsfound that phonological processing of Chinese charactersrecruits a neural system involving left middle frontal andposterior parietal gyri, cortical regions that are known tocontribute to spatial information representation, spatialworking memory, and coordination of cognitive resourcesas a central executive system. Interestingly, when the bilin-gual subjects read English words, this neural system wasmost active, whereas brain areas mediating English monol-inguals’ fine-grained phonemic analysis were only weaklyactivated. The authors concluded that bilingual subjectswere applying their L1 strategies to L2 reading. In otherwords, the lack of letter-to-sound conversion rules in Chi-nese led Chinese readers to being less capable of processingEnglish by recourse to an analytic reading system on whichEnglish monolinguals rely. These findings support the ideathat language experience tunes the cortex.

The crucial question how the first language affects theacquisition of second languages is a rather difficult topicto investigate. A promising approach is the study by Fran-ceschini et al. (2001) who correlated images of local brainactivation during speech production and perception withthe language profiles of single persons. Language profileswere obtained by means of so called language biographies.The term language biographies refers to an autobiograph-ical oral narration, thematically focussed on experiences ofthe informants with his/her own languages during thecourse of life, directed to an interview partner (Schutze,1987). It was reported that correlates exist between the typeof acquisition (early bilingualism vs. late bilingualismincluding third languages) and brain activation usingfMRI. Wattendorf et al. (2003a) showed that there is a crit-ical period early in life in which exposure to one or two lan-guages determines permanently the participation of thefrontal network in language processing. It was found thatan activation of the frontal network occurs in early multi-linguals, but not in late multilinguals. Furthermore, thefrontal activation was differently organised: Broca’s areawas preferentially involved during processing of both L1(early acquired language) and L3 (late acquired language);in contrast, the lateral prefrontal cortex and the orbito-frontal cortex showed relevant activation for the L1 condi-tion only (Wattendorf et al., 2003b). Certainly, this kind ofqualitative and inductive approach has its limitations. Nev-ertheless, to my knowledge, this is one of the first successfulsystematic approaches which aimed to bridge the gapbetween language biographies and brain images. Using anon-speech auditory paradigm, Wattendorf et al. (2002)found a pronounced activity in the left inferior parietal cor-tex and planum temporale in subjects who had beenexposed to two different languages before the age of three.It was concluded that an enriched linguistic environmentmay lead to a modulation of processing strategies indefined cortical areas.

Mechelli et al. (2000) reported that learning a secondlanguage increases the density of grey matter in the leftinferior parietal cortex of bilinguals relative to monoling-uals, and that the degree of structural reorganisation in thisregion is modulated by the proficiency attained and the ageat acquisition. The authors found that there is a more pro-nounced increase in early rather than late bilinguals, andthat the density in this region increases with second lan-guage proficiency but decreases as the age of acquisitionincreases. It was suggested that early bilinguals mayacquire a second language through social experience,rather than as a result of a genetic predisposition. Mostrecently Klein et al. (2006b) investigated the neural sub-strates involved in the production of a second language(French) after the age of five as compared with those brainregions involved in the repetition of the native language(English). The authors compared word and non-word rep-etition. Results indicate that subjects activated the left ven-tral premotor area under both word and non-wordrepetition in the second language to a greater extent thanin the native language. Activation of the premotor cortex(lateral Brodmann area 6) was observed in similar locationsduring both word and non-word repetition. Future studiesare needed to examine real-word and non-word repetitionin bilingual subjects in order to disentangle the confound-ing effects of language-specific and language-acquisitionalvariables. Taken together the findings are in agreementwith the hypothesis that the structure of the human brainis altered by the experience of acquiring a second language.

5.2.2. Encoding and retrieval of word pairs

in multilinguals – a PET-study

In our PET-study (Halsband et al., 2002) we addressedthe question whether memory processing in two languagesbelonging to different linguistic groups use common neuralsystems. We looked for shared and non-shared neural sub-strates in a paired-word association paradigm for such con-trasting languages as Finnish and English.

We used O-15 water PET to study differences in cerebralactivation patterns associated with the verbal memory pro-cessing of concrete and abstract word pairs in the nativelanguage of the subjects (Finnish) compared with a fluentforeign language (English). We tried to disentangle the neu-ral mechanisms of encoding and retrieval in multilingualsubjects who, among other languages (see below) were flu-ent in two widely different linguistic groups, i.e., a non-Indo-European language, Finnish and an Indo-Europeanlanguage, English.

Ten late Finnish-English multilinguals took part in thisstudy. Their mother tongue was Finnish. English wasacquired as a second language at school after the age often years. In addition to the English language all of oursubjects had learnt Swedish at school. Furthermore, allbut two subjects acquired a third foreign language:German, Russian or French. One subject took additionalcourses in Spanish. So, all of our subjects were multiling-uals whereby their first and predominant foreign language


was English. In addition, our subjects reported that theywere confronted with English in their daily activities (workand relaxation including music, films and televisionprograms).

Subjects were right-handed males (age 27.3 ± 5.1 years,mean ± SD, range 22–36 years) with no known history ofneurological or psychiatric illness. All but one of the sub-jects had undergone an MRI examination (1.5 T) of thebrain, where no structural abnormalities were found. Thesubject, who could not take an MRI examination due tometal implants in his denture, had an unremarkable com-puterised tomography (CT) scan. The research projectwas approved by the Joint Ethical Committee of the Uni-versity and University Hospital of Turku, Finland. Eachsubject gave informed, written consent for participationin the study according to the guide-lines of the Declarationof Helsinki.

We used a within-subject design, which meant that eachsubject underwent both a native language session and anEnglish session. Subjects had to encode and retrieve foursets of 12 visually presented paired word associates. Studywords were two-syllable Finnish or English words. Theword pairs were semantically unrelated and, therefore, dif-ficult to associate. ‘‘Hard’’ word associations (as intro-duced by Wechsler (1987) in his Wechsler Memory Scale,Subtest VII) were used to increase the mnestic demands(see Fig. 1).

The stimulus words were presented on a 2100 computerscreen placed at a distance of about 70 cm from the eyes(Font: Times New Roman, size: 72 points). Subjects wereinstructed to read them aloud (duration of presentation4 s, 1 s interval) and to learn the paired associations. In

Fig. 1. Experimental paradigm: subjects were instructed to encode andretrieve sets of 12 visually presented paired word associates. Two-syllableword pairs in the native language (Finnish) or foreign language (English)were used. Word pair sets consisted of highly imaginable words andanother set of abstract words. During retrieval scans only the first word ofthe pair was shown and subjects had to retrieve the associated word frommemory. The reference task was a presentation of two-syllable non-sensewords formed according to the spelling rules of the Finnish or Englishlanguage, respectively.

order to avoid lateralisation effects the second word waswritten under the first word, the letters were black on awhite screen and centred. Between encoding and retrievalscans, the same word pair associates were presented in ran-dom order 1–3 times according to the number of encodingrepetitions needed to retrieve at least 80% of the word pairassociates. During retrieval scans, the first word of the pairwas shown. The subjects had to read the first word aloudand to retrieve the associated word from memory andexpress it verbally. The reference task was the presentationof two-syllable non-sense words formed according to thespelling rules, but having no semantical meaning. The sub-jects were required to read the non-sense words aloud, butthey were not requested to memorise them. The details ofthe experimental paradigm of paired-word associationmemory have been described earlier (Halsband et al.,2002).

Scanning was done on two separate days. In the firstscanning session the subjects were requested to learn andto retrieve word pairs in their mother tongue; the secondscanning session involved paired-word association learningin the foreign language.

Session I (Finnish): Each subject underwent twelve O-15water PET scans. Two word pair sets consisted of highlyimageable words (e.g. POLKU – small road vs. KOIRA– dog) and another two sets of abstract words (e.g. UHKA– threat vs. SUURE – unit). These words were selected onthe basis of the Finnish word frequency handbook (Sau-kkonen et al., 1979).

Session II (English): The same subjects were scannedduring the learning and retrieval of English word pairs.The technical execution of the PET scans and the principlesof the experimental paradigm were the same as describedabove, except for the fact that the word pairs were in Eng-lish. The English proficiency of the subjects was tested withan ad hoc questionnaire before starting the experimentalPET sessions. The subjects had to encode and retrieve foursets of 12 English word pairs. The English words were cho-sen according to Paivio et al. (1966, 1968), independently ofthe selection of the Finnish stimulus words. In order to ruleout familiarity effects, great care was taken that the samenouns were not used twice in the two different languages.For instance, if in the English condition the high frequencyword ‘‘monkey’’ was used, the Finnish word list did notcontain a noun referring to this specific animal categoryor a similar species (apes); instead the Finnish word listmade use of the word ‘‘koira’’ (dog).

Scans of rCBF were obtained for each single subjectusing a GE Advance PET Scanner (General Motors Med-ical Systems, Milwaukee, Wisconsin, USA). This apparatushas been previously described (Lewellen et al., 1996).Regional cerebral blood flow (rCBF) during each cognitivetask was measured by recording the distribution of radio-activity in the brain following an intravenous injection of300 MBq of O-15-labelled water (10 ml in 10–15 s) througha forearm cannula. Twelve tasks were carried out duringa three-hour session. The minimum interval between the

Table 1Encoding of words with high imagery content compared to referencecondition

Talairachcoordinates

Z BA Region

x y z

Foreign language

36 42 36 4.46 10 Prefrontal cortex (right)�22 26 0 4.03 11 Orbitofrontal cortex (left)�26 54 12 3.90 10 Prefrontal cortex (left)

20 �38 �28 3.44 Hippocampal formation (right)�14 �38 �20 4.50 Hippocampal formation (left)�46 �72 28 3.95 39 Angular/supramarginal gyrus (left)

6 �78 52 3.68 7 Precuneus (right)

Mother tongue

8 26 �24 3.80 11 Orbitofrontal cortex (right)32 �58 �4 3.44 Hippocampal formation (right)18 �36 �12 4.59 Hippocampal formation (left)

Fig. 2. Comparison of adjusted mean rCBF in ten subjects betweenretrieval of word pairs with high imagery content and reference. Spatialdistributions of significant voxels are shown as integrated projectionsalong sagittal, coronal and transverse views of the brain. Foreign language(a) and native language (b) compared against reference condition.


O-15 water injections was 10 min. As each of the twelvescans was concerned, the cognitive task began 15 s beforethe administration of O-15 water. Emission data wereacquired in 3-dimensional mode for 90 s starting at theentry of the tracer into the brain, for which the criterionwas the true coincidence rate exceeding the threshold of15,000 counts/s. Data were framed into a single staticframe of 90 s (Holm et al., 1995; Laine et al., 1994).

The data were first transformed into the ANALYSE for-mat using a converter program especially developed forthis purpose at Turku PET Centre. The actual quantitativeanalysis of the 90 s images was carried out with StatisticalParametric Mapping (SPM96, The Wellcome Departmentof Cognitive Neurology, London, UK) software (Fristonet al., 1995a,b) on a SPARC 20 workstation (Sun Micro-systems). Calculations were performed with Matlab version4.2 c. Each reconstructed O-15 water scan was realignedaccording to the bi-commissural line into a stereotaxicspace corresponding to the atlas of Talairach and Tour-noux (1988) using a PET template and normalised accord-ing to Friston et al. (1995a). A Gaussian filter with a fullwidth half maximum (15 mm) was applied to smooth eachimage to compensate for inter-subject differences and tosuppress high frequency noise in the images. Differencesin global activity within and between subjects wereremoved by the analysis of covariance (ANCOVA) on avoxel by voxel basis with global counts as covariate ofregional activity across subjects for each task, as inter-and intrasubject differences in global activity may obscureregional alterations in activity following cognitive stimula-tion. For each pixel in stereotactic space the ANCOVAgenerated a condition-specific, adjusted mean rCBF value(normalised to 50 ml/100 ml per min) and an associatedadjusted error variance (Van den Heuvel et al., 2003).The ANCOVA allowed comparison of the means acrossthe different conditions using t statistics. The resultingmap of t values constituted a statistical parametric map(Friston et al., 1995a).

The results were analysed both using a comparison tothe reference task and on the other hand, subtracting theforeign language from the mother tongue and vice versa(cognitive subtraction). Voxels were identified as signifi-cantly activated if they passed the height threshold ofZ = 3.72 (p < 0.0001) and at least belonged to a cluster of33 activated voxels (p < 0.05, corrected for multiple com-parisons) (Friston et al., 1994). The results were as follows:

5.2.2.1. High imagery word pairs: encoding. During encod-ing in the foreign language the prefrontal cortex (BA 10)was activated on both sides (right: Z = 4.46, leftZ = 3.90), whereas the orbitofrontal cortex (BA 11) wassignificantly active only on the left side (Z = 4.03). The hip-pocampal formation was bilaterally activated (right:Z = 3.44, left: Z = 4.50). Furthermore, the angular/supra-marginal gyrus (BA 39) was active on the left side(Z = 3.95) and the precuneus (BA 7) on the right side(Z = 3.68). Encoding high imagery word pairs in one’s

mother tongue resulted in a bilateral hippocampal acti-vation (right: Z = 3.44, left: Z = 4.59) and a predomi-nantly right orbitofrontal activation (BA 11) (Z = 3.80)(see Table 1).

5.2.2.2. High imagery word pairs: retrieval. Both, the retrie-val of word pairs in the foreign language and in one’smother tongue resulted in bilateral increases in rCBF inthe precuneus (English: BA 7: bilateral Z = 6.35; Finnish:BA 7: right Z = 3.94, left Z = 4.84) and in the prefrontalcortex (English: BA 10: right Z = 6.77, BA 10/11: leftZ = 4.54; Finnish: BA 10/11: right Z = 5.65, BA 10: leftZ = 4.75) (Fig. 2 and Table 2). In the foreign language,there was additionally a significant increase in rCBF inthe right angular and supramarginal gyri (BA 39/40:Z = 4.83) (Fig. 2a).

Table 2Encoding of words with low imagery content compared to referencecondition

Talairach coordinates Z BA Region

x y z

Foreign language

36 46 32 4.37 9 Prefrontal cortex (right)�20 48 0 3.72 10 Prefrontal cortex (left)�4 �38 28 4.08 31 Cingulate gyrus (left)

4 �78 56 4.02 7 Precuneus (right)

Mother tongue

18 62 4 3.24 10 Prefrontal cortex (right)�48 16 �12 3.50 47 Prefrontal cortex (left)

0 �62 �28 3.53 Cerebellum, vermis

Table 3Retrieval of words with high imagery content compared to referencecondition


Z BA Region

x y z

Foreign language

18 54 0 6.77 10 Prefrontal cortex (right)14 16 �16 4.03 11 Prefrontal cortex (right)�22 48 0 4.54 10/11 Prefrontal cortex (left)

60 �54 28 4.83 39/40 Angular/supramarginal gyrus (right)0 �78 44 6.35 7 Precuneus (bilateral)

Mother tongue

20 54 �4 5.65 10 Prefrontal cortex (right)�14 56 �12 4.75 10/11 Prefrontal cortex (left)�4 �14 20 5.50 25 Cingulate gyrus (left)12 �72 36 3.94 7 Precuneus (right)�8 �76 48 4.84 7 Precuneus (left)�12 �36 �20 4.93 Cerebellum (left)


The cognitive subtraction ‘‘foreign language minusmother tongue’’ just passed the height threshold andshowed (Fig. 3a and Table 5) right-sided activation of thelower medial temporal area (BA 20, Z = 3.76). In contrast,retrieval of native words activated the left cingulate gyrus(BA 25, Z = 5.50) and the left cerebellar hemisphere(Z = 4.93). The cognitive subtraction ‘‘mother tongueminus foreign language’’ showed an activation of Broca’sarea (BA 45: left activation Z = 4.50) (Fig. 3b and Table3) and in the precuneus on the right side (BA 7: Z = 3.84).

5.2.2.3. Low imagery words: encoding. As a shared neuralsubstrate of both languages, the prefrontal cortex (BA10/47) was bilaterally activated (English: BA 9/10, right:Z = 4.37, left: Z = 3.72; Finnish: BA 10/47, right:Z = 3.24, left: Z = 3.50). Encoding the word pairs in Eng-lish resulted in additional activations in the left cingulategyrus (BA 31) (Z = 4.08) and the right precuneus (BA 7;Z = 4.02). In contrast, the cerebellar vermis (Z = 3.53)and the right secondary visual cortex (BA 19; Z = 4.43)were active in the native language condition (Table 3).

Fig. 3. Comparison of adjusted mean rCBF in ten subjects betweenretrieval of word pairs and reference. Spatial distributions of significantvoxels are shown as integrated projections along sagittal, coronal andtransverse views of the brain. Retrieval of high imagery word pairs:Foreign language (a) and native language (b) compared against referencecondition.

5.2.2.4. Low imagery words: retrieval. The precuneus(English: left precuneus, BA 7: Z = 5.76; Finnish: BA 7,bilateral activation, Z = 5.16), prefrontal cortex (English:bilateral prefrontal cortex, BA 10/11: right, Z = 6.69; BA10: left, Z = 5.71; Finnish: right prefrontal cortex, BA 10:Z = 4.95) serve as common structures in the retrieval ofabstract word pairs in the native and foreign language.Retrieval of foreign word pairs resulted in additional acti-vations in the left cingulate gyrus (BA 29: Z = 4.13). Thecognitive subtraction ‘foreign language minus native lan-guage’ indicated activation of the left-sided medial frontalgyrus (BA 8, Z = 5.41). In contrast, retrieving the wordpairs in one’s mother tongue activated the right cerebellarhemisphere (Z = 4.99) (Fig. 4 and Table 4).

The cognitive subtraction ‘mother tongue minus foreignlanguage’ showed activation of Broca’s area (BA 44: leftactivation Z = 4.42) (Fig. 5 and Table 5).

Fig. 4. Comparison of adjusted mean rCBF in ten subjects betweenretrieval of word pairs and reference. Spatial distributions of significantvoxels are shown as integrated projections along sagittal, coronal andtransverse views of the brain. Retrieval of low imagery word pairs:Foreign language (a) and native language (b) compared against referencecondition.

Table 4Retrieval of words with low imagery content compared to referencecondition

Talairach coordinates Z BA Region

x y z

Foreign language

18 52 �4 6.69 10/11 Prefrontal cortex (right)�22 48 0 5.71 10 Prefrontal cortex (left)�2 �44 20 4.13 29 Cingulate gyrus (left)�2 �78 48 5.76 7 Precuneus (left)

Mother tongue

20 56 �4 4.95 10 Prefrontal cortex (right)0 �80 44 5.16 7 Precuneus (bilateral)2 �54 �8 4.99 Cerebellum (right)

Fig. 5. Cognitive subtraction ‘‘foreign language (a) minus native language(b)’’: retrieval of low imagery words. Spatial distributions of significantvoxels are shown as integrated projections along sagittal, coronal andtransverse views of the brain.

Table 5Retrieval of word pairs as studied with cognitive subtraction


Z BA Region

x y z

Retrieval of high imagery word pairs (foreign language – mother tongue)

50 �16 �28 3.76 20 Lower medial temporal area (right)

Retrieval of low imagery word pairs (foreign language – mother tongue)

�30 24 56 5.41 8 Medial frontal gyrus (left)

Retrieval of high imagery word pairs (mother tongue – foreign language)

�54 4 12 4.50 45 Broca’s area4 �52 72 3.84 7 Precuneus (right)

Retrieval of low imagery word pairs (mother tongue – foreign language)

�54 8 8 4.42 44 Broca’s area


The results of our encoding paradigm confirm previousfindings which emphasise the role of the prefrontal cortexand the hippocampal formation (Blaxton et al., 1996; Hals-

band et al., 1998; Kapur et al., 1994; Krause et al., 1999a,b;Squire et al., 1992). The pivotal role of hippocampus inmemory processes has been extensively documented(Eldridge et al., 2000; Mellet et al., 2000; Schacter et al.,1999).

Our study (Halsband et al., 2002) showed common cor-tical structures in the retrieval of Finnish and English wordpairs in (1) the precuneus, and (2) prefrontal cortex. Withreference to the precuneus, findings underline the impor-tant role of this structure as a module subserving verbalmemory and retrieval independent of the language usedand the imagery content of the presented material. Resultssupport the hypothesis of Fabbro (1999) which suggeststhat the cortical representations of different languages inbi/multilingual subjects partly overlap. This does notexclude the possibility that within the same cortical areasdistinct neural circuits independently subserve different lan-guage sets. Overlapping mechanisms are also in agreementwith the results obtained with electro-cortical stimulationduring neurosurgical operations (Ojemann, 1991; Ojemannand Whitaker, 1978).

Furthermore, a consistent prefrontal activation wasfound during encoding and retrieval in all but one experi-mental condition (encoding high imagery words in Finn-ish). It remains unclear why in only one condition ourfindings failed to reach significance. In all of our previousstudies (e.g. Halsband et al., 1998; Krause et al., 1999a,b;Schmidt et al., 2002) and in 7/8 experimental conditionsof the present investigation, the prefrontal cortex wasactive. These findings are in agreement with existing datafrom animals and humans (Buckner et al., 1995; Fuster,1995; Goldman-Rakic, 1987; Goldman-Rakic et al., 1992;Halsband et al., 1998; Squire et al., 1992; Tulving et al.,1994a,b) and with neuropsychological studies of braindamaged patients (Milner et al., 1985; Moscovitch, 1992;Paradis, 1994; Schacter, 1996; Warrington and Weiskrantz,1982). The common denominator of these studies is thepivotal role of prefrontal cortex in declarative memory.

Brain mechanisms of the two languages showed also dif-ferential activations in Broca’s area and in the cerebellumas well as in the angular/supramarginal gyri according tothe language used (see below).

5.2.2.5. Dorsolateral prefrontal cortex. Our results showedthat bilateral activity patterns are observed during retrievalphases with predominance for activity in the non-dominanthemispheres in the prefrontal structures. The presentfindings can only be partly accounted for by the modelof hemispheric encoding/retrieval asymmetry (HERA).The HERA model (Tulving et al., 1994a) states that theleft and right prefrontal cortices are disproportionatelyinvolved in the encoding and retrieval of episodic memo-ries, respectively. According to HERA, the left prefrontalcortex is more involved than the right prefrontal cortexin episodic memory encoding, whereas the right prefrontalcortex is more involved than the left prefrontal cortexin episodic memory retrieval. The findings of our study


confirm the conclusion put forth by Fletcher and Henson(2001) ‘‘The HERA generalisation may not be sufficient,however, in that our review included many studies of ver-bal retrieval that activate both left and right frontal cortex,or even left frontal cortex alone’’. In another review, Leeet al. (2000) concluded that between one third and a halfof all functional neuroimaging studies of episodic memoryencoding do not adhere to the HERA pattern.

Recently, Owen (2003) correctly put forth the criticalremark that in order to establish how specific frontalregions are specialised for particular memory sub-processesone has to put forth a greater commitment to such doubledissociation methodology than it is usually currently therule. Our findings are in line with the view that interhemi-spheric interactions play a crucial role during the retrievalof both native and foreign word pairs. The results are inaccordance with other studies which suggest that the origi-nal HERA model underestimated the role of the leftprefrontal cortex during memory retrieval (e.g. Buckner,1996; Halsband et al., 1998; Lepage et al., 2000). Thispoints to the necessity for a revision of the retrieval-relatedaspects of the HERA model.

Category-related premotor and prefrontal correlates oflexical retrieval have been reported on other studies (e.g.Damasio et al., 1996; Grabowski et al., 1998; Martinet al., 1996). As the prefrontal processing of bilingual wordpairs is concerned, our study did not show a significant dif-ference between the categories ‘‘high imagery content’’ and‘‘low imagery content’’. This applies both to the mothertongue and the foreign language.

5.2.2.6. Broca’s area. Broca’s area (BA 44, 45) was acti-vated both with the retrieval of concrete and abstractwords as the cognitive subtraction mother tongue minusforeign language was carried out. This finding will empha-sise the role of Broca’s area in the retrieval of native words,irrespective of the fact whether they are concrete orabstract. In the present study, no activation of Broca’s areawas found as foreign words were retrieved from memory.As for the mother tongue, our findings support the resultsobtained by Kim et al. (1997) who showed with fMRI thatBroca’s area is activated with the native language. On theother hand, there are also differences: Kim et al. (1997)showed that within the frontal-lobe language-sensitiveregions (Broca’s area) foreign languages acquired in adult-hood are spatially separated from native languages. Thedifference between our results and those of Kim et al.(1997) may be reconciled in part by the higher spatial res-olution of the fMRI technique as compared to PET. Inaddition, using SPM analysis the results of several subjectswere combined and averaged. This further reduces theeffective resolution since individual variations in the local-isation of the language areas were not taken adequatelyinto account. Another crucial difference was that the para-digm used by Kim et al. (1997) was based on internalspeech describing events that occurred during a specifiedperiod of the previous day. In contrast, in the present

study, the retrieval of word pairs without syntax was inves-tigated. One may argue that distinct activations withinBroca’s area for native and second languages could bedependent on the use of different syntactic conditionsrather than on the processing of phonetic structures ofthe different languages. This hypothesis is in accordancewith the brain imaging study by Klein et al. (1995). Theaim of their study was to investigate the neural substratesunderlying phonological or semantic word generation inbilingual English-French speaking subjects. Their resultssuggest common neural substrates in phonological andsemantic word generation tasks irrespective of whethersubjects used their mother tongue or a foreign language.

The subtraction analysis of the two languages revealedthat in Finnish the cerebellum and Broca’s area were moreactivated than in English. This interesting finding deservesfurther investigations. It remains unclear whether thelinguistic/phonological characteristics of the Finnishlanguage are more demanding or whether the native lan-guage in general uses more sophisticated networks forword production. Further experiments are needed to ana-lyse the neurolinguistical aspects of these languages undermore complex experimental conditions using whole sen-tence constructions.

5.2.2.7. Precuneus. This was the first study to show a con-sistent precuneus activation during memory retrieval ofword pairs in different languages and for both highlyimageable and abstract words. Our results indicate a signif-icant and predominantly bilateral activation of the precu-neus under all experimental conditions using differentlanguages and irrespective of the imagery content of theword pair associates.

The results are in agreement with earlier brain imagingstudies which showed a precuneus activation during verbalmemory retrieval using the native language (Fletcher et al.,1995a,b; Halsband et al., 1998; Krause et al., 1999b;Mottaghy et al., 1999; Shallice et al., 1994). The precuneusactivation occured for words with high and low imagerycontent and during visual and auditory presentationmodalities (Krause et al., 1999b). Our results extend theexisting evidence and emphasise the role of precuneus forboth foreign and native word pairs.

In spite of extensive information about lesions of theparietal lobe in various neurological disorders there are rel-atively few data about specific lesions of the precuneus(Cabeza et al., 1997; Ross, 1980). However, there is ana-tomical evidence indicating that precuneus has connectionswith prefrontal (Goldman-Rakic, 1988; Petrides and Pan-dya, 1984) and with temporal, occipital and thalamic areas(Blum et al., 1950; Pribram and Barry, 1956). This connec-tivity creates the basis for the functional concerted actionof precuneus during retrieval.

5.2.2.8. Angular/supramarginal gyri, cingulate areas. Angu-lar and supramarginal gyri are activated only when foreignwords with high imagery content are retrieved. It has been


shown (Price et al., 1999) that switching the input languageresults in the activation of the supramarginal gyri, whichmay play an important role in the cognitive control of lan-guage processes. Using fMRI Yetkin et al. (1996) showedthat the number of activated pixels was greatest for the lan-guage in which the subject was least fluent. When nativeconcrete words or foreign abstract words are retrieved leftcingulate areas (BA 25 for native concrete words and BA29 for foreign abstract words) are activated. The functionalsignificance of these findings is open and further data areneeded. It has recently been shown that the anterior cingu-late areas in the vicinity of these areas participate in theonline monitoring of performance and error detection(Carter et al., 1998; Ochsner et al., 2001).

5.2.2.9. Cerebellum. There is significant cerebellar activa-tion only concerning the retrieval of concrete and abstractnative word pairs, whereas no cerebellar activation couldbe seen as foreign words were retrieved. This may referto overlearnt automatic motor patterns associated withthe mother tongue. The present results are in agreementwith our earlier findings which indicated cerebellar activa-tion during the retrieval of visually presented word pairassociates (Halsband et al., 1998). Clinical lesion studiessupport the view of a critical role of the cerebellum inhigher cognitive function (Bracke-Tolkmitt et al., 1989;Fiez et al., 1992).

In the present investigation the brain areas of the twolanguages shared common components though differentialactivation patterns were found in Broca’s area, the cerebel-lum and the angular/supramarginal gyri. Finnish and Eng-lish used in the present study represent widely differentlinguistic groups, non-Indo-European vs. Indo-European.We presented the word pairs in the nominative case inorder to avoid the extensive morphology of the Finnishlanguage with 14 cases for each noun (Laine et al., 1994)and to exclude unnecessary variation. Similarly, Kleinet al. (1999) carried out a PET study on the cerebral orga-nisation of Chinese-English bilingual subjects. They arguedfor shared neural substrates even for such contrasting lan-guages as Mandarin Chinese (non-Indo-European) andEnglish (Indo-European).

5.2.3. General comments

Recent evidence suggests that experience through learn-ing partly determines the development and organisation ofthe human brain. In particular language experience seemsto influence the functional organisation of language-rele-vant systems.

There is evidence that cortical cell assemblies represent-ing action verbs include additional areas in motor and pre-motor cortices (Dehaene, 1995; Pulvermuller et al., 1999).In our study (Halsband et al., 2002) we used neutral, non-emotional nouns; however, it is difficult to assess the emo-tional value of the words; different subjects may react invarious ways to the same words due to their own personallife-time memories (Dolan et al., 2000).

Further studies are needed to clarify the cerebral repre-sentation of the second language by systematically varyingage of acquisition, levels of proficiency, and language expo-sure (Moreno and Kutas, 2005). There is recent evidencethat the proficiency level may play a larger role as com-pared to the age of acquisition in the cerebral representa-tion of semantic processing (Klein et al., 2006a,b; Peraniet al., 1998; Wartenburger et al., 2003).

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