Functional separation of languages in the bilingual brain: a comparison of electrical stimulation language mapping in 25 bilingual patients and 117 monolingual control patients

OBJECT: The aim of this investigation was to address three questions in bilingualism research: 1) are multiple languages functionally separated within the bilingual brain; 2) are these languages similarly organized; and 3) does language organization in bilinguals mirror that in monolinguals? 9: During awake dominant-hemisphere craniotomy in each of 25 bilingual patients, the authors mapped both languages by using identical object-naming stimuli. Essential sites for primary (L1) and secondary (L2) languages were compared. Sites were photographically recorded and plotted onto an anatomically referenced grid system. Language organization in bilinguals was then compared with that in 117 monolinguals and 11 monolingual children. CONCLUSIONS: The authors found distinct language-specific sites as well as shared sites that support both languages. The L1 and L2 representations were similar in total cortical extent but significantly different in anatomical distribution. The L2-specific sites were located exclusively in the posterior temporal and parietal regions, whereas the L1 and shared sites could be found throughout the mapped regions. Bilinguals possessed seven perisylvian language zones, in which L2 sites were significantly underrepresented when compared with the distribution of language sites in monolinguals. These L2-restricted zones overlapped the primary language areas found in monolingual children, indicating that these zones become dedicated to L1 processing. These findings support three conclusions. First, it is necessary to map both languages in bilinguals because L1 and L2 sites are functionally distinct. Second, differences exist in the organization of L1 and L2 sites, with L2-specific sites located exclusively in the posterior temporal and parietal lobes. Third, language organization comparisons in bilingual and monolingual brains demonstrate the presence of L2-restricted zones, which are dedicated to L1.     

Segregating semantic and syntactic aspects of processing in the human brain: an fMRI investigation of different word types

The processing of single words that varied in their semantic (concrete/abstract word) and syntactic (content/function word) status was investigated under different task demands (semantic/ syntactic task) in an event-related functional magnetic resonance imaging experiment. Task demands to a large degree determined which subparts of the neuronal network supporting word processing were activated. Semantic task demands selectively activated the left pars triangularis of the inferior frontal gyrus (BA 45) and the posterior part of the left middle/superior temporal gyrus (BA 21/22/37). In contrast, syntactic processing requirements led to an increased activation in the inferior tip of the left frontal operculum (BA 44) and the cortex lining the junction of the inferior frontal and inferior precentral sulcus (BA 44/6). Moreover, for these latter areas a word class by concreteness interaction was observed when a syntactic judgement was required. This interaction can be interpreted as a prototypicality effect: non-prototypical members of a word class, i.e. concrete function words and abstract content words, showed a larger activation than prototypical members, i.e. abstract function words and concrete content words. The combined data suggest that the activation pattern underlying word processing is predicted neither by syntactic class nor semantic concreteness but, rather, by task demands focusing either on semantic or syntactic aspects. Thus, our findings that semantic and syntactic aspects of processing are both functionally distinct and involve different subparts of the neuronal network underlying word processing support a domain-specific organization of the language system.     

Bilingualism tunes the anterior cingulate cortex for conflict monitoring

Monitoring and controlling 2 language systems is fundamental to language use in bilinguals. Here, we reveal in a combined functional (event-related functional magnetic resonance imaging) and structural neuroimaging (voxel-based morphometry) study that dorsal anterior cingulate cortex (ACC), a structure tightly bound to domain-general executive control functions, is a common locus for language control and resolving nonverbal conflict. We also show an experience-dependent effect in the same region: Bilinguals use this structure more efficiently than monolinguals to monitor nonlinguistic cognitive conflicts. They adapted better to conflicting situations showing less ACC activity while outperforming monolinguals. Importantly, for bilinguals, brain activity in the ACC, as well as behavioral measures, also correlated positively with local gray matter volume. These results suggest that early learning and lifelong practice of 2 languages exert a strong impact upon human neocortical development. The bilingual brain adapts better to resolve cognitive conflicts in domain-general cognitive tasks.     

Human temporal lobe activation by speech and nonspeech sounds

Functional organization of the lateral temporal cortex in humans is not well understood. We recorded blood oxygenation signals from the temporal lobes of normal volunteers using functional magnetic resonance imaging during stimulation with unstructured noise, frequency-modulated (FM) tones, reversed speech, pseudowords and words. For all conditions, subjects performed a material-nonspecific detection response when a train of stimuli began or ceased. Dorsal areas surrounding Heschl's gyrus bilaterally, particularly the planum temporale and dorsolateral superior temporal gyrus, were more strongly activated by FM tones than by noise, suggesting a role in processing simple temporally encoded auditory information. Distinct from these dorsolateral areas, regions centered in the superior temporal sulcus bilaterally were more activated by speech stimuli than by FM tones. Identical results were obtained in this region using words, pseudowords and reversed speech, suggesting that the speech-tones activation difference is due to acoustic rather than linguistic factors. In contrast, previous comparisons between word and nonword speech sounds showed left-lateralized activation differences in more ventral temporal and temporoparietal regions that are likely involved in processing lexical-semantic or syntactic information associated with words. The results indicate functional subdivision of the human lateral temporal cortex and provide a preliminary framework for understanding the cortical processing of speech sounds.     

Language control and lexical competition in bilinguals: an event-related FMRI study

Language selection (or control) refers to the cognitive mechanism that controls which language to use at a given moment and context. It allows bilinguals to selectively communicate in one target language while minimizing the interferences from the nontarget language. Previous studies have suggested the participation in language control of different brain areas. However, the question remains whether the selection of one language among others relies on a language-specific neural module or general executive regions that also allow switching between different competing behavioral responses including the switching between various linguistic registers. In this functional magnetic resonance imaging study, we investigated the neural correlates of language selection processes in German-French bilingual subjects during picture naming in different monolingual and bilingual selection contexts. We show that naming in the first language in the bilingual context (compared with monolingual contexts) increased activation in the left caudate and anterior cingulate cortex. Furthermore, the activation of these areas is even more extended when the subjects are using a second weaker language. These findings show that language control processes engaged in contexts during which both languages must remain active recruit the left caudate and the anterior cingulate cortex (ACC) in a manner that can be distinguished from areas engaged in intralanguage task switching.     

Mental addition in bilinguals: an FMRI study of task-related and performance-related activation

Behavioral studies show that bilinguals are slower and less accurate when performing mental calculation in their nondominant (second; L2) language than in their dominant (first; L1) language. However, little is known about the neural correlates associated with the performance differences observed between bilinguals' 2 languages during arithmetic processing. To address the cortical activation differences between languages, the current study examined task-related and performance-related brain activation during mental addition when problems were presented auditorily in participants' L1 and L2. Eleven Chinese-English bilinguals heard 2-digit addition problems that required exact or approximate calculations. Functional magnetic resonance imaging results showed that auditorily presented multidigit addition in bilinguals activates bilateral inferior parietal and inferior frontal regions in both L1 and L2. Language differences were observed in the form of greater activation for L2 exact addition in the left inferior frontal area. A negative correlation between brain activation and behavioral performance during mental addition in L2 was observed in the left inferior parietal area. Current results provide further evidence for the effects of language-specific experience on arithmetic processing in bilinguals at the cortical level.     

Organization of language areas in bilingual patients: a cortical stimulation study

OBJECT: In an attempt to gain a better understanding of how multiple languages are represented in the human brain, the authors studied bilingual patients who underwent surgery for brain tumors, during which the authors mapped cortical language sites by using electrostimulation. METHODS: Reading, counting, and word retrieval tasks were studied in 12 right-handed bilingual patients with no language deficit. All bilingual patients were native to France. One patient spoke four languages. The patients constituted a nonhomogeneous group in terms of language proficiency or age of acquisition. Languages were evaluated and classified into three major groups, depending on proficiency and date of acquisition. Strict conditions of language site validation were applied, separating typical anomia sites from speech arrest or other language sites (such as hesitation sites). A total of 30 speech arrest sites, 16 anomia sites, and three sites of language difficulties (not typically classified as speech arrest) were found throughout the 26 language studies performed. Strict overlapping of language areas (for all language tasks) was found in five patients, whereas the remaining seven had at least one area that was language-specific and sometimes task-specific. Specific areas for a particular language were found for word retrieval tasks (anomia) in eight sites (50%) but also in six (20%) of the reading or counting sites (speech arrest), either in frontal (three patients) or in temporoparietal (four patients) regions. Among the four early bilingual patients tested (languages acquired before the age of 7 years), three had language-specific cortical areas. Interestingly, six patients in this series who had a discrepancy between two languages did not have more cortical areas devoted to the less proficient language (with acknowledgment of the limit in cortical exposure available for testing by the craniotomy). CONCLUSIONS: In this series, the authors found that bilingual patients could have common but also different cortical areas for both languages in temporoparietal areas and in frontal areas. In some cases, the authors found that language tasks such as counting, reading, or word retrieval in different languages can be sustained by language- and task-specific cortical areas. In bilingual patients, cortical mapping should ideally be performed using different language tasks in all languages in which the patient is fluent.     

Language localization with activation positron emission tomography scanning.

We report the first instance of the use of 3-dimensional magnetic resonance imaging anatomically correlated to positron emission tomography (PET) scanning to identify language areas in a patient with an arteriovenous malformation (AVM) in the posterior speech region. The patient was a 24-year-old right-handed woman with an angiographically proven AVM (3-4 cm) in the left mid-posterior second temporal convolution in whom a left intracarotid injection of sodium Amytal produced significant language disruption. A baseline PET cerebral blood flow study identified the AVM, and an activation PET scan performed during the reading and speaking of simple words showed increased activity in the left parastriate cortex (the second visual area), in the left posterior third frontal convolution (Broca's area), and in the left inferior and midtemporal gyri (Wernicke's area). Increased activity was also noted in the right and left transverse temporal (Heschl's) gyri, in the left precentral gyrus, in the left medial superior frontal gyrus (the supplementary motor area), and in the right cerebellum. We conclude that activation PET scanning is useful in the preoperative assessment of patients who harbor cerebral AVMs in classically described speech regions.     

Distinct frontal regions subserve evaluation of linguistic and emotional aspects of speech intonation

In addition to the propositional content of verbal utterances, significant linguistic and emotional information is conveyed by the tone of speech. To differentiate brain regions subserving processing of linguistic and affective aspects of intonation, discrimination of sentences differing in linguistic accentuation and emotional expressiveness was evaluated by functional magnetic resonance imaging. Both tasks yielded rightward lateralization of hemodynamic responses at the level of the dorsolateral frontal cortex as well as bilateral thalamic and temporal activation. Processing of linguistic and affective intonation, thus, seems to be supported by overlapping neural networks comprising partially right-sided brain regions. Comparison of hemodynamic activation during the two different tasks, however, revealed bilateral orbito-frontal responses restricted to the affective condition as opposed to activation of the left lateral inferior frontal gyrus confined to evaluation of linguistic intonation. These findings indicate that distinct frontal regions contribute to higher level processing of intonational information depending on its communicational function. In line with other components of language processing, discrimination of linguistic accentuation seems to be lateralized to the left inferior-lateral frontal region whereas bilateral orbito-frontal areas subserve evaluation of emotional expressiveness.     

Functional segregation within pars opercularis of the inferior frontal gyrus: evidence from fMRI studies of imitation and action observation

Recent neuroimaging studies have suggested that the inferior frontal gyrus (IFG) is important for action observation and imitation. In order to further explore the role of IFG in action observation and imitation, we pooled data from seven functional magnetic resonance imaging studies involving observation and imitation of simple finger movements performed in our laboratory. For imitation we found two peaks of activation in the pars opercularis, one in its dorsal sector and the other in its ventral sector. The dorsal sector of the pars opercularis was also activated during action observation, whereas the ventral sector was not. In addition, the pars triangularis was activated during action observation but not during imitation. This large dataset suggests a functional parcellation of the IFG that we discuss in terms of human mirror areas and the computational motor control architecture of internal models.     

Category-specific conceptual processing of color and form in left fronto-temporal cortex

To investigate the cortical basis of color and form concepts, we examined event-related functional magnetic resonance imaging (fMRI) responses to matched words related to abstract color and form information. Silent word reading elicited activity in left temporal and frontal cortex, where category-specific activity differences were also observed. Whereas color words preferentially activated anterior parahippocampal gyrus, form words evoked category-specific activity in fusiform and middle temporal gyrus as well as premotor and dorsolateral prefrontal areas in inferior and middle frontal gyri. These results demonstrate that word meanings and concepts are not processed by a unique cortical area, but by different sets of areas, each of which may contribute differentially to conceptual semantic processing. We hypothesize that the anterior parahippocampal activation to color words indexes computation of the visual feature conjunctions and disjunctions necessary for classifying visual stimuli under a color concept. The predominant premotor and prefrontal activation to form words suggests action-related information processing and may reflect the involvement of neuronal elements responding in an either-or fashion to mirror neurons related to adumbrating shapes.     

Conjoint and extended neural networks for the computation of speech codes: the neural basis of selective impairment in reading words and pseudowords

The computation of speech codes (i.e. phonology) is an important aspect of word reading. Understanding the neural systems and mech- anisms underlying phonological processes provides a foundation for the investigation of language in the brain. We used high-resolution three-dimensional positron emission tomography (PET) to investigate neural systems essential for phonological processes. The burden of neural activities on the computation of speech codes was maximized by three rhyming tasks (rhyming words, pseudowords and words printed in mixed letter cases). Brain activation patterns associated with these tasks were compared with those of two baseline tasks involving visual feature detection. Results suggest strong left lateralized epicenters of neural activity in rhyming irrespective of gender. Word rhyming activated the same brain regions engaged in pseudoword rhyming, suggesting conjoint neural networks for phonological processing of words and pseudowords. However, pseudoword rhyming induced the largest change in cerebral blood flow and activated more voxels in the left posterior prefrontal regions and the left inferior occipital-temporal junction. In addition, pseudoword rhyming activated the left supramarginal gyrus, which was not apparent in word rhyming. These results suggest that rhyming pseudowords requires active participation of extended neural systems and networks not observed for rhyming words. The implications of the results on theories and models of visual word reading and on selective reading dysfunctions after brain lesions are discussed.     

Sound to language: different cortical processing for first and second languages in elementary school children as revealed by a large-scale study using fNIRS

A large-scale study of 484 elementary school children (6-10 years) performing word repetition tasks in their native language (L1-Japanese) and a second language (L2-English) was conducted using functional near-infrared spectroscopy. Three factors presumably associated with cortical activation, language (L1/L2), word frequency (high/low), and hemisphere (left/right), were investigated. L1 words elicited significantly greater brain activation than L2 words, regardless of semantic knowledge, particularly in the superior/middle temporal and inferior parietal regions (angular/supramarginal gyri). The greater L1-elicited activation in these regions suggests that they are phonological loci, reflecting processes tuned to the phonology of the native language, while phonologically unfamiliar L2 words were processed like nonword auditory stimuli. The activation was bilateral in the auditory and superior/middle temporal regions. Hemispheric asymmetry was observed in the inferior frontal region (right dominant), and in the inferior parietal region with interactions: low-frequency words elicited more right-hemispheric activation (particularly in the supramarginal gyrus), while high-frequency words elicited more left-hemispheric activation (particularly in the angular gyrus). The present results reveal the strong involvement of a bilateral language network in children's brains depending more on right-hemispheric processing while acquiring unfamiliar/low-frequency words. A right-to-left shift in laterality should occur in the inferior parietal region, as lexical knowledge increases irrespective of language.     

Transcortical sensory aphasia due to a left frontal subcortical haemorrhage

A case of transcortical sensory aphasia caused by a cerebral haemorrhage in the left frontal lobe is presented. A 72-year-old right-handed woman was admitted to the hospital, with a history of acute onset of speech disturbance and headache. On initial assessment, her spontaneous speech was fluent. She had no difficulty initiating speech, articulated normally, and did not exhibit logorrhea. Her ability to repeat phonemes and short sentences (5-6 words) was fully preserved, however she had severe difficulty with visual recognition of words, and with aural comprehension at the word level, although she was able to read words aloud. Computed tomography and magnetic resonance imaging showed cerebral haemorrhage in the left frontal lobe, involving the superior and middle frontal gyrus. Single photon emission CT revealed a wider area of low perfusion over the entire left frontal lobe, including the superior, middle and inferior frontal gyrus. The aphasia symptoms, mainly poor comprehension, disappeared quickly several weeks after the event. This may have been due to a reduction in the size of the haematoma and a resolution of the oedema around the haematoma. Clinically, the transcortical sensory aphasia in this case was indistinguishable from that caused by damage to the posterior language areas. Further case reports of transcortical sensory aphasia associated with frontal lobe lesions would help to confirm whether a relatively rapid recovery is characteristic in cases such as this.     

When language meets action: the neural integration of gesture and speech

Although generally studied in isolation, language and action often co-occur in everyday life. Here we investigated one particular form of simultaneous language and action, namely speech and gestures that speakers use in everyday communication. In a functional magnetic resonance imaging study, we identified the neural networks involved in the integration of semantic information from speech and gestures. Verbal and/or gestural content could be integrated easily or less easily with the content of the preceding part of speech. Premotor areas involved in action observation (Brodmann area [BA] 6) were found to be specifically modulated by action information "mismatching" to a language context. Importantly, an increase in integration load of both verbal and gestural information into prior speech context activated Broca's area and adjacent cortex (BA 45/47). A classical language area, Broca's area, is not only recruited for language-internal processing but also when action observation is integrated with speech. These findings provide direct evidence that action and language processing share a high-level neural integration system.     

Discordance between functional magnetic resonance imaging during silent speech tasks and intraoperative speech arrest

OBJECT: The goal of this study was to investigate discordance between the location of speech arrest during awake cortical mapping, a common intraoperative indicator of hemispheric dominance, and silent speech functional magnetic resonance (fMR) imaging maps of frontal language function. METHODS: Twenty-one cases were reviewed retrospectively. Images of silent speech fMR imaging activation were coregistered to anatomical MR images obtained for neuronavigation. These were compared with the intraoperative cortical photographs and the behavioral results of electrocorticography during awake craniotomy. An fMR imaging control study of three healthy volunteers was then conducted to characterize the differences between silent and vocalized speech fMR imaging protocols used for neurosurgical planning. CONCLUSIONS: Results of fMR imaging showed consistent and predominant activation of the inferior frontal gyrus (IFG) during silent speech tasks. During intraoperative mapping, however, 16 patients arrested in the precentral gyrus (PRG), well posterior to the fMR imaging activity. Of those 16, 14 arrested only in the PRG and not in the IFG as silent speech fMR imaging predicted. The control fMR imaging study showed that vocalized speech fMR imaging shifts the location of the fMR imaging prediction to include the motor strip and may be more appropriate for neurosurgical planning.     

Word reading and posterior temporal dysfunction in amnestic mild cognitive impairment

Patient studies that combine functional magnetic resonance imaging with chronometric analysis of language dysfunction may reveal the critical contribution of brain areas to language processes as well as shed light on disease pathogenesis. In amnestic mild cognitive impairment (MCI), a prodromal stage of Alzheimer's disease, we examined whether the brain system for associative-semantic judgments with words or with pictures is affected and how this relates to off-line chronometric analysis of word reading and picture naming. A consecutive memory clinic-based series of 13 amnestic MCI patients as well as 13 matched controls participated. One area, the lower bank of the posterior third of the left superior temporal sulcus (STS), showed a significant group-by-task interaction: In controls, it was activated during the associative-semantic condition with words compared with the visuoperceptual control condition but not when the same tasks were compared with pictures as input. In MCI, this word-specific activation was significantly reduced. Response amplitude correlated (r = 0.90) with the steepness of the slope of the time-accuracy curve for word reading. Our data provide converging evidence for a critical contribution of the lower bank of the left posterior STS to mapping word form onto word meaning (lexical-semantic retrieval).     

The role of semantics and grammatical class in the neural representation of words

On the basis of neuropsychological and functional imaging evidence, meaning and grammatical class (particularly the verb-noun distinction) have been proposed as organizational principles of linguistic knowledge in the brain. However, previous studies investigating verb and noun processing have been confounded by the presence of systematic correlations between word meaning and grammatical class. In this positron emission tomography study, we investigated implicit word processing using stimuli that allowed the effects of semantic and grammatical properties to be examined independently, without grammatical-semantic confounds. We found that left hemisphere cortical activation during single-word processing was modulated by word meaning, but not by grammatical class. Motor word processing produced significant activation in left precentral gyrus, whereas sensory word processing produced significant activation in left inferior temporal and inferior frontal regions. In contrast to previous studies, there were no effects of grammatical class in left inferior frontal gyrus (IFG). Instead, we found semantic-based differences within left IFG: anterior, but not posterior, left IFG regions responded preferentially to sensory words. These findings demonstrate that the neural substrates of implicit word processing are determined by semantic rather than grammatical properties and suggest that word comprehension involves the activation of modality-specific representations linked to word meaning.     

Temporal dissociation of early lexical access and articulation using a delayed naming task--an FMRI study

Neuroimaging studies of overt speech hold an important practical advantage allowing monitoring of subject performance, particularly valuable in disorders like aphasia. However, speech production is not a monotonic process but a complex sequence of stages. Levelt and colleagues have described these as roughly corresponding to two originally independent systems--conceptual and sensorimotor--that are linked in the formulation and expression of spoken language. In the initial stages a word is chosen to match a concept (lexical selection); in the later stages the sound and motor patterns are encoded and the word is uttered (articulation). It has been difficult to discriminate these stages using conventional neuroimaging techniques. We designed a functional magnetic resonance imaging study in an attempt to do this, by introducing a latency into a conventional naming paradigm, delaying the articulated response. Our results showed that left hemisphere perisylvian areas were active throughout, interacting with visual and heteromodal areas during early lexical access and with motor and auditory areas during overt articulation. These results are consistent with the broadest version of the Levelt model and with that derived from Chomsky's minimalist program in which a core language system interacts with conceptual-intentional systems and articulatory-perceptual systems during the early and late stages of lexical access respectively.