Brain & Language 121 (2012) 124–129

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Brain & Language

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The contribution of functional near-infrared spectroscopy (fNIRS)to the presurgical assessment of language function in children

Anne Gallagher a, Renée Béland b,c, Maryse Lassonde b,c,⇑a Harvard Medical School;Carol and James Herscot Center for Tuberous Sclerosis Complex, Department of Neurology;Massachusetts General Hospital, Boston, MA, USAb Centre de Recherche en Neuropsychologie et Cognition, Université de Montréal, Montreal, Quebec, Canadac Centre de Recherche de l’Hôpital Sainte-Justine, Center Hospitalier Universitaire Sainte-Justine, Montreal, Quebec, Canada

a r t i c l e i n f o a b s t r a c t

Article history:Accepted 21 March 2011Available online 21 April 2011

Keywords:Optical imagingChildrenSpeech lateralizationNeurological diseaseEpilepsySurgeryIntracarotid amobarbital testFunctional magnetic resonance imagingBrain mapping

0093-934X/$ - see front matter � 2011 Elsevier Inc. Adoi:10.1016/j.bandl.2011.03.006

⇑ Corresponding author. Address: Département dMontréal, C.P. 6128, Succ. Centre-Ville, Montreal, Qc.,343 5787.

E-mail address: maryse.lassonde@umontreal.ca (M

Before performing neurosurgery, an exhaustive presurgical assessment is required, usually including aninvestigation of language cerebral lateralization. Among the available procedures, the intracarotid amo-barbital test (IAT) was formerly the most widely used. However, this procedure has many limitations: it isinvasive and potentially traumatic, especially for children. To overcome these limitations, neuroimagingtechniques such as functional magnetic resonance imaging (fMRI) have been used. Again, these methodsare difficult to use with children, who must remain motionless during data acquisition. Functional near-infrared spectroscopy (fNIRS) is a noninvasive functional imaging technique that is easily applied to pedi-atric and cognitively limited patients. It has been used recently in epileptic children for presurgicalassessment of expressive and receptive language brain lateralization. The aim of this review is to presentthe contribution of fNIRS to the presurgical assessment of language function in children with neurologicaldiseases.

� 2011 Elsevier Inc. All rights reserved.

1. Introduction gery, various presurgical techniques have been developed to assess

In most individuals, functional integrity of the left cerebralhemisphere is required to produce and understand language.When the left hemisphere has been injured or exposed to chronicdeleterious episodes, language function reorganization is likely tooccur, especially when these events occur at a young age (Rasmus-sen & Milner, 1977). Language functions can then be taken over bythe right hemisphere or both hemispheres. Accordingly, individu-als with brain abnormalities show greater language dominancevariety than healthy individuals (e.g., Berl et al., 2005). Childrenwith neurological diseases such as refractory epilepsy, tumors, orcortical vascular malformations sometimes require neurosurgery.These procedures can result in neuropsychological deficits thatare often specific to the resected area. For example, left frontal ortemporal lobe resection may induce aphasia or word finding diffi-culties. The latter can then lead to learning difficulties as well asacademic, social, and occupational problems (Dodrill & Clemmons,1984; Helmstaedter, Gleissner, Zentner, & Elger, 1998; Mayeux,Brandt, Rosen, & Benson, 1980). Prevention of such deficits istherefore essential. To minimize the risk of postsurgical languagedeficits in individuals who undergo left frontal or temporal sur-

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e Psychologie, Université deCanada H3C 3J7. Fax: +1 514

. Lassonde).

language cerebral lateralization.Until recently, the intracarotid amobarbital test (IAT) or Wada

test (Rutten, Ramsey, Van Rijen, Alpherts, & Van Veelen, 2002; Wada& Rasmussen, 1960) was the most widely used procedure to explorelanguage brain lateralization prior to neurosurgery. Sodium amytalis injected into one of the carotid arteries through a transfemoralcatheter (Loring, Lee, & Meader, 1994; Smith, 2001) to produce atemporary anesthesia in the ipsilateral cerebral hemisphere, duringwhich it is possible to assess language and memory functions of thecontralateral hemisphere. Language task results then provide a rel-atively reliable indication of language cerebral lateralization(Branch, Milner, & Rasmussen, 1964; DeVos, Wyllie, Geckler, Kota-gal, & Comair, 1995; Rouleau, Robidoux, Labrecque, & Denault,1997; Trenerry & Loring, 1995). However, this procedure is invasive,and its validity cannot be verified by test–retest studies (Boas, 1999).Nor does the IAT provide precise spatial information on languagelocalization (Gaillard, Bookheimer, Hertz-Pannier, & Blaxton,1997), and it is constrained by the timing variability of the sodiumamytal action (Bouwer, Jones-Gotman, & Gotman, 1993). Moreover,the patient’s altered state of consciousness and behavioral and emo-tional reactions can obscure the results (Terennery and Loring). Fi-nally, the technique is difficult to apply to young children(Williams & Rausch, 1992), a significant limitation considering thatan early surgical intervention is often crucial (Engel, 1987), and inpatients with mental retardation, or language and/or behavior prob-

A. Gallagher et al. / Brain & Language 121 (2012) 124–129 125

lems (Pelletier, Sauerwein, Lepore, St-Amour, & Lassonde, 2007),which are often found with neurological diseases (Jambaqué, Las-sonde, & Dulac, 2001). Given these considerable limitations andthe recent accessibility to safer alternative techniques, many centersworldwide have significantly reduced or halted their use of IAT inthe last 15 years (Baxendale, Thompson, & Duncan, 2008).

As alternatives to IAT, minimally invasive techniques such aspositron emission tomography (PET) (Hunter et al., 1999; Kaplanet al., 1999) and single photon emission computed tomography(SPECT) (Borbély et al., 2003) and recent noninvasive imaging tech-niques such as functional magnetic resonance imaging (fMRI)(Gaillard et al., 2004; Thiel et al., 1998) and magnetoencephalogra-phy (MEG) (Papanicolaou et al., 2004) have been used to investi-gate language dominance. However, as with IAT, thesetechniques are sometimes difficult to use in young children andpatients with serious cognitive or behavioral problems. It is diffi-cult if not impossible for young children to lie motionless in thescanner for a relatively long period of time. In addition, there isno way of verifying whether children are actually performing themental task as instructed, as they must remain silent during dataacquisition to avoid movement artefacts.

2. Functional near-infrared spectroscopy

Functional near-infrared spectroscopy (fNIRS) is a noninvasivefunctional imaging technique that is easily applied to pediatricand cognitively limited patients (e.g., Wilcox, Bortfeld, Woods,Wruck, & Boas, 2005). It allows measuring hemodynamic changes,which are used as an indicator of neural activity (Villringer, Plank,Hock, Schleinkofer, & Dirnagl, 1993). The different light absorptionspectra of oxy-hemoglobin (HbO) and deoxy-hemoglobin (HbR)within the near-infrared spectrum allow measuring concentrationchanges in these substances in living tissues, providing informa-tion on cerebral activation (Boas et al., 2001; Gratton & Fabiani,2007). A typical cerebral activation is characterized by a small,short decrease in HbO and an increase in HbR, known as the initialdip, and regional oxygenation, probably due to underlying neuro-nal activity. This is followed by a large increase in HbO concentra-tion accompanied by a decrease in HbR concentration in a givencerebral region, reflecting local arterial blood flow (Fig. 1a).

During fNIRS recording, near-infrared light of at least two wave-lengths between 680 and 1000 nm is directed through optic fibersto the patient’s head. The wavelengths and the number of wave-lengths used vary depending on the fNIRS equipment. Increasingthe number of wavelengths allows more accurate estimation ofHbO and HbR concentration changes. HbO is preferentially ab-sorbed by wavelengths closer to 680 nm and HbR by wavelengthscloser to 1000 nm. Light travels through the scalp and the skull to adepth of a few centimeters in the cerebral tissue following a bana-na shaped trajectory (Fig. 2). Light detectors are placed on the scalpa few centimeters away from the source. The closer the detector tothe source, the better the lateral spatial resolution, but the greaterthe distance between detector and source, the deeper the light canpenetrate. The distance between source and detector is thereforeset to obtain a good compromise between lateral and depth spatialresolution, typically at between 2 and 5 cm. The amount of de-tected light reflects the absorption of the two wavelengths in tar-geted cerebral areas. This allows using a modified Beer–LambertzLaw to quantify the relative HbO and HbR concentration changes(for a review see Minagawa-Kawai, Mori, Hebden, & Dupoux,2008). For a brief description of a complete fNIRS recording session(from material preparation to data analyses), see Shalinsky,Kovelman, Berends, and Petitto (2009).

User-friendly data analysis software has only recently becomeavailable for fNIRS users. Formerly, each research team developed

their own data analysis tools. This constituted a substantial obsta-cle for clinical fNIRS use. In the last decade, fNIRS equipment anddata analysis tools have developed rapidly. Software that enablethe analysis (e.g., normalization, filtering, averaging) and visualiza-tion of fNIRS data are now available, and some are publicly acces-sible on websites (e.g., HomER, Photon Migration ImagingLaboratory: http://www.nmr.mgh.harvard.edu/DOT/; and NIRS-SPM, Bio Imaging Signal Processing (BISP) laboratory: http://bisp.-kaist.ac.kr/NIRS-SPM.html). Moreover, they are relatively easy touse. Recent technical advances have greatly contributed to the ex-panded use of fNIRS for clinical applications.

3. Advantages and limitations of fNIRS

Like other imaging techniques, fNIRS has many advantages overIAT. For instance, fNIRS is a noninvasive technique that can beadministered to a patient repeatedly. As part of a presurgical lan-guage assessment, fNIRS not only investigates language brain later-alization, it also provides specific information on languagelocalization. Importantly, unlike other imaging methods (Gratton& Fabiani, 2001a; Gratton & Fabiani, 2001b; Strangman, Boas, &Sutton, 2002; Villringer & Chance, 1997), fNIRS imposes no majorrestrictions on movement during recording, which makes it suit-able for studies in mentally challenged individuals as well as youngchildren, including infants (Wilcox, Bortfeld, Woods, Wruck, &Boas, 2008; Wilcox et al., 2005). In contrast to fMRI and MEG, bothof which usually require covert articulation, the expressive lan-guage tasks used with fNIRS can involve overt articulation withoutthe physical constraints that impede articulatory gestures. Duringdata acquisition, the child is seated comfortably in a chair or onthe parent’s lap, allowing direct contact with the experimenter.Second, the equipment is portable, allowing bedside assessment(Hintz et al., 2001; Liebert et al., 2005), and is much less costly thanfMRI or PET. Third, fNIRS offers better temporal resolution thanfMRI, due to a much greater sampling rate (at least 10 Hz for fNIRScompared to 0.5 Hz for fMRI), so it can measure phenomena suchas early-phase deoxygenation in the activated cortex, called the‘‘initial dip.’’ Another advantage of fNIRS is that it appears to besensitive to bilateral speech patterns (Gallagher et al., 2007), whichare less efficiently detected with fMRI. In fact, fMRI has correctlylateralized language functions in both hemispheres in most cases,but appears to be less efficient in detecting bi-hemispheric speechorganization (Benke et al., 2006). Finally, fNIRS allows measuringindependent HbO and HbR concentration changes, unlike changesin the fMRI BOLD signal, which are based mainly on local magneticfield variations induced by HbR changes. HbR changes are thoughtto be proportional to changes in oxygen consumption, which resultfrom changes in cerebral blood flow (Raichle, 1998). Although sev-eral hemodynamic phenomena remain unclear, independent mea-sures of HbO and HbR concentration changes can provide a betterunderstanding of the physiology underlying language processingand cerebral reorganization patterns, which can be useful in pre-surgical assessment.

The main disadvantage of fNIRS is the shallow photon penetra-tion (between 3 and 5 cm). This impedes reliable data recording ofsubcortical structure activation (e.g., in the thalamus), and maymake it difficult to use in individuals with a dense skull and/orthick, dark hair. However, the limited penetration depth does nothave a major impact on studies investigating cortical areas suchas language areas.

4. fNIRS as an alternative technique for language investigation

fNIRS has been shown to allow functional brain lateralizationand localization of responses to auditory speech stimuli in healthy

Fig. 1. fNIRS data from a 9-years-old boy with epilepsy undergoing a language presurgical assessment using fNIRS. (a) The graph illustrates typical cerebral languageactivation characterized by a large increase in HbO concentration (thick lines) accompanied by a small decrease in HbR concentration (thin lines), larger in left Broca andWernicke areas (blue lines) compared to the homologous right counterparts (pink lines). The figure shows a 10-block-averaged time course, including baseline (�30 to 0 s),language task (0–30 s), resting period (30–60 s), control task (60–90 s), and resting period (90–105 s). Hemoglobin data represents an average of all channels covering theregions of interest, and are more pronounced in the language task than the control task. A typical initial dip (short reduction in HbO) is also observed before activation. Thishemoglobin pattern is characterized by a first and longer activation peaking at 27 s (see blue arrow) followed by a second shorter activation peaking at 52 s (see pink arrow).A similar hemoglobin pattern is observed in the mirror counterparts (pink lines) from an average of HbO and HbR data obtained from all channels placed over these regions. Itis noteworthy that the HbR pattern is characterized by a first very small increase in HbO (peaking at 25 s) followed by a cerebral activation at 52 s. The blue arrow shows thatthe maximal increase in HbO in the left hemisphere associated with the language task occurred approximately 27 s after baseline (5.19 lmol). The expressive languagelaterality index was calculated at this time (orange vertical line). The pink arrow indicates that the maximum increase in HbO elicited by the same task in the righthemisphere occurred at approximately 52 s after baseline. The right side of the figure (b) presents 3D reconstructions of the 9-years-old patient’s MRI with projected HbTdata. HbT data are typically shown on a 3D map because to represent the addition of HbO and HbR data, which cannot be clearly displayed simultaneously on a single brainreconstruction. Top panel: the left view shows an increase in HbT in Broca and Wernicke areas (average data from all channels covering this region during activation period:between 25 and 45 s). Bottom panel: an increase in HbT is also observed in right homologous regions (average data from all channels covering this region during activationperiod: between 45 and 60 s), but at lower amplitude. Data indicate a left-greater-than-right cerebral language activation in this young patient.

126 A. Gallagher et al. / Brain & Language 121 (2012) 124–129

and neurologically impaired adults (Kennan, Kim, Maki, Koizumi, &Constable, 2002; Noguchi, Takeuchi, & Sakai, 2002; Watanabeet al., 1998; Watson, Dodrill, Farrell, Holmes, & Miller, 2004) aswell as healthy and epileptic children (Bortfeld, Wruck, & Boas,2007; Gallagher, Bastien et al., 2008; Gallagher, Lassonde et al.,2008; Gallagher et al., 2007; Minawaga-Kawai et al., 2007) andhealthy infants (Bortfeld, Fava, & Boas, 2009; Saito et al., 2007).In adults, good correlation between fNIRS and fMRI or IAT was ob-tained in all studies that compared laterality indices between thesetechniques. For example, Kennan et al. showed that fNIRS can beused in healthy adults to assess activity lateralization in the pre-frontal area during semantic and syntactic decision tasks. Theauthors reported a strong correlation between laterality indicescalculated using fNIRS and fMRI in all six participants. In anotherstudy, Watanabe et al. showed perfect concordance between fNIRSand IAT language cerebral lateralization indices across six epilepticadults who performed a verbal fluency task during fNIRS recording.

In a pediatric population, Pena et al. (2003) performed bilateraltemporal fNIRS recordings in 12 sleeping full-term neonates (be-tween 2 and 5 days old at measurement). The children showedgreater left than right temporal activation while listening to a fe-male voice read a children’s story. Reverse backward speech and si-lent control conditions were also presented and were notassociated with hemispheric differences. This study provided thefirst evidence that left-hemisphere language specialization, similarto language brain lateralization found in healthy adults, is presentat birth in the human brain. Recently, Kotilahti et al. (2010) repli-cated this finding in a group of 13 infants aged between one and4 days. Wartenburger et al. (2007) used fNIRS and found right-

hemisphere cerebral specialization for processing prosodic infor-mation in 51 healthy 4-years-old children. Unlike left-hemispherelanguage lateralization, right-hemisphere cerebral organization forprosody processing does not seem to be established at birth (Saitoet al., 2007). Taken together, these studies confirm the usefulnessof fNIRS for exploring the neurobiology and organization of lan-guage development in the young human brain.

Only a few studies have used fNIRS to investigate languagebrain lateralization and localization in neurologically impairedchildren, and to date these studies have been conducted only inour laboratory. In the following sections, we present the contribu-tion of this relatively new technique to the presurgical assessmentof language function in children with neurological diseases. All ourstudies were performed using a frequency domain multi-channelImagent Oximeter (ISS Inc., Urbana–Champaign, USA) with 32sources operating at 680 nm, 32 sources operating at 830 nm,and eight photomultiplier detectors. Methodological details are gi-ven in the cited papers.

5. fNIRS investigation of expressive language in children

In our first study, we compared fNIRS results obtained whileparticipants performed an expressive language task with those ob-tained by fMRI and/or IAT in two healthy adults, two epilepticadults, and four epileptic children (Gallagher et al., 2007). Asemantic verbal fluency task was used. Participants had to nameas many items as possible in a specific category (e.g., colors, bodyparts, fruits), and had to continue as long as a visual cue remainedon a screen in front of them (30 s). fNIRS results showed left-hemi-

Fig. 2. Functional near-infrared spectroscopy uses an array of optic fiber sourcesand detectors distributed over the whole scalp or portions of the scalp coveringdefined areas of interest (see the picture in the bottom-right corner). As shown onthe larger image of the cerebral MRI, several near-infrared source lights (at leasttwo wavelengths between 680 and 1000 nm at each source location) are placed onthe patient’s scalp to allow light to travel through the scalp, the skull, and into thecerebral tissue. Light detectors are placed on the scalp a few centimeters (ideallybetween 2 and 5 cm) from the source. Red banana shaped trajectories illustratevolumes described by photons that reach the detectors. Other photons are absorbedby HbO, HbR, water, or other substances, are scattered away from the detectors, andtravel deep into the brain or leave the brain without reaching any fNIRS detectors.

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sphere language dominance in the two healthy adults and the twoadults with epilepsy. Left-hemisphere language dominance wasdemonstrated in three of the four epileptic children, whereas thefourth child showed bilateral activation in regions correspondingto Broca and Wernicke areas that was similar in both hemispheres.This suggests a bilateral speech representation that may have oc-curred through cerebral plasticity as a compensatory mechanism(see Fig. 1a for an illustration of the task procedure, the fNIRS datatime course, and a cerebral activation). We obtained concordanceof language dominance between both fNIRS and fMRI results andfNIRS and IAT results for all participants. We also obtained clearfNIRS results for two children for whom IAT and fMRI could notbe performed due to the very young age (3 years) of one childand a neurological condition (pervasive developmental disorderwith moderate mental deficiency) in the other. Although neitherchild was able to remain motionless during fNIRS data acquisition,this did not compromise the data analysis, which showed left-hemisphere speech dominance in both children, indicating thatfNIRS has high tolerance to body movement.

As part of the presurgical assessment, a 9-years-old boy with aprobable left temporal epileptic focus who could tolerate neitherIAT nor fMRI due to language problems and anxiety was assessedusing fNIRS (Gallagher, Bastien et al., 2008). Results of the semanticverbal fluency task showed left-hemisphere dominance, includingboth Broca and Wernicke areas, suggesting possible intrahemi-spheric cerebral reorganization for expressive language, as Wer-nicke area is typically activated in receptive language tasks (seeFig. 1 for illustrative results).

In another case study (Gallagher, Lassonde et al., 2008), weadministered the same language protocol to a 10-years-old right-handed epileptic boy as part of his presurgical assessment. IctalSPECT, PET, EEG-fMRI, and EEG-MEG results suggested a right fron-

tal ictal onset zone. Paradoxically, the neuropsychological assess-ment showed language deficits (word finding difficulties, slowverbal information planning and processing) and attentional prob-lems. Consequently, language cerebral lateralization was investi-gated using fNIRS. Although both left and right cerebralactivation was found during the expressive language task, activa-tion in the left inferior-posterior frontal gyrus (Broca area) wasgreater than in the right analogous region, suggesting left-hemi-sphere dominance for expressive language. No new language defi-cits appeared following the limited right frontal corticectomy,suggesting that the right-hemisphere activation measured withfNIRS was not mandatory for the language processing involved inthe expressive language task.

6. fNIRS investigation of receptive language in children

All previous fNIRS studies conducted in adults and childrenwith epilepsy have assessed expressive language cerebral localiza-tion or lateralization. However, for a complete language investiga-tion, presurgical assessment should provide information about notonly expressive but also receptive language processing. In an intactbrain, expressive language and receptive language are mainly asso-ciated with different cerebral areas: respectively Broca (pars operc-ularis and triangularis of the inferior frontal gyrus or Brodmann’sareas 44 and 45) and Wernicke (posterior section of the superiortemporal gyrus as well as infero-posterior part of the parietal lobeor Brodmann areas 22, 39, and 40) area. Thus, each language type(expressive and receptive) may be subject to different functionalreorganization patterns that could significantly influence postsur-gical cognitive and communicative outcomes if not taken intoaccount.

Receptive language paradigms may be easier to use than lan-guage tasks with young children and mentally challenged patients,because they do not usually require the subject to actively partic-ipate. We used a passive story listening task during fNIRS to assessreceptive language in a 9-years-old boy (Gallagher, Bastien et al.,2008; see previous section on patient information) as part of hispresurgical assessment. This receptive language task has been pro-ven reliable to assess receptive language localization (Paquetteet al., 2010), and we also obtained clear and reliable results. We re-corded bilateral temporo-frontal activation that was similar inboth hemispheres, suggesting possible intra- and interhemisphericcerebral reorganization for receptive language. This case report isthe first study to show the usefulness of fNIRS for investigatingreceptive language cerebral localization and lateralization in anepileptic child. However, more data are needed to validate the pro-tocol. A study involving a passive story listening task during fNIRSrecording in several adult and pediatric epileptic surgical candi-dates is currently underway at our laboratory.

7. Choice of language tasks

Many techniques for presurgical assessment of language brainlateralization are currently available. Regardless of the neuroimag-ing technique used, the choice of tasks to include in the experimen-tal protocol is crucial because the task needs to activate specificneural networks (Price, 2000). First, the task set must elicit reliablelanguage-related activity. More specifically, valid language tasksshould activate both expressive and receptive language processingareas, in the frontal and temporal lobes. The experiments must beadapted to the targeted clinical population, and should be as shortas possible to ensure that all patients can bear the procedure. Sim-ple tasks are preferable for pediatric and mentally challenged pop-ulations. Moreover, increasing complexity of language task wasshown to induce greater cerebral activation and a more bilateral

128 A. Gallagher et al. / Brain & Language 121 (2012) 124–129

activation pattern (Hertz-Pannier et al., 1997), which is unsuitablefor a language lateralization protocol. Hence, presurgical languageassessment protocols must be carefully designed, and include avariety of language tasks that can reliably assess language andcomprehensively assess language lateralization.

In the literature, several tasks were shown to be appropriate forlanguage brain lateralization in children, and results were congru-ent with those obtained with other language lateralization tools,such as fMRI, IAT, and cortical electrostimulation mapping. As anexpressive language task, a verb generation task was shown to in-duce strong inferior frontal activation in the dominant hemisphere(e.g., Hertz-Pannier et al., 1997). The above-described verbal flu-ency task is easier for young children than a verb generation task,and it is also suitable for language cerebral lateralization (Galla-gher, Bastien et al., 2008; Gallagher, Lassonde et al., 2008; Galla-gher et al., 2007). Receptive language was assessed duringneuroimaging recording using semantic or syntactic decision tasks(e.g., Binder et al., 1996; Kennan et al., 2002). Although these tasksare efficient for language brain lateralization, they are difficult foryoung children to perform. As an alternate child-friendly paradigm,a story listening task is very easy to perform and was shown to in-duce strong superior and middle temporal gyrus activation in thedominant cerebral hemisphere (e.g., Karunanayaka et al., 2007; Pa-quette et al., 2010).

8. Conclusion

The above-reported studies indicate that fNIRS has the potentialto become a viable, noninvasive alternative to the Wada Test fordetermining speech cerebral lateralization and localization in chil-dren and other clinical populations that have difficulty remainingmotionless or are reluctant to submit to more invasive techniques.Recent studies suggest that fNIRS is a reliable technique to investi-gate both expressive and receptive language in children. Despitethe tremendous work accomplished in recent years, many hard-ware, software, and data analysis tools remain to be developed.More studies in larger patient populations are needed, using para-digms that generate consistent results across centers, before fNIRScan be considered a clinical alternative to the Wada test for presur-gical exploration of language functions in children. Until such time,fNIRS is a promising technique that can be applied in combinationwith other noninvasive, child-friendly techniques such as neuro-psychological assessment and Doppler sonography (Knecht et al.,1998).

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