Relationship Between Task-Related Gamma Oscillations and BOLD Signal: New Insights From Combined fmri and Intracranial EEG
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1 Human Bain Mapping 28: (2007) Relationship Between Task-Related Gamma Oscillations and BOLD Signal: New Insights Fom Combined fmri and Intacanial EEG Jean-Philippe Lachaux, 1 * Piee Fonlupt, 1 Philippe Kahane, 2,3 Loella Minotti, 2,3 Dominique Hoffmann, 4,5 Olivie Betand, 1 and Monica Baciu 6 1 INSERM U821 Bain Dynamics and Cognition, Lyon, Fance 2 Depatment of Neuology, Genoble Hospital, Genoble, Fance 3 INSERM JE2413, Genoble, Fance 4 Depatment of Neuosugey, Genoble Hospital, Genoble, Fance 5 INSERM 318, Genoble, Fance 6 CNRS UMR 5105, Laboatoie de Psychologie et Neuocognition, Univesité Piee Mendès-Fance, Genoble, Fance Abstact: Cognitive neuoscience elies on two sets of techniques to map the neual netwoks undelying cognition in humans: ecodings of eithe egional metabolic changes (fmri o PET) o fluctuations in the neual electomagnetic fields (EEG and MEG). Despite majo advances in the last few yeas, an explicit linkage between the two is still missing and the neuoimaging community faces two complementay but unelated sets of functional desciptions of the human bain. Such an explicit famewok, linking the two appoaches in potentially complex cognitive tasks and in a vaiety of bain egions would pemit to combine them into fine spatio-tempoally-gained human bain mapping pocedues. We combined fmri and inta-canial EEG ecodings of the same epileptic patients duing a semantic decision task and found a close spatial coespondence between egions of fmri activations and ecoding sites showing EEG enegy modulations in the gamma ange (>40 Hz). Ou findings futhe suppot pevious findings that gamma band modulations co-localize with BOLD vaiations and also indicate that fmri may be used as a constaint to impove souce econstuction of gamma band EEG esponses. Hum Bain Mapp 28: , VC 2007 Wiley-Liss, Inc. Key wods: fmri; EEG; gamma band; eading This aticle contains supplementay mateial available via the Intenet at suppmat *Coespondence to: Jean-Philippe Lachaux, Mental Pocesses and Bain Activation, INSERM Unité 280, Cente Hospitalie Le Vinatie, Bãtiment 452, 95 Boulevad Pinel, Bon 69500, Fance. lachaux@lyon.insem.f Received fo publication 13 July 2006; Revision 31 Octobe 2006; Accepted 1 Novembe 2006 DOI: /hbm Published online 1 Febuay 2007 in Wiley InteScience (www. intescience.wiley.com). INTRODUCTION fmri high spatial but poo tempoal esolution and EEG poo spatial but high tempoal esolution ae in pinciple complementay by natue. Though fusing the two techniques is highly desiable, it is no tivial task. The activity of a small neual population duing a time window of the ode of seconds is measued by fmri as a couple of haemodynamic values and by EEG as a composite signal with a complex oganization in time and fequency. Indeed, the electophysiological esponse evoked by a sensoy stimulation, o a moto output always takes VC 2007 Wiley-Liss, Inc.
2 fmri vs. EEG Task-Related Modulations the fom of an oganised collection of event-elated potentials as well as synchonizations and desynchonizations in seveal fequency bands including theta (4 7 Hz), alpha (8 12 Hz), beta (15 30 Hz) and gamma anges (>40 Hz). In fact, a numbe of studies have demonstated that components of EEG esponses often have diffeent spatial and tempoal oganisation, as well as pesenting diffeent eactivity to modulations in a subject s cognitive activity [Cone et al., 1998a,b; Fouche et al., 2003; Lachaux et al., 2005], stongly suggesting that they eflect diffeent neual mechanisms and functions. It emains still unclea which (o which combinations) of these components has the stongest influence on the BOLD signal and this seiously limits the functional intepetation of fmri signals. Most of ou cuent knowledge about the electophysiological coelates of the BOLD signal come fom ecent animals studies combining simultaneous haemodynamic and spikes/local field potentials measuements [Kayse et al., 2004; Kim et al., 2004; Logothetis et al., 2001; Niessing et al., 2005]. Those studies have all shown a close coespondence between the BOLD signal and the gamma band component of the LFP, in both monkey and cat visual cotex. This constitutes a good eason to pay specially close attention to the gamma band; othes include (a) the putative ole of gamma band synchonization in neual communication [Fies, 2005; Vaela et al., 2001], stongly suppoted by numeous micoelectodes animal studies [Singe, 1999]; (b) the epeated obsevation, in human intacanial EEG studies, that seveal peceptual, moto and cognitive pocesses ae accompanied by focal enegy inceases in the gamma band, matching quite pecisely in thei anatomical oganisation the netwoks implicated in the same pocesses by fmri studies (e.g., moto pogamming [Aoki et al., 2001; Cone et al., 1998a; Lachaux et al., 2006; Szuhaj et al., 2005], memoy [Fell et al., 2001; Howad et al., 2003; Mainy et al., in pess] o visual peception [Klopp et al., 1999; Lachaux et al., 2000, 2005; Tallon-Baudy et al., 2001, 2005; Tanji et al., 2005]). Using the same expeimental attentional paadigm in intacanial EEG patients and in nomal subjects investigated by fmri evidence a significant spatial conguence in the netwoks of activations evealed by the two techniques [Bovelli et al., 2005]. On the othe hand, the same peceptual and moto pocesses have fequently been associated with enegy suppessions o desynchonization in the alpha and beta bands [Pfutschelle, 2001] though the anatomical localization of these enegy modulations did not match so neatly ou knowledge of cotical functional anatomy (such as the spatial mapping of the moto cotex homunculus [Cone et al., 1998b]). Taken togethe, these obsevations stongly suggest that a close anatomical coespondence may indeed exist between activation netwoks evealed by fmri and EEG gamma band esponses. A ecent study even postulated a fomal mechanism elating the phenomena measued by the two techniques [Niessing et al., 2005]: local gamma band enegy modulations would equie the synchonizing action of inhibitoy inteneuons, whose activity would substantially contibute to local oxygen consumption. Ideally, the putative elationship between BOLD and gamma band signals should be futhe tested, not only in animals, but also in humans. So fa, animal studies have only addessed this elationship fo extemely simple cognitive pocesses (unde anesthesia in most designs,), exclusively in the visual cotex. Yet gamma band activations ae exquisitely vaiable acoss individuals, bain egions, expeimental paadigms and vigilance levels [Engel et al., 1999; Fell et al., 2003; Fies et al., 2001]. Theefoe and given that the pimay use of fmri is the investigation of human cognition, the putative elationship between fmri and gamma band EEG activity should also be tested fo human subjects unde multiple cognitive situations with combined fmri and EEG ecodings sampling distibuted bain egions. Intaceebal EEG ecodings fom patients with intactable epilepsy offe a unique vista to ecod electophysiological activity in esticted human bain egions with a spatial pecision equivalent to that of fmri. While at pesent, intacanial ecodings cannot be made simultaneously with fmri, fo safety, ethical and legal easons, it is nonetheless possible to ecod the same patients with both techniques and in the same cognitive paadigms in a couple of days. To ou knowledge, this constitutes the most pomising possibility to date fo compaing EEG and fmri signals in humans. Thanks to the collaboation of thee epileptic patients, we wee able to implement pecisely such an expeimental design, in a eading task paadigm. Fo the fist study of this kind, we focused on the simple question of whethe BOLD vaiations and EEG gamma band enegy modulations induced by this eading task pesented compatible anatomical distibutions. An explicit elationship between the two would imply that EEG ecoding sites with stong gamma band enegy inceases evidenced in a contast between two expeimental conditions, should spatially coelate with fmri activation clustes obseved in the same contast. We tested pecisely this pediction in a contast between semantic pocessing vesus the visual analysis of stings of chaactes. MATERIALS AND METHODS Subjects All thee patients (P1, a 17-yea-old male, P2, an 18- yea-old female; P3, a 20-yea-old female;) suffeed fom dug-esistant patial epilepsy and wee candidates fo sugey. Because the location of the epileptic foci could not be identified by noninvasive methods, intaceebal ecodings wee made by means of steeotactically implanted multilead depth electodes (steeotactic EEG, SEEG). The selection of implant sites was based on puely clinical consideations with no efeence to the pesent expeimental potocol. Witten infomed consent was obtained fom all 1369
3 Lachaux et al. patients. All thee patients wee ight-handed (Edimbugh scale) native Fench speakes. Expeimental EEG sessions wee conducted 4 days afte implantation. MRI scans evidenced left hippocampal scleosis in P2 and P1, and left tempoal anteo-lateal ganglioglioma in P3. The epileptogenic zone poved to be tempoal anteo-mesial in P2, and tempoal mesio-lateal in P3 and P1. Electodes Implantation In all thee patients, 13 (P1), 15 (P2) and 12 (P3) semiigid electodes wee implanted in the left hemisphee, dominant fo language (see Supplementay Fig. S5), in diffeent cotical aeas based on the suspected locations of seizue oigin. Each electode had a diamete of 0.8 mm and compised mm long leads, 1.5 mm apat [Dixi, Besançon, Fance], depending on the taget egion (see Supplementay Fig. S5). Thus, vaious mesial and lateal tempoal and juxta-tempoal cotical aeas wee ecoded, including sulcal cotex and insula. The electode contacts wee identified on each individual steeotaxic scheme, and then anatomically localized using the steeotaxic atlas of Talaiach and Tounoux [Talaiach and Tounoux, 1988]. In addition, compute-assisted matching of post-implantation CT-scan with a pe-implantation 3-D MRI (VOXIM R, IVS Solutions, Gemany) povided a diect visualization of electode contacts with espect to each patient s bain anatomy: SEEG ecoding sites wee positioned onto the anatomical MRI which was modified to include makes in each SEEG site and then co-egisteed to the functional volumes of the patient, to associate each SEEG site with a specific fmri voxel. MR Acquisition Functional MR imaging was pefomed on a 1.5 Tesla MR image (Philips NT) equipped with echo-plana (EPI) acquisition. Twenty-five adjacent, axial slices (thickness 5 mm each) wee imaged sequentially. Fo each subject, only one functional scan was acquied duing each fmri session. The imaging volume was oiented paallel to the bicommissual plane. Positioning of the image planes was pefomed on scout images acquied in the sagital plane. An EPI MR pulse sequence was used. The main MR acquisition paametes of this sequence wee: TR ¼ 2770 ms, TE ¼ 45 ms, flip angle ¼ 908, acquisition time pe slice ¼ 37 ms, field-of-view ¼ mm 2, imaging matix ¼ 64 64, econstuction matix ¼ , total scan duation ¼ 14 min and 46 s. Subsequent to the functional scan, a high esolution 3D anatomical MR scan was obtained fom the volume examined duing functional scans acquisition. The fmri sessions wee conducted befoe the SEEG sessions in one patient (P3), and afte the SEEG sessions in the othe two (P1 and P2). Task and Stimuli The electodes position in pei-sylvian cotex of the dominant hemisphee motivated the choice of a language task. The paadigm was intended to involve high-level cognitive pocesses unique to humans and well-documented with fmri. The patients wee ecoded in thee diffeent conditions: two othogaphic and visual tasks (VISUAL) and (SYMBOL) and one semantic task (SEMANTIC). In the VIS- UAL condition, subjects wee shown a seies of five- o sixlette consonant stings inconguent with Fench language gaphotactic ules (i.e. xwxqn ) and thei task was to identify whethe the sting contained twice the same chaacte. In the SYMBOL condition, the conditions and the task wee identical except that the lettes wee eplaced by uneadable symbols, unknown to the subjects white Kaalyn Pattesen false font chaactes (examples of which can be seen in (Pice, 2000)). As data analysis evealed no diffeences between the VISUAL and SYMBOL conditions, both wee fused into the CONTROL task. In the SEMANTIC task, subjects wee asked to judge whethe five o six lettes wods epesented living entities o not. A block design was used which altenated nine peiods, each one composed of thee epochs (VISUAL, SYM- BOL and SEMAN epochs), the ode of which was vaied pseudo-andomly between blocks. Each epoch lasted 1 min and compised of 20 stimuli. All stimuli wee pesented foveally on a 17@ compute sceen, as black lowe-case lettes on a white backgound (couie font, size 35 mm). Between stimuli, a black cosshai (size 35 mm) was pesented in the cente of the sceen. Stimuli wee pesented fo duations of 2 s each with a andom intestimuli intevals anging between 2,800 and 3,200 ms. The patients wee instucted to espond by pessing a manual key with the index finge of thei left hand. Stimuli wee geneated by means of Psyscope V.1.1 (Canegie Mellon Depatment of Psychology) unning on a Macintosh compute (Powe Macintosh 9600). They wee shown to subjects inside the magnet by means of a video pojecto (Eiki LC 6000), a pojection sceen situated behind the magnet and a mio cented above the subject s eyes. EEG Data Analysis Intaceebal ecodings wee conducted using an audiovideo-eeg monitoing system (Micomed, Teviso, Italy), which allowed the simultaneous ecoding of 63 depth- EEG channels sampled at 512 Hz [ Hz bandwidth]. Recoding sites showing clea epileptifom activities wee excluded fom the analysis, and among the emaining sites, monopola and bipola data wee systematically inspected, both aw and high-pass filteed (above 15 Hz), and any tial showing epileptic spikes in any of those taces was discaded. Note that high-pass filteing was used only fo atifact detection, all the analyses wee pefomed on aw unfilteed data. 1370
4 fmri vs. EEG Task-Related Modulations Time-Fequency Analysis EEG signals wee evaluated with the softwae package fo electophysiological analysis (ELAN-Pack) developed at the INSERM U280 laboatoy. Fo each single tial, bipola deivations computed between adjacent electode contacts wee analyzed in the time-fequency domain by convolution with complex Gaussian Molet s wavelets, thus poviding a time-fequency powe map Pðt; f Þ¼jwðt; f ÞsðtÞj 2 ; whee w(t,f) was fo each time t and fequency f a complex Molet s wavelet wðt; f Þ¼A expð t 2 =2s 2 t Þexpð2ipftÞ; with A ¼ðs pffiffiffi t p Þ 1=2 and s t ¼ 1=ð2ps f Þ and s f a function of the fequency f: s f ¼ f =7 (Tallon-Baudy et al., 1996). Nomalized time-fequency maps wee computed fo each bipola deivation, fo visualization pupose. This nomalization was done sepaately fo each fequency, and consisted in (a) subtacting the mean powe duing a [ 500 ms: 100 ms] pestimulus baseline and (b) dividing by the standad deviation of the powe duing this same baseline. Compaison between conditions (SEMANTIC vs. CON- TROL) wee done via a Mann-Whitney non-paametic analysis applied on the aw time-fequency values of enegy, on a set of time-fequency tiles [80 ms 8 Hz] coveing a [ 500:2500 ms] [1:200 Hz] domain with an ovelap of 50% along both time and fequency axis (one test pe tile compaing the values obtained fo all the tials in the two conditions). The esults of this analysis ae time-fequency maps indicating TF domains in which EEG enegy is significantly diffeent between the two conditions; those maps wee used to diectly estimate the duation of those effects in the gamma band. fmri Data Analysis The functional data wee pe-pocessed with SPM2 softwae ( implemented in Matlab (The Mathwoks, Inc.). The analysis was pefomed independently on each patient. fmri data wee fist (a) ealigned to a scan ecoded halfway within the time seies fo motion coection and (b) spatially smoothed in the x,y diection (Gaussian kenel, 6 mm half-width). The fist two scans within a block wee discaded to avoid modelling of the haemodynamic esponse and the global activity in each scan was coected by gand mean scaling. Functional data analysis used a Geneal Linea Model using the conditions as factos of inteest and the uns as confounds to compute paamete estimates. Since the two conditions consonant stings and Kaalyn Pattesen wee pooled togethe into a single contol condition, the esult was finally expessed by the contast (named semantic-contol ) 2*"wod -( consonant stings þ Kaalyn Pattesen ) and by the P value coesponding to the compaison of this contast to zeo at each voxel. Those P values ae indicated in the figues fo each patient. RESULTS AND DISCUSSION As announced in the intoduction, ou objective was to detemine whethe fmri, taken in isolation, has any pedictive value about the anatomical location of coss-condition gamma band modulations. Following ou stating hypothesis that gamma band enegy modulations impose local haemodynamic signals vaiations, a logical pediction was that in the SEMANTIC CONTROL contast, at least one BOLD activation cluste should be found in the immediate vicinity of each EEG ecoding site showing diffeences in gamma band enegy in the same contast. Testing this pediction implied fist, identifying EEG sites with a significant coss-conditions diffeence in gamma band enegy, and second, estimating the distance between such sites and the closest BOLD activation cluste (anatomical locations of which can be found in Supplementay Tables I, II and III). TABLE I. Pecise anatomical location of the sites with a significant diffeence in gamma band enegy between the two expeimental conditions a Patient Site x y z Location P1 U Supeio tempoal gyus, posteio pat (BA42) P1 U Supeio tempoal gyus, posteio pat (BA42) P1 U Supeio tempoal gyus, posteio pat (BA42) P1 U Supeio tempoal gyus, posteio pat (BA42) P1 Y Infeio fontal gyus, ostal pat (BA46) P2 S Post-cental opeculum (BA43) P2 Q Infeio fontal gyus, caudal pat (BA44) P2 G Infeio fontal gyus, ostal pat (BA45/46) P3 U Supeio tempoal gyus, posteio pat (BA22) P3 U Supeio tempoal gyus, posteio pat (BA22) P3 U Supeio tempoal gyus, posteio pat (BA22) P3 U Supeio tempoal gyus, posteio pat (BA22) P3 T Supeio tempoal gyus, posteio pat (BA22) P3 F Lingual gyus (BA37/19) P3 V Supa-maginalis gyus (BA39/40) a Selected using the citeion defined in Figue 1; x, y, and z ae the Talaiach coodinates of the sites in millimetes. 1371
5 Lachaux et al. EEG time-fequency analysis evealed stong statistical diffeences between semantic and contol conditions in fequencies above 40 Hz, i.e. in the gamma band. Yet, those diffeences acoss conditions occued only in a small subset of the ecoding sites (15 out of 89). In those 15 sites, heeafte efeed to as gamma sites (see Table I), the modulations wee chaacteized by thei wide fequency extent (typically up to 150 Hz) and thei duation: the statistical diffeence lasting at least 100 ms in the [ Hz] band (see Fig. 1a). Figue 2 and Supplementay Figues S1 and S3 show fo each patient time-fequency maps fo gamma sites in both CONTROL and SEMANTIC conditions, in elation to thei fmri activation maps in the SEMANTIC CONTROL contast. Next, we measued the distance sepaating each of those gamma sites fom its neaest fmri activation cluste (activation clustes being defined as sets of contiguous voxels above the significance theshold in the SEMAN- TIC CONTROL contast, see methods). This analysis evealed that 12 out of the 15 (80%) gamma sites wee located <15 mm away fom an fmri activation cluste, which coesponds to an anatomical sepaation of a voxel o less (Fig. 1b). In compaison, 35 out of the 74 (47%) non-gamma sites wee <15 mm away fom an fmri activation cluste. To test statistically the hypothesis that the 12 close gamma sites wee close to fmri activation clustes than the othe 77 sites (the thee emaining and distant gamma sites eceive ou special attention in the next paagaph), we designed a simple andomization test consisting in (a) foming fo each patient a taget goup with the subset of the 12 gamma sites coesponding to thei implantation and 1,000 suogate goups of simila size andomly dawn fom all the ecoded sites within each goup, and (b) calculating the aveage distance sepaating a site fom its neaest BOLD cluste. This pocedue showed that fo all thee patients, this aveage distance was significantly smalle fo the taget goup than fo the suogate goups (P1: smalle than 0.002% of the suogate goups (P ¼ ). P2: P ¼ ;P3:P ¼ ). A close investigation of the thee distant gamma sites evealed that although they displayed an initial, and tansient, supeioity effect fo the SEMANTIC condition, they wee also chaacteized by a late invesion of this effect, with a stonge gamma enegy fo the CONTROL condition afte ms (see Figs. 2 and 3; Supplementay Figs. S1 and S2 fo statistical maps). Such effects evesals caused the total gamma enegy duing the whole esponse window to be equivalent in the two conditions o even slightly highe fo the CONTROL condition. This may explain why they did not coespond to any activation in the fmri SEMANTIC CONTROL, given the fact that fmri slices wee acquied evey 3 s. We wish to highlight those thee examples as they illustate potentially meaningful diffeences in neual activations which can only be evealed by time-esolved neual ecodings. Figue 1. Spatial elationship between BOLD and SEEG gamma modulations. (a) Maximal duation of significant enegy diffeence between the SEMANTIC and the CONTROL conditions in the [ Hz] band, fo all the EEG sites. Fo each site, this value coesponds to the duation of the longest time window, acoss all fequencies in the gamma band, duing which the P-value fo the Mann-Whitney compaison between the two conditions stays lowe than Sites fo which this duation exceeds 100 ms ae efeed to as gamma sites in the text. The makes shapes indicate which patient was ecoded; (b) same fo the 15 sites fo which the maximal duation is longe than 100 ms. Sites close than 10 mm (esp. 15 mm) away fom a fmri activation cluste (i.e. sets of contiguous voxels above the significance theshold) in the SEMANTIC CONTROL ae shown in geen (esp. blue), the emaining sites ae shown in ed. [Colo figue can be viewed in the online issue, which is available at In addition to the SEMANTIC CONTROL contast, we also tested whethe the evese CONTROL SEMANTIC contast would eveal bain egions with stonge BOLD signal in the contol condition and how those egions would espond in the gamma band (Fig. S6). Thee wee 1372
6 fmri vs. EEG Task-Related Modulations indeed such effects in all thee patients, pedominantly in the visual cotex, which was expected since the contol task equied detailed visual inspection of the chaacte stings. Except in patient P3, thee wee no EEG ecoding sites in the vicinity of those negative BOLD esponses (<15 mm). In patient P3, thee ecoding sites wee located <15 mm fom negative BOLD clustes (see Fig. S6), howeve, no significant diffeences wee found between conditions. The pevious examples do not dispove the suspected elationship between BOLD signals and gamma band activations: altogethe, ou analysis showed that sites with a gamma enegy incease globally stonge in the SEMAN- TIC CONTROL contast wee significantly close than the othe sites to fmri activation clustes evealed in the same contast. This implies that fmri could be used, in this paticula expeimental situation, as a spatial pedicto of such gamma modulations; that is, fmri could indicate cotical egions whee sites with a stonge gamma band esponse in the semantic condition would be moe likely to be found. Howeve, this pedictive powe should not be undestood in the stong sense that any SEEG site in the vicinity of a fmri cluste should ecod task-elated gamma modulations. While significant gamma band modulations wee obseved in the vicinity of fmri activation clustes, the convese was in geneal not tue. This was expected because depth electodes sample only esticted potions of the volumes suounding the fmri activation clustes: Figue 2. Semantic Contol contasts in fmri and SEEG (patient P1). The top panel shows the fmri images of statistically significant inceases in BOLD signal fom the CONTROL to the SEMAN- TIC condition (ed voxels), thesholded at P < 0.001, supeimposed on tansvese sections of P1 s bain. Yellow dots indicate the bain sites ecoded in SEEG, while blue lines point at sites U 9 and Y 14 whee task-elated EEG modulations longe than 100 ms wee obseved in the [ Hz] band. The bottom panels show fo each of those sites the time-fequency maps in the two conditions (left and middle maps, each time-couse is expessed in units of the standad deviation of the [ 500: 100 ms] pestimulus peiod). Time-fequency maps on the ight show the P-values of a Mann-Whitney compaison between the SEMANTIC and CONTROL conditions. Regions whee the SEMANTIC (esp. CONTROL) condition dominates ae indicated by a blue plus (esp. minus) sign. U 9, shows a clea supeioity effect of the SEMANTIC condition and is adjacent to a fmri activation cluste, in the posteio pat of the supeio tempoal gyus. Y 14, in the infeio fontal gyus, is >15 mm away fom the neaest BOLD cluste, but the effect thee is ambiguous: the gamma enegy is initially stonge fo the semantic condition, befoe the effect eveses afte 500 ms. See the supplementay mateials fo a simila figue fo the othe two patients. [Colo figue can be viewed in the online issue, which is available at
7 Lachaux et al. gamma modulations wee vey focal (see Fig. S4, supplementay mateials), and it follows that the pesence of an fmri activation cluste in a bain egion may imply a local incease of gamma enegy somewhee in its suounding, without necessay involving the ignition of the entie suoundings. Indeed, Figue S4 illustates the case of two ecoding sites sepaated by only 3.5 mm along the same electode. Although the two sites wee equally close to the neaest fmri activation cluste, they displayed shaply diffeent gamma modulations. In summay, ou esults suppot the view that the functional netwoks evealed by fmri ae spatially conguent with the mosaic of gamma activations evealed in humans by intacanial EEG ecodings. Obviously, a single study is not sufficient to pove a systematic elationship between the two phenomena, especially given the small numbe of patients investigated hee, but this one cooboates, in maybe the most diect expeimental context in humans given pesent safety constaints, the link aleady demonstated in animal models, with thei associated stengths and limitations. A definitive poof will now equie a multiplicity of studies of this kind, combining fmri and intacanial EEG in the same patients, acoss a wide ange of bain exploations and cognitive situations, in conjunction with futhe animal studies. The two imaging appoaches, SEEG and fmri, appea in fact vey complementay, neithe of them being sufficient by itself: intacanial EEG ecodings suffe fom thei limited sampling of the bain volume, while fmri is ill-suited to distinguishing between activations with simila global enegy but diffeent time couses. Altogethe, this study encouages futhe eseach effots to combine fmri, eithe with intaceebal EEG, o scalp EEG (and MEG) though souce-econstuction algoithms. ACKNOWLEDGMENTS The authos thank Valéie Balle, Paticia Boschetti, Caole Chatelad, Véonique Dolin, Eliane Gamblin, and Matine Juillad fo thei invaluable technical help; and Benjamin Schoendoff and Kaim Jebi fo thei pecious comments on the manuscipt. J.-P.L. was suppoted by a gant fom the Fyssen Fundation. Figue 3. Biphasic enegy modulations in the gamma band. Each gaph shows the mean enegy pofile in the [ Hz] fequency band fo the CONTROL (gay) and SEMANTIC (black) conditions. (a,b,c) coespond to the only sites with a clea condition-effect in the gamma band which ae fa (>15 mm) fom a BOLD contast cluste. In all thee cases, the initial bust of gamma enegy is stonge in the SEMANTIC condition, while its tail is stonge in the CONTROL condition. Such effects, which may be fequent in functional imaging studies, ae poblematic fo fmri. (d) shows an unambiguous semantic supeioity effect fo compaison. 1374
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