Fast presurgical functional mapping using task-related intracranial high gamma activity

Laboratory investigation

Restricted access


Electrocorticography (ECoG) is a powerful tool for presurgical functional mapping. Power increase in the high gamma band has been observed from ECoG electrodes on the surface of the sensory motor cortex during the execution of body movements. In this study the authors aim to validate the clinical usage of high gamma activity in presurgical mapping by comparing ECoG mapping with traditional direct electrical cortical stimulation (ECS) and functional MRI (fMRI) mapping.


Seventeen patients with epilepsy participated in an ECoG motor mapping experiment. The patients executed a 5-minute hand/tongue movement task while the ECoG signal was recorded. All 17 patients also underwent extraoperative ECS mapping to localize the motor cortex. Eight patients also participated in a presurgical fMRI study. The high gamma activity on ECoG was modeled using the general linear model (GLM), and the regions showing significant gamma power increase during the task condition compared with the rest condition were localized. The maps derived from GLM-based ECoG mapping, ECS, and fMRI were then compared.


High gamma activity in the motor cortex can be reliably modulated by motor tasks. Localization of the motor regions achieved with GLM-based ECoG mapping was consistent with the localization determined by ECS. The maps also appeared to be highly localized compared with the fMRI activations. Using the ECS findings as the reference, GLM-based ECoG mapping showed a significantly higher sensitivity than fMRI (66.7% for ECoG, 52.6% for fMRI, p < 0.05), while the specificity was high for both techniques (> 97%). If the current-spreading effect in ECS is accounted for, ECoG mapping may produce maps almost identical to those produced by ECS mapping (100% sensitivity and 99.5% specificity).


General linear model–based ECoG mapping showed a superior performance compared to traditional ECS and fMRI mapping in terms of efficiency and accuracy. Using this method, motor functions can be reliably mapped in less than 5 minutes.

Abbreviations used in this paper:BOLD = blood oxygen level dependent; ECoG = electrocorticography; ECS = electrical cortical stimulation; fMRI = functional MRI; GLM = general linear model; TTL = transistor-transistor logic.

Article Information

Address correspondence to: Bo Hong, Ph.D., Department of Biomedical Engineering, School of Medicine, Tsinghua University, Medical School Building B204, Qinghua Yuan 1, Beijing 100084, China. email:

Please include this information when citing this paper: published online April 19, 2013; DOI: 10.3171/2013.2.JNS12843.

© AANS, except where prohibited by US copyright law.



  • View in gallery

    Left: Schematic diagram of the experimental setup. Surgical patients with implanted subdural electrodes performed hand or tongue movement tasks in 20-second blocks interleaved with 8-second rest blocks. The type of movement (hand or tongue) was indicated by a visual cue displayed on the screen throughout the block. In each task block, the patient grasped the hand contralateral to the side of electrode implantation, or stuck out his tongue immediately following an auditory cue (duration 0.2 seconds, average interstimulus interval 4 seconds). Each block involved only one type of movement. Right: The GLM design matrix. The upper 2 plots show the contrast vectors of the hand and tongue movement tasks. The lower graph depicts the design matrix, with each row corresponding to one sample point of the ECoG. The full design matrix contains 4 columns. The first 2 columns represent the hand and tongue movement; the third column represents the rest condition, and the fourth is the constant. The 2 task columns were obtained by replacing the first 3 seconds of each trial with a high gamma response template. s = seconds.

  • View in gallery

    Left: The relative power (task/rest) of the ECoG signal recorded from the representative electrode during movement (from 0.3 to 1.3 seconds after the auditory cue onset). The representative electrode was chosen if the patient showed or reported symptoms related to the sensory motor cortex when stimulated with the minimum current intensity during the ECS test. The blue curve represents the relative power spectra averaged across all 17 patients. The movement task induced a significant power increase in the high gamma band but a decrease in the alpha (8–13 Hz) and beta (15–30 Hz) bands. The power in the low gamma band did not show any significant change. Right: The time-frequency plane was divided into small time-frequency bins (each bin is 15 msec × 1 Hz). The power spectra in the time-frequency bins showing significant task versus rest difference were averaged across all subjects. The modulation effect of the movement tasks was clearly demonstrated in the high gamma band and some of the low-frequency bands.

  • View in gallery

    Hand and tongue motor areas localized by ECS, ECoG, and fMRI. The mapping results were projected to each individual's brain surface reconstructed from the T1-weighted MR images. Each row represents the results obtained in 1 patient. The number on the left is the case number as shown in Table 1. The left 3 columns illustrate the hand motor regions mapped by ECS, ECoG, and fMRI, respectively. The right 3 columns are the maps of the tongue motor regions. The blue dots in the ECS maps indicate negative electrodes (no symptoms related to sensory motor cortex reported when stimulated) and the yellow dots indicate positive electrodes. The ECoG results were the t-values of all electrodes determined by the GLM rendered on the cortical surface. The fMRI activation maps were also the t-values determined by the GLM. The ECoG maps were highly consistent with the ECS findings and were more localized than fMRI results.

  • View in gallery

    Overall sensitivity and specificity of ECoG and fMRI mapping. To determine the sensitivity and specificity, ECS results were used as the reference. The sensitivity and specificity in each patient are listed in Table 2. The overall percentage is computed as the total number of electrodes belonging to A, B, C, or D conditions (defined in Table 2) over all tasks and patients (17 patients for ECoG, 8 patients for fMRI). Compared with fMRI, ECoG mapping results are significantly more consistent with the ECS findings. *p < 0.05, paired t-test.

  • View in gallery

    A: A high gamma response template was obtained by averaging the single-trial gamma-band activity. The blue curves are the fitted gamma functions of single trials recorded from the representative electrodes. The black curve is the high gamma response template derived from averaging the blue curves. B: The gamma band was separated into multiple subbands, and the mean power in these subbands was averaged across all trials/tasks/subjects. For each trial, the mean power during the time window of 0–2 seconds was calculated. Compared with other subbands, the 60- to 90-Hz band has the highest power during movement tasks. C: The broadband (30-Hz bin) high gamma envelope has a greater signal-to-noise ratio than the narrow band (10-Hz bin). The broadband high gamma activity, especially between 60 and 90 Hz, has a greater t-statistic value than the other subbands within the same ECoG data set. D: Using the gamma template, fewer trials are needed to achieve the same performance than when the square template or the peak template are used. On average, the gamma template needs 20 trials, the square template needs 50 trials, and the peak template needs 29 trials for the same performance. SNR = signal-to-noise ratio. Patient ID = case number (Table 1).



Biswal BYetkin FZHaughton VMHyde JS: Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34:5375411995


Bittar RGOlivier ASadikot AFAndermann FPike GBReutens DC: Presurgical motor and somatosensory cortex mapping with functional magnetic resonance imaging and positron emission tomography. J Neurosurg 91:9159211999


Blume WTJones DCPathak P: Properties of after-discharges from cortical electrical stimulation in focal epilepsies. Clin Neurophysiol 115:9829892004


Brainard DH: The psychophysics toolbox. Spat Vis 10:4334361997


Brown ECRothermel RNishida MJuhász CMuzik OHoechstetter K: In vivo animation of auditory-language-induced gamma-oscillations in children with intractable focal epilepsy. Neuroimage 41:112011312008


Brunner PRitaccio ALLynch TMEmrich JFWilson JAWilliams JC: A practical procedure for real-time functional mapping of eloquent cortex using electrocorticographic signals in humans. Epilepsy Behav 15:2782862009


Canolty RTEdwards EDalal SSSoltani MNagarajan SSKirsch HE: High gamma power is phase-locked to theta oscillations in human neocortex. Science 313:162616282006


Cordes DHaughton VMArfanakis KWendt GJTurski PAMoritz CH: Mapping functionally related regions of brain with functional connectivity MR imaging. AJNR Am J Neuroradiol 21:163616442000


Crone NEHao L: The functional significance of event-related spectral changes (ERD/ERS) from the perspective of electrocorticography. Clin Neurophysiol (Suppl) 54:4354422002


Crone NEHao LHart J JrBoatman DLesser RPIrizarry R: Electrocorticographic gamma activity during word production in spoken and sign language. Neurology 57:204520532001


Crone NEMiglioretti DLGordon BLesser RP: Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. II. Event-related synchronization in the gamma band. Brain 121:230123151998


Crone NEMiglioretti DLGordon BSieracki JMWilson MTUematsu S: Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. I. Alpha and beta event-related desynchronization. Brain 121:227122991998


Edwards ENagarajan SSDalal SSCanolty RTKirsch HEBarbaro NM: Spatiotemporal imaging of cortical activation during verb generation and picture naming. Neuroimage 50:2913012010


Fandino JKollias SSWieser HGValavanis AYonekawa Y: Intraoperative validation of functional magnetic resonance imaging and cortical reorganization patterns in patients with brain tumors involving the primary motor cortex. J Neurosurg 91:2382501999


Fernández Gde Greiff Avon Oertzen JReuber MLun SKlaver P: Language mapping in less than 15 minutes: real-time functional MRI during routine clinical investigation. Neuroimage 14:5855942001


Fischl BSalat DHBusa EAlbert MDieterich MHaselgrove C: Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33:3413552002


Friston KJFrith CDTurner RFrackowiak RS: Characterizing evoked hemodynamics with fMRI. Neuroimage 2:1571651995


Friston KJHolmes APPoline JBGrasby PJWilliams SCFrackowiak RSJ: Analysis of fMRI time-series revisited. Neuroimage 2:45531995


Friston KJHolmes APWorsley KJPoline JPFrith CDFrackowiak RSJ: Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp 2:1892101995


Galaburda AMRosen GDSherman GF: Individual variability in cortical organization: its relationship to brain laterality and implications to function. Neuropsychologia 28:5295461990


Gaona CMSharma MFreudenburg ZVBreshears JDBundy DTRoland J: Nonuniform high-gamma (60–500 Hz) power changes dissociate cognitive task and anatomy in human cortex. J Neurosci 31:209121002011


Gross JSchnitzler ATimmermann LPloner M: Gamma oscillations in human primary somatosensory cortex reflect pain perception. PLoS Biol 5:e1332007


Haglund MMBerger MSShamseldin MLettich EOjemann GA: Cortical localization of temporal lobe language sites in patients with gliomas. Neurosurgery 34:5675761994


Hauck MLorenz JEngel AK: Attention to painful stimulation enhances gamma-band activity and synchronization in human sensorimotor cortex. J Neurosci 27:927092772007


Hirsch JRuge MIKim KHCorrea DDVictor JDRelkin NR: An integrated functional magnetic resonance imaging procedure for preoperative mapping of cortical areas associated with tactile, motor, language, and visual functions. Neurosurgery 47:7117222000


Holodny AISchulder MLiu WCWolko JMaldjian JAKalnin AJ: The effect of brain tumors on BOLD functional MR imaging activation in the adjacent motor cortex: implications for image-guided neurosurgery. AJNR Am J Neuroradiol 21:141514222000


Hoogenboom NSchoffelen JMOostenveld RParkes LMFries P: Localizing human visual gamma-band activity in frequency, time and space. Neuroimage 29:7647732006


Ihara AHirata MYanagihara KNinomiya HImai KIshii R: Neuromagnetic gamma-band activity in the primary and secondary somatosensory areas. Neuroreport 14:2732772003


Jack CR JrThompson RMButts RKSharbrough FWKelly PJHanson DP: Sensory motor cortex: correlation of presurgical mapping with functional MR imaging and invasive cortical mapping. Radiology 190:85921994


Kirsch HESepkuty JPCrone NE: Multimodal functional mapping of sensorimotor cortex prior to resection of an epileptogenic perirolandic lesion. Epilepsy Behav 5:4074102004


Kleiner MBrainard DPelli D: What's new in Psychtoolbox-3?. Perception 36:Suppl142007. (Abstract)


Lachaux JPGeorge NTallon-Baudry CMartinerie JHugueville LMinotti L: The many faces of the gamma band response to complex visual stimuli. Neuroimage 25:4915012005


Lachaux JPJerbi KBertrand OMinotti LHoffmann DSchoendorff B: A blueprint for real-time functional mapping via human intracranial recordings. PLoS ONE 2:e10942007


Lesser RPLüders HKlem GDinner DSMorris HHHahn J: Cortical after-discharge and functional response thresholds: results of extraoperative testing. Epilepsia 25:6156211984


Lesser RPLüders HKlem GDinner DSMorris HH IIIHahn J: Ipsilateral trigeminal sensory responses to cortical stimulation by subdural electrodes. Neurology 35:176017631985


Leuthardt ECMiller KAnderson NRSchalk GDowling JMiller J: Electrocorticographic frequency alteration mapping: a clinical technique for mapping the motor cortex. Neurosurgery 60:4 Suppl 22602712007


Liu HBuckner RLTalukdar TTanaka NMadsen JRStufflebeam SM: Task-free presurgical mapping using functional magnetic resonance imaging intrinsic activity. Laboratory investigation. J Neurosurg 111:7467542009


Mainy NJung JBaciu MKahane PSchoendorff BMinotti L: Cortical dynamics of word recognition. Hum Brain Mapp 29:121512302008


McGonigle DJHowseman AMAthwal BSFriston KJFrackowiak RSHolmes AP: Variability in fMRI: an examination of intersession differences. Neuroimage 11:7087342000


Miller KJdenNijs MShenoy PMiller JWRao RPNOjemann JG: Real-time functional brain mapping using electrocorticography. Neuroimage 37:5045072007


Miller KJLeuthardt ECSchalk GRao RPNAnderson NRMoran DW: Spectral changes in cortical surface potentials during motor movement. J Neurosci 27:242424322007


Miyanari AKaneoke YIhara AWatanabe SOsaki YKubo T: Neuromagnetic changes of brain rhythm evoked by intravenous olfactory stimulation in humans. Brain Topogr 18:1891992006


Mueller WMYetkin FZHammeke TAMorris GL IIISwanson SJReichert K: Functional magnetic resonance imaging mapping of the motor cortex in patients with cerebral tumors. Neurosurgery 39:5155211996


Ojemann GOjemann JLettich EBerger M: Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. J Neurosurg 71:3163261989


Penfield W: The circulation of the epileptic brain. Res Publ Assoc Res Nerv Ment Dis 18:6056371937


Pfurtscheller GGraimann BHuggins JELevine SPSchuh LA: Spatiotemporal patterns of beta desynchronization and gamma synchronization in corticographic data during self-paced movement. Clin Neurophysiol 114:122612362003


Pieper SHalle MKikinis R: 3D Slicer. Proc IEEE Int Symp Biomed Imaging 1:6326352004


Ray SNiebur EHsiao SSSinai ACrone NE: High-frequency gamma activity (80–150Hz) is increased in human cortex during selective attention. Clin Neurophysiol 119:1161332008


Roland JBrunner PJohnston JSchalk GLeuthardt EC: Passive real-time identification of speech and motor cortex during an awake craniotomy. Epilepsy Behav 18:1231282010


Roux FEBoulanouar KRanjeva JPTremoulet MHenry PManelfe C: Usefulness of motor functional MRI correlated to cortical mapping in Rolandic low-grade astrocytomas. Acta Neurochir (Wien) 141:71791999


Sanai NMirzadeh ZBerger MS: Functional outcome after language mapping for glioma resection. N Engl J Med 358:18272008


Schalk GLeuthardt ECBrunner POjemann JGGerhardt LAWolpaw JR: Real-time detection of event-related brain activity. Neuroimage 43:2452492008


Siegel MDonner THOostenveld RFries PEngel AK: High-frequency activity in human visual cortex is modulated by visual motion strength. Cereb Cortex 17:7327412007


Sinai ABowers CWCrainiceanu CMBoatman DGordon BLesser RP: Electrocorticographic high gamma activity versus electrical cortical stimulation mapping of naming. Brain 128:155615702005


Steinmetz HFürst GFreund HJ: Variation of perisylvian and calcarine anatomic landmarks within stereotaxic proportional coordinates. AJNR Am J Neuroradiol 11:112311301990


Szelényi AJoksimovic BSeifert V: Intraoperative risk of seizures associated with transient direct cortical stimulation in patients with symptomatic epilepsy. J Clin Neurophysiol 24:39432007


Tallon-Baudry CBertrand OHénaff MAIsnard JFischer C: Attention modulates gamma-band oscillations differently in the human lateral occipital cortex and fusiform gyrus. Cereb Cortex 15:6546622005


Towle VLYoon HACastelle MEdgar JCBiassou NMFrim DM: ECoG gamma activity during a language task: differentiating expressive and receptive speech areas. Brain 131:201320272008


Wu MWisneski KSchalk GSharma MRoland JBreshears J: Electrocorticographic frequency alteration mapping for extraoperative localization of speech cortex. Neurosurgery 66:E407E4092010


Yetkin FZMueller WMMorris GLMcAuliffe TLUlmer JLCox RW: Functional MR activation correlated with intraoperative cortical mapping. AJNR Am J Neuroradiol 18:131113151997


Zanos SMiller KJOjemann JG: Electrocorticographic spectral changes associated with ipsilateral individual finger and whole hand movement. Conf Proc IEEE Eng Med Biol Soc 593959422008




All Time Past Year Past 30 Days
Abstract Views 42 42 17
Full Text Views 133 133 25
PDF Downloads 104 104 9
EPUB Downloads 0 0 0


Google Scholar