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Peter T. Lin, Mitchel S. Berger and Srikantan S. Nagarajan

Object

In this study the role of magnetic source imaging for preoperative motor mapping was evaluated by using a single-dipole localization method to analyze motor field data in 41 patients.

Methods

Data from affected and unaffected hemispheres were collected in patients performing voluntary finger flexion movements. Somatosensory evoked field (SSEF) data were also obtained using tactile stimulation. Dipole localization using motor field (MF) data was successful in only 49% of patients, whereas localization with movement-evoked field (MEF) data was successful in 66% of patients. When the spatial distribution of MF and MEF dipoles in relation to SSEF dipoles was analyzed, the motor dipoles were not spatially distinct from somatosensory dipoles.

Conclusions

The findings in this study suggest that single-dipole localization for the analysis of motor data is not sufficiently sensitive and is nonspecific, and thus not clinically useful.

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Ann-Christine Duhaime and Steven M. Stufflebeam

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Phiroz E. Tarapore, Matthew C. Tate, Anne M. Findlay, Susanne M. Honma, Danielle Mizuiri, Mitchel S. Berger and Srikantan S. Nagarajan

Object

Direct cortical stimulation (DCS) is the gold-standard technique for motor mapping during craniotomy. However, preoperative noninvasive motor mapping is becoming increasingly accurate. Two such noninvasive modalities are navigated transcranial magnetic stimulation (TMS) and magnetoencephalography (MEG) imaging. While MEG imaging has already been extensively validated as an accurate modality of noninvasive motor mapping, TMS is less well studied. In this study, the authors compared the accuracy of TMS to both DCS and MEG imaging.

Methods

Patients with tumors in proximity to primary motor cortex underwent preoperative TMS and MEG imaging for motor mapping. The patients subsequently underwent motor mapping via intraoperative DCS. The loci of maximal response were recorded from each modality and compared. Motor strength was assessed at 3 months postoperatively.

Results

Transcranial magnetic stimulation and MEG imaging were performed on 24 patients. Intraoperative DCS yielded 8 positive motor sites in 5 patients. The median distance ± SEM between TMS and DCS motor sites was 2.13 ± 0.29 mm, and between TMS and MEG imaging motor sites was 4.71 ± 1.08 mm. In no patients did DCS motor mapping reveal a motor site that was unrecognized by TMS. Three of 24 patients developed new, early neurological deficit in the form of upper-extremity paresis. At the 3-month follow-up evaluation, 2 of these patients were significantly improved, experiencing difficulty only with fine motor tasks; the remaining patient had improvement to 4/5 strength. There were no deaths over the course of the study.

Conclusions

Maps of the motor system generated with TMS correlate well with those generated by both MEG imaging and DCS. Negative TMS mapping also correlates with negative DCS mapping. Navigated TMS is an accurate modality for noninvasively generating preoperative motor maps.

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Jeffrey I. Berman, Mitchel S. Berger, Sungwon Chung, Srikantan S. Nagarajan and Roland G. Henry

Object

Resecting brain tumors involves the risk of damaging the descending motor pathway. Diffusion tensor (DT)–imaged fiber tracking is a noninvasive magnetic resonance (MR) technique that can delineate the subcortical course of the motor pathway. The goal of this study was to use intraoperative subcortical stimulation mapping of the motor tract and magnetic source imaging to validate the utility of DT-imaged fiber tracking as a tool for presurgical planning.

Methods

Diffusion tensor-imaged fiber tracks of the motor tract were generated preoperatively in nine patients with gliomas. A mask of the resultant fiber tracks was overlaid on high-resolution T1- and T2-weighted anatomical MR images and used for stereotactic surgical navigation. Magnetic source imaging was performed in seven of the patients to identify functional somatosensory cortices. During resection, subcortical stimulation mapping of the motor pathway was performed within the white matter using a bipolar electrode.

Results

A total of 16 subcortical motor stimulations were stereotactically identified in nine patients. The mean distance between the stimulation sites and the DT-imaged fiber tracks was 8.7 ±3.1 mm (±standard deviation). The measured distance between subcortical stimulation sites and DT-imaged fiber tracks combines tracking technique errors and all errors encountered with stereotactic navigation.

Conclusions

Fiber tracks delineated using DT imaging can be used to identify the motor tract in deep white matter and define a safety margin around the tract.

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Srikantan Nagarajan, Heidi Kirsch, Peter Lin, Anne Findlay, Susanne Honma and Mitchel S. Berger

Object

The goal of this study was to examine the sensitivity and specificity in preoperative localization of hand motor cortex by imaging regional event-related desynchronization (ERD) of brainwaves in the β frequency band (15–25 Hz) involved in self-paced movement.

Methods

Using magnetoencephalography (MEG), the authors measured ERD that occurred before self-paced unilateral index finger flexion in 66 patients with brain tumors, epilepsy, and arteriovenous malformations.

Results

The authors applied an adaptive spatial filtering algorithm to MEG data and found that peaks of the tomographic distribution of β-band ERD sources reliably localized hand motor cortex compared with electrical cortical stimulation. They also observed high specificity in estimating contralateral hand motor cortical representations relative to somatosensory cortex. Neither presence nor location of tumor changed the qualitative or quantitative location of motor cortex relative to somatosensory cortex.

Conclusions

An imaging protocol using ERD obtained by adaptive spatial filtering of MEG data can be used for extremely reliable preoperative localization of hand motor cortex.

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Edward F. Chang, Srikantan S. Nagarajan, Mary Mantle, Nicholas M. Barbaro and Heidi E. Kirsch

Object

Routine scalp electroencephalography (EEG) cannot always distinguish whether generalized epileptiform discharges are the result of primary bilateral synchrony or secondary bilateral synchrony (SBS) from a focal origin; this is an important distinction because the latter may be amenable to resection. Whole-head magnetoencephalography (MEG) has superior spatial resolution compared with traditional EEG, and can potentially elucidate seizure foci in challenging epilepsy cases in which patients are undergoing evaluation for surgery.

Methods

Sixteen patients with medically intractable epilepsy in whom SBS was suspected were referred for magnetic source (MS) imaging. All patients had bilateral, synchronous, widespread, and most often generalized spike-wave discharges on scalp EEG studies, plus some other clinical (for example, seizure semiology) or MR imaging feature (for example, focal lesion) suggesting focal onset and hence possible surgical candidacy. The MS imaging modality is the combination of whole-head MEG and parametric reconstruction of corresponding electrical brain sources. An MEG and simultaneous EEG studies were recorded with a 275-channel whole-head system. Single-equivalent current dipoles were estimated from the MEG data, and dipole locations and orientations were superimposed on patients' MR images.

Results

The MS imaging studies revealed focal dipole clusters in 12 (75%) of the 16 patients, of which a single dipole cluster was identified in 7 patients (44%). Patient age, seizure type, duration of disease, video-EEG telemetry, and MR imaging results were analyzed to determine factors predictive of having clusters revealed on MS imaging. Of these factors, only focal MR imaging anatomical abnormalities were associated with dipole clusters (chi-square test, p = 0.03). Selective resections (including the dipole cluster) in 7 (87%) of 8 patients resulted in seizure-free or rare seizure outcomes (Engel Classes I and II).

Conclusions

Magnetic source imaging may provide noninvasive anatomical and neurophysiological confirmation of localization in patients in whom there is a suspicion of SBS (based on clinical or MR imaging data), especially in those with an anatomical lesion. Identification of a focal seizure origin has significant implications for both resective and nonresective treatment of intractable epilepsy.

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Heidi E. Kirsch, Zhao Zhu, Susanne Honma, Anne Findlay, Mitchel S. Berger and Srikantan S. Nagarajan

Object

Before resective brain surgery, localization of the functional regions is necessary to minimize postoperative deficits. The face area has been relatively difficult to map noninvasively by using functional imaging techniques. Preoperative localization of face somatosensory cortex with magnetoencephalography (MEG) may allow the surgeon to predict the location of mouth motor areas.

Methods

The authors compared the location of face somatosensory cortex obtained with somatosensory evoked fields during preoperative MEG with the mouth motor areas identified during intraoperative electrocortical stimulation (ECS) mapping in 13 patients undergoing resection of brain tumor.

Results

In this group of patients, ECS mouth motor sites were usually anterior and lateral to MEG localizations of lip somatosensory cortex. The consistent quantitative relationship between results of these two mapping procedures allows the practitioner to predict the location of mouth motor cortex based on noninvasive preoperative MEG measurements.

Conclusions

Based on this result, the authors suggest that somatosensory mapping using MEG can be used to guide intraoperative mapping and neurosurgical planning.

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Phiroz E. Tarapore, Anne M. Findlay, Sara C. LaHue, Hana Lee, Susanne M. Honma, Danielle Mizuiri, Tracy L. Luks, Geoffrey T. Manley, Srikantan S. Nagarajan and Pratik Mukherjee

Object

Traumatic brain injury (TBI) is one of the leading causes of morbidity worldwide. One mechanism by which blunt head trauma may disrupt normal cognition and behavior is through alteration of functional connectivity between brain regions. In this pilot study, the authors applied a rapid automated resting state magnetoencephalography (MEG) imaging technique suitable for routine clinical use to test the hypothesis that there is decreased functional connectivity in patients with TBI compared with matched controls, even in cases of mild TBI. Furthermore, they posit that these abnormal reductions in MEG functional connectivity can be detected even in TBI patients without specific evidence of traumatic lesions on 3-T MR images. Finally, they hypothesize that the reductions of functional connectivity can improve over time across serial MEG scans during recovery from TBI.

Methods

Magnetoencephalography maps of functional connectivity in the alpha (8- to 12-Hz) band from 21 patients who sustained a TBI were compared with those from 18 age- and sex-matched controls. Regions of altered functional connectivity in each patient were detected in automated fashion through atlas-based registration to the control database. The extent of reduced functional connectivity in the patient group was tested for correlations with clinical characteristics of the injury as well as with findings on 3-T MRI. Finally, the authors compared initial connectivity maps with 2-year follow-up functional connectivity in a subgroup of 5 patients with TBI.

Results

Fourteen male and 7 female patients (17–53 years old, median 29 years) were enrolled. By Glasgow Coma Scale (GCS) criteria, 11 patients had mild, 1 had moderate, and 3 had severe TBI, and 6 had no GCS score recorded. On 3-T MRI, 16 patients had abnormal findings attributable to the trauma and 5 had findings in the normal range. As a group, the patients with TBI had significantly lower functional connectivity than controls (p < 0.01). Three of the 5 patients with normal findings on 3-T MRI showed regions of abnormally reduced MEG functional connectivity. No significant correlations were seen between extent of functional disconnection and injury severity or posttraumatic symptoms (p > 0.05). In the subgroup undergoing 2-year follow-up, the second MEG scan demonstrated a significantly lower percentage of voxels with decreased connectivity (p < 0.05) than the initial MEG scan.

Conclusions

A rapid automated resting-state MEG imaging technique demonstrates abnormally decreased functional connectivity that may persist for years after TBI, including cases classified as “mild” by GCS criteria. Disrupted MEG connectivity can be detected even in some patients with normal findings on 3-T MRI. Analysis of follow-up MEG scans in a subgroup of patients shows that, over time, the abnormally reduced connectivity can improve, suggesting neuroplasticity during the recovery from TBI. Resting state MEG deserves further investigation as a prognostic and predictive biomarker for TBI.

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Philip L. Perez, Sarah S. Wang, Susan Heath, Jennifer Henderson-Sabes, Danielle Mizuiri, Leighton B. Hinkley, Srikantan S. Nagarajan, Paul S. Larson and Steven W. Cheung

OBJECTIVE

The object of this study was to define caudate nucleus locations responsive to intraoperative direct electrical stimulation for tinnitus loudness modulation and relate those locations to functional connectivity maps between caudate nucleus subdivisions and auditory cortex.

METHODS

Six awake study participants who underwent bilateral deep brain stimulation (DBS) electrode placement in the caudate nucleus as part of a phase I clinical trial were analyzed for tinnitus modulation in response to acute stimulation at 20 locations. Resting-state 3-T functional MRI (fMRI) was used to compare connectivity strength between centroids of tinnitus loudness-reducing or loudness-nonreducing caudate locations and the auditory cortex in the 6 DBS phase I trial participants and 14 other neuroimaging participants with a Tinnitus Functional Index > 50.

RESULTS

Acute tinnitus loudness reduction was observed at 5 caudate locations, 4 positioned at the body and 1 at the head of the caudate nucleus in normalized Montreal Neurological Institute space. The remaining 15 electrical stimulation interrogations of the caudate head failed to reduce tinnitus loudness. Compared to the caudate head, the body subdivision had stronger functional connectivity to the auditory cortex on fMRI (p < 0.05).

CONCLUSIONS

Acute tinnitus loudness reduction was more readily achieved by electrical stimulation of the caudate nucleus body. Compared to the caudate head, the caudate body has stronger functional connectivity to the auditory cortex. These first-in-human findings provide insight into the functional anatomy of caudate nucleus subdivisions and may inform future target selection in a basal ganglia–centric neuromodulation approach to treat medically refractory tinnitus.

Clinical trial registration no.: NCT01988688 (clinicaltrials.gov)