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Kaitlyn Casimo, Fabio Grassia, Sandra L. Poliachik, Edward Novotny, Andrew Poliakov and Jeffrey G. Ojemann

Prior studies of functional connectivity following callosotomy have disagreed in the observed effects on interhemispheric functional connectivity. These connectivity studies, in multiple electrophysiological methods and functional MRI, have found conflicting reductions in connectivity or patterns resembling typical individuals. The authors examined a case of partial anterior corpus callosum connection, where pairs of bilateral electrocorticographic electrodes had been placed over homologous regions in the left and right hemispheres. They sorted electrode pairs by whether their direct corpus callosum connection had been disconnected or preserved using diffusion tensor imaging and native anatomical MRI, and they estimated functional connectivity between pairs of electrodes over homologous regions using phase-locking value. They found no significant differences in any frequency band between pairs of electrodes that had their corpus callosum connection disconnected and those that had an intact connection. The authors’ results may imply that the corpus callosum is not an obligatory mediator of connectivity between homologous sites in opposite hemispheres. This interhemispheric synchronization may also be linked to disruption of seizure activity.

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Carter D. Wray, Diana L. Kraemer, Tong Yang, Sandra L. Poliachik, Andrew L. Ko, Andrew Poliakov, Adam O. Hebb, Edward J. Novotny and Jeffrey G. Ojemann

The presurgical evaluation of patients with epilepsy often requires an intracranial study in which both subdural grid electrodes and depth electrodes are needed. Performing a craniotomy for grid placement with a stereotactic frame in place can be problematic, especially in young children, leading some surgeons to consider frameless stereotaxy for such surgery. The authors report on the use of a system that uses electromagnetic impulses to track the tip of the depth electrode. Ten pediatric patients with medically refractory focal lobar epilepsy required placement of both subdural grid and intraparenchymal depth electrodes to map seizure onset. Presurgical frameless stereotaxic targeting was performed using a commercially available electromagnetic image-guided system. Freehand depth electrode placement was then performed with intraoperative guidance using an electromagnetic system that provided imaging of the tip of the electrode, something that has not been possible using visually or sonically based systems. Accuracy of placement of depth electrodes within the deep structures of interest was confirmed postoperatively using CT and CT/MR imaging fusion. Depth electrodes were appropriately placed in all patients. Electromagnetic-tracking–based stereotactic targeting improves the accuracy of freehand placement of depth electrodes in patients with medically refractory epilepsy. The ability to track the electrode tip, rather than the electrode tail, is a major feature that enhances accuracy. Additional advantages of electromagnetic frameless guidance are discussed.

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Fabio Grassia, Andrew V. Poliakov, Sandra L. Poliachik, Kaitlyn Casimo, Seth D. Friedman, Hillary Shurtleff, Carlo Giussani, Edward J. Novotny Jr., Jeffrey G. Ojemann and Jason S. Hauptman

OBJECTIVE

Functional connectivity magnetic resonance imaging (fcMRI) is a form of fMRI that allows for analysis of blood oxygen level–dependent signal changes within a task-free, resting paradigm. This technique has been shown to have efficacy in evaluating network connectivity changes with epilepsy. Presurgical data from patients with unilateral temporal lobe epilepsy were evaluated using the fcMRI technique to define connectivity changes within and between the diseased and healthy temporal lobes using a within-subjects design.

METHODS

Using presurgical fcMRI data from pediatric patients with unilateral temporal lobe epilepsy, the authors performed seed-based analyses within the diseased and healthy temporal lobes. Connectivity within and between temporal lobe seeds was measured and compared.

RESULTS

In the cohort studied, local ipsilateral temporal lobe connectivity was significantly increased on the diseased side compared to the healthy temporal lobe. Connectivity of the diseased side to the healthy side, on the other hand, was significantly reduced when compared to connectivity of the healthy side to the diseased temporal lobe. A statistically significant regression was observed when comparing the changes in local ipsilateral temporal lobe connectivity to the changes in inter–temporal lobe connectivity. A statistically significant difference was also noted in ipsilateral connectivity changes between patients with and those without mesial temporal sclerosis.

CONCLUSIONS

Using fcMRI, significant changes in ipsilateral temporal lobe and inter–temporal lobe connectivity can be appreciated in unilateral temporal lobe epilepsy. Furthermore, fcMRI may have a role in the presurgical evaluation of patients with intractable temporal lobe epilepsy.

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Carter D. Wray, Tim M. Blakely, Sandra L. Poliachik, Andrew Poliakov, Sharon S. McDaniel, Edward J. Novotny, Kai J. Miller and Jeffrey G. Ojemann

Object

The gold-standard method for determining cortical functional organization in the context of neurosurgical intervention is electrical cortical stimulation (ECS), which disrupts normal cortical function to evoke movement. This technique is imprecise, however, as motor responses are not limited to the precentral gyrus. Electrical cortical stimulation also can trigger seizures, is not always tolerated, and is often unsuccessful, especially in children. Alternatively, endogenous motor and sensory signals can be mapped by somatosensory evoked potentials (SSEPs), functional MRI (fMRI), and electrocorticography of high gamma (70–150 Hz) signal power, which reflect normal cortical function. The authors evaluated whether these 4 modalities of mapping sensorimotor function in children produce concurrent results.

Methods

The authors retrospectively examined the charts of all patients who underwent epilepsy surgery at Seattle Children's Hospital between July 20, 1999, and July 1, 2011, and they included all patients in whom the primary motor or somatosensory cortex was localized via 2 or more of the following tests: ECS, SSEP, fMRI, or high gamma electrocorticography (hgECoG).

Results

Inclusion criteria were met by 50 patients, whose mean age at operation was 10.6 years. The youngest patient who underwent hgECoG mapping was 2 years and 10 months old, which is younger than any patient reported on in the literature. The authors localized the putative sensorimotor cortex most often with hgECoG, followed by SSEP and fMRI; ECS was most likely to fail to localize the sensorimotor cortex.

Conclusions

Electrical cortical stimulation, SSEP, fMRI, and hgECoG generally produced concordant localization of motor and sensory function in children. When attempting to localize the sensorimotor cortex in children, hgECoG was more likely to produce results, was faster, safer, and did not require cooperation. The hgECoG maps in pediatric patients are similar to those in adult patients published in the literature. The sensorimotor cortex can be mapped by hgECoG and fMRI in children younger than 3 years old to localize cortical function.

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Sandra L. Poliachik, Andrew V. Poliakov, Laura A. Jansen, Sharon S. McDaniel, Carter D. Wray, John Kuratani, Russell P. Saneto, Jeffrey G. Ojemann and Edward J. Novotny Jr

Object

Imaging-guided surgery (IGS) systems are widely used in neurosurgical practice. During epilepsy surgery, the authors routinely use IGS landmarks to localize intracranial electrodes and/or specific brain regions. The authors have developed a technique to coregister these landmarks with pre- and postoperative scans and the Montreal Neurological Institute (MNI) standard space brain MRI to allow 1) localization and identification of tissue anatomy; and 2) identification of Brodmann areas (BAs) of the tissue resected during epilepsy surgery. Tracking tissue in this fashion allows for better correlation of patient outcome to clinical factors, functional neuroimaging findings, and pathological characteristics and molecular studies of resected tissue.

Methods

Tissue samples were collected in 21 patients. Coordinates from intraoperative tissue localization were downloaded from the IGS system and transformed into patient space, as defined by preoperative high-resolution T1-weighted MRI volume. Tissue landmarks in patient space were then transformed into MNI standard space for identification of the BAs of the tissue samples.

Results

Anatomical locations of resected tissue were identified from the intraoperative resection landmarks. The BAs were identified for 17 of the 21 patients. The remaining patients had abnormal brain anatomy that could not be meaningfully coregistered with the MNI standard brain without causing extensive distortion.

Conclusions

This coregistration and landmark tracking technique allows localization of tissue that is resected from patients with epilepsy and identification of the BAs for each resected region. The ability to perform tissue localization allows investigators to relate preoperative, intraoperative, and postoperative functional and anatomical brain imaging to better understand patient outcomes, improve patient safety, and aid in research.

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Kurt E. Weaver, Andrew Poliakov, Edward J. Novotny, Jared D. Olson, Thomas J. Grabowski and Jeffrey G. Ojemann

OBJECTIVE

The acquisition and refinement of cognitive and behavioral skills during development is associated with the maturation of various brain oscillatory activities. Most developmental investigations have identified distinct patterns of low-frequency electrophysiological activity that are characteristic of various behavioral milestones. In this investigation, the authors focused on the cross-sectional developmental properties of high-frequency spectral power from the brain’s default mode network (DMN) during goal-directed behavior.

METHODS

The authors contrasted regionally specific, time-evolving high gamma power (HGP) in the lateral DMN cortex between 3 young children (age range 3–6 years) and 3 adults by use of electrocorticography (ECoG) recordings over the left perisylvian cortex during a picture-naming task.

RESULTS

Across all participants, a nearly identical and consistent response suppression of HGP, which is a functional signature of the DMN, was observed during task performance recordings acquired from ECoG electrodes placed over the lateral DMN cortex. This finding provides evidence of relatively early maturation of the DMN. Furthermore, only HGP relative to evoked alpha and beta band power showed this level of consistency across all participants.

CONCLUSIONS

Regionally specific, task-evoked suppression of the high-frequency components of the cortical power spectrum is established early in brain development, and this response may reflect the early maturation of specific cognitive and/or computational mechanisms.

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Hillary Shurtleff, Molly Warner, Andrew Poliakov, Brian Bournival, Dennis W. Shaw, Gisele Ishak, Tong Yang, Mahesh Karandikar, Russell P. Saneto, Samuel R. Browd and Jeffrey G. Ojemann

Object

The authors describe their experience with functional MR (fMR) imaging in children as young as 5 years of age, or even younger in developmental age equivalent. Functional MR imaging can be useful for identifying eloquent cortex prior to surgical intervention. Most fMR imaging clinical work has been done in adults, and although children as young as 8 years of age have been included in larger clinical series, cases in younger children are rarely reported.

Methods

The authors reviewed presurgical fMR images in eight patients who were 8 years of age or younger, six of whom were 5 or 6 years of age. Each patient had undergone neuropsychological testing. Three patients functioned at a below-average level, with adaptive functioning age scores of 3 to 4 years. Self-paced finger tapping (with passive movement in one patient) and silent language tasks were used as activation tasks. The language task was modified for younger children, for whom the same (not novel) stimuli were used for extensive practice ahead of time and in the MR imaging unit. Patient preparation involved techniques such as having experienced staff present to work with patients and providing external management during imaging. Six of eight patients had extensive training and practice prior to the procedure. In the two youngest patients, this training included use of a mock MR unit.

Results

All cases yielded successful imaging. Finger tapping in all seven of the patients who could perform it demonstrated focal motor activation in the frontal-parietal region, with expected activation elsewhere, including in the cerebellum. Three of four patients had the expected verb generation task activations, with left-hemisphere dominance, including a 6-year-old child who functioned at the 3-year, 9-month level. The only child (an 8-year-old) who was not prepared prior to the imaging session for the verb generation task failed this task due to movement artifact.

Conclusions

Despite the challenges of successfully using fMR imaging in very young and clinically involved patients, these studies can be performed successfully in children with a chronological age of 5 or 6 years and a developmental age as young as 3 or 4 years.

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Anthony C. Wang, George M. Ibrahim, Andrew V. Poliakov, Page I. Wang, Aria Fallah, Gary W. Mathern, Robert T. Buckley, Kelly Collins, Alexander G. Weil, Hillary A. Shurtleff, Molly H. Warner, Francisco A. Perez, Dennis W. Shaw, Jason N. Wright, Russell P. Saneto, Edward J. Novotny, Amy Lee, Samuel R. Browd and Jeffrey G. Ojemann

OBJECTIVE

The potential loss of motor function after cerebral hemispherectomy is a common cause of anguish for patients, their families, and their physicians. The deficits these patients face are individually unique, but as a whole they provide a framework to understand the mechanisms underlying cortical reorganization of motor function. This study investigated whether preoperative functional MRI (fMRI) and diffusion tensor imaging (DTI) could predict the postoperative preservation of hand motor function.

METHODS

Thirteen independent reviewers analyzed sensorimotor fMRI and colored fractional anisotropy (CoFA)–DTI maps in 25 patients undergoing functional hemispherectomy for treatment of intractable seizures. Pre- and postoperative gross hand motor function were categorized and correlated with fMRI and DTI findings, specifically, abnormally located motor activation on fMRI and corticospinal tract atrophy on DTI.

RESULTS

Normal sensorimotor cortical activation on preoperative fMRI was significantly associated with severe decline in postoperative motor function, demonstrating 92.9% sensitivity (95% CI 0.661–0.998) and 100% specificity (95% CI 0.715–1.00). Bilaterally robust, symmetric corticospinal tracts on CoFA-DTI maps were significantly associated with severe postoperative motor decline, demonstrating 85.7% sensitivity (95% CI 0.572–0.982) and 100% specificity (95% CI 0.715–1.00). Interpreting the fMR images, the reviewers achieved a Fleiss’ kappa coefficient (κ) for interrater agreement of κ = 0.69, indicating good agreement (p < 0.01). When interpreting the CoFA-DTI maps, the reviewers achieved κ = 0.64, again indicating good agreement (p < 0.01).

CONCLUSIONS

Functional hemispherectomy offers a high potential for seizure freedom without debilitating functional deficits in certain instances. Patients likely to retain preoperative motor function can be identified prior to hemispherectomy, where fMRI or DTI suggests that cortical reorganization of motor function has occurred prior to the operation.