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Kaan Yagmurlu, Erik H. Middlebrooks, Necmettin Tanriover and Albert L. Rhoton Jr.

OBJECT

The aim of this study was to examine the arcuate (AF) and superior longitudinal fasciculi (SLF), which together form the dorsal language stream, using fiber dissection and diffusion imaging techniques in the human brain.

METHODS

Twenty-five formalin-fixed brains (50 hemispheres) and 3 adult cadaveric heads, prepared according to the Klingler method, were examined by the fiber dissection technique. The authors’ findings were supported with MR tractography provided by the Human Connectome Project, WU-Minn Consortium. The frequencies of gyral distributions were calculated in segments of the AF and SLF in the cadaveric specimens.

RESULTS

The AF has ventral and dorsal segments, and the SLF has 3 segments: SLF I (dorsal pathway), II (middle pathway), and III (ventral pathway). The AF ventral segment connects the middle (88%; all percentages represent the area of the named structure that is connected to the tract) and posterior (100%) parts of the superior temporal gyri and the middle part (92%) of the middle temporal gyrus to the posterior part of the inferior frontal gyrus (96% in pars opercularis, 40% in pars triangularis) and the ventral premotor cortex (84%) by passing deep to the lower part of the supramarginal gyrus (100%). The AF dorsal segment connects the posterior part of the middle (100%) and inferior temporal gyri (76%) to the posterior part of the inferior frontal gyrus (96% in pars opercularis), ventral premotor cortex (72%), and posterior part of the middle frontal gyrus (56%) by passing deep to the lower part of the angular gyrus (100%).

CONCLUSIONS

This study depicts the distinct subdivision of the AF and SLF, based on cadaveric fiber dissection and diffusion imaging techniques, to clarify the complicated language processing pathways.

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Abuzer Güngör, Serhat Baydin, Erik H. Middlebrooks, Necmettin Tanriover, Cihan Isler and Albert L. Rhoton Jr.

OBJECTIVE

The relationship of the white matter tracts to the lateral ventricles is important when planning surgical approaches to the ventricles and in understanding the symptoms of hydrocephalus. The authors' aim was to explore the relationship of the white matter tracts of the cerebrum to the lateral ventricles using fiber dissection technique and MR tractography and to discuss these findings in relation to approaches to ventricular lesions.

METHODS

Forty adult human formalin-fixed cadaveric hemispheres (20 brains) and 3 whole heads were examined using fiber dissection technique. The dissections were performed from lateral to medial, medial to lateral, superior to inferior, and inferior to superior. MR tractography showing the lateral ventricles aided in the understanding of the 3D relationships of the white matter tracts with the lateral ventricles.

RESULTS

The relationship between the lateral ventricles and the superior longitudinal I, II, and III, arcuate, vertical occipital, middle longitudinal, inferior longitudinal, inferior frontooccipital, uncinate, sledge runner, and lingular amygdaloidal fasciculi; and the anterior commissure fibers, optic radiations, internal capsule, corona radiata, thalamic radiations, cingulum, corpus callosum, fornix, caudate nucleus, thalamus, stria terminalis, and stria medullaris thalami were defined anatomically and radiologically. These fibers and structures have a consistent relationship to the lateral ventricles.

CONCLUSIONS

Knowledge of the relationship of the white matter tracts of the cerebrum to the lateral ventricles should aid in planning more accurate surgery for lesions within the lateral ventricles.

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Abuzer Güngör, Şevki Serhat Baydın, Vanessa M. Holanda, Erik H. Middlebrooks, Cihan Isler, Bekir Tugcu, Kelly Foote and Necmettin Tanriover

OBJECTIVE

Despite the extensive use of the subthalamic nucleus (STN) as a deep brain stimulation (DBS) target, unveiling the extensive functional connectivity of the nucleus, relating its structural connectivity to the stimulation-induced adverse effects, and thus optimizing the STN targeting still remain challenging. Mastering the 3D anatomy of the STN region should be the fundamental goal to achieve ideal surgical results, due to the deep-seated and obscure position of the nucleus, variable shape and relatively small size, oblique orientation, and extensive structural connectivity. In the present study, the authors aimed to delineate the 3D anatomy of the STN and unveil the complex relationship between the anatomical structures within the STN region using fiber dissection technique, 3D reconstructions of high-resolution MRI, and fiber tracking using diffusion tractography utilizing a generalized q-sampling imaging (GQI) model.

METHODS

Fiber dissection was performed in 20 hemispheres and 3 cadaveric heads using the Klingler method. Fiber dissections of the brain were performed from all orientations in a stepwise manner to reveal the 3D anatomy of the STN. In addition, 3 brains were cut into 5-mm coronal, axial, and sagittal slices to show the sectional anatomy. GQI data were also used to elucidate the connections among hubs within the STN region.

RESULTS

The study correlated the results of STN fiber dissection with those of 3D MRI reconstruction and tractography using neuronavigation. A 3D terrain model of the subthalamic area encircling the STN was built to clarify its anatomical relations with the putamen, globus pallidus internus, globus pallidus externus, internal capsule, caudate nucleus laterally, substantia nigra inferiorly, zona incerta superiorly, and red nucleus medially. The authors also describe the relationship of the medial lemniscus, oculomotor nerve fibers, and the medial forebrain bundle with the STN using tractography with a 3D STN model.

CONCLUSIONS

This study examines the complex 3D anatomy of the STN and peri-subthalamic area. In comparison with previous clinical data on STN targeting, the results of this study promise further understanding of the structural connections of the STN, the exact location of the fiber compositions within the region, and clinical applications such as stimulation-induced adverse effects during DBS targeting.

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Erik H. Middlebrooks, Sanjeet S. Grewal, Matthew Stead, Brian N. Lundstrom, Gregory A. Worrell and Jamie J. Van Gompel

OBJECTIVE

Deep brain stimulation (DBS) of the anterior nucleus of the thalamus (ANT) is a promising therapy for refractory epilepsy. Unfortunately, the variability in outcomes from ANT DBS is not fully understood. In this pilot study, the authors assess potential differences in functional connectivity related to the volume of tissue activated (VTA) in ANT DBS responders and nonresponders as a means for better understanding the mechanism of action and potentially improving DBS targeting.

METHODS

This retrospective analysis consisted of 6 patients who underwent ANT DBS for refractory epilepsy. Patients were classified as responders (n = 3) if their seizure frequency decreased by at least 50%. The DBS electrodes were localized postoperatively and VTAs were computationally generated based on DBS programming settings. VTAs were used as seed points for resting-state functional MRI connectivity analysis performed using a control dataset. Differences in cortical connectivity to the VTA were assessed between the responder and nonresponder groups.

RESULTS

The ANT DBS responders showed greater positive connectivity with the default mode network compared to nonresponders, including the posterior cingulate cortex, medial prefrontal cortex, inferior parietal lobule, and precuneus. Interestingly, there was also a consistent anticorrelation with the hippocampus seen in responders that was not present in nonresponders.

CONCLUSIONS

Based on their pilot study, the authors observed that successful ANT DBS in patients with epilepsy produces increased connectivity in the default mode network, which the authors hypothesize increases the threshold for seizure propagation. Additionally, an inhibitory effect on the hippocampus mediated through increased hippocampal γ-aminobutyric acid (GABA) concentration may contribute to seizure suppression. Future studies are planned to confirm these findings.

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Satoshi Matsuo, Serhat Baydin, Abuzer Güngör, Erik H. Middlebrooks, Noritaka Komune, Koji Iihara and Albert L. Rhoton Jr.

OBJECTIVE

A postoperative visual field defect resulting from damage to the occipital lobe during surgery is a unique complication of the occipital transtentorial approach. Though the association between patient position and this complication is well investigated, preventing the complication remains a challenge. To define the area of the occipital lobe in which retraction is least harmful, the surface anatomy of the brain, course of the optic radiations, and microsurgical anatomy of the occipital transtentorial approach were examined.

METHODS

Twelve formalin-fixed cadaveric adult heads were examined with the aid of a surgical microscope and 0° and 45° endoscopes. The optic radiations were examined by fiber dissection and MR tractography techniques.

RESULTS

The arterial and venous relationships of the lateral, medial, and inferior surfaces of the occipital lobe were defined anatomically. The full course of the optic radiations was displayed via both fiber dissection and MR tractography. Although the stems of the optic radiations as exposed by both techniques are similar, the terminations of the fibers are slightly different. The occipital transtentorial approach provides access for the removal of lesions involving the splenium, pineal gland, collicular plate, cerebellomesencephalic fissure, and anterosuperior part of the cerebellum. An angled endoscope can aid in exposing the superior medullary velum and superior cerebellar peduncles.

CONCLUSIONS

Anatomical findings suggest that retracting the inferior surface of the occipital lobe may avoid direct damage and perfusion deficiency around the calcarine cortex and optic radiations near their termination. An accurate understanding of the course of the optic radiations and vascular relationships around the occipital lobe and careful retraction of the inferior surface of the occipital lobe may reduce the incidence of postoperative visual field defect.

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Karim ReFaey, Kaisorn L. Chaichana, Anteneh M. Feyissa, Tito Vivas-Buitrago, Benjamin H. Brinkmann, Erik H. Middlebrooks, Jake H. McKay, David J. Lankford, Shashwat Tripathi, Elird Bojaxhi, Grayson E. Roth, William O. Tatum and Alfredo Quiñones-Hinojosa

OBJECTIVE

Epilepsy is common among patients with supratentorial brain tumors; approximately 40%–70% of patients with glioma develop brain tumor–related epilepsy (BTRE). Intraoperative localization of the epileptogenic zone during surgical tumor resection (real-time data) may improve intervention techniques in patients with lesional epilepsy, including BTRE. Accurate localization of the epileptogenic signals requires electrodes with high-density spatial organization that must be placed on the cortical surface during surgery. The authors investigated a 360° high-density ring-shaped cortical electrode assembly device, called the “circular grid,” that allows for simultaneous tumor resection and real-time electrophysiology data recording from the brain surface.

METHODS

The authors collected data from 99 patients who underwent awake craniotomy from January 2008 to December 2018 (29 patients with the circular grid and 70 patients with strip electrodes), of whom 50 patients were matched-pair analyzed (25 patients with the circular grid and 25 patients with strip electrodes). Multiple variables were then retrospectively assessed to determine if utilization of this device provides more accurate real-time data and improves patient outcomes.

RESULTS

Matched-pair analysis showed higher extent of resection (p = 0.03) and a shorter transient motor recovery period during the hospitalization course (by approximately 6.6 days, p ≤ 0.05) in the circular grid patients. Postoperative versus preoperative Karnofsky Performance Scale (KPS) score difference/drop was greater for the strip electrode patients (p = 0.007). No significant difference in postoperative seizures between the 2 groups was present (p = 0.80).

CONCLUSIONS

The circular grid is a safe, feasible tool that grants direct access to the cortical surgical surface for tissue resection while simultaneously monitoring electrical activity. Application of the circular grid to different brain pathologies may improve intraoperative epileptogenic detection accuracy and functional outcomes, while decreasing postoperative complications.

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Sanjeet S. Grewal, Erik H. Middlebrooks, Timothy J. Kaufmann, Matthew Stead, Brian N. Lundstrom, Gregory A. Worrell, Chen Lin, Serhat Baydin and Jamie J. Van Gompel

When medically intractable epilepsy is multifocal or focal but poorly localized, neuromodulation can be useful therapy. One such technique is deep brain stimulation (DBS) targeting the anterior nucleus of the thalamus (ANT). Unfortunately, the ANT is difficult to visualize in standard MRI sequences and its indirect targeting is difficult because of thalamic variability and atrophy in patients with epilepsy. The following study describes the novel use of the fast gray matter acquisition T1 inversion recovery (FGATIR) MRI sequence to delineate the mammillothalamic tract for direct targeting of the ANT through visualizing the termination of the mammillothalamic tract in the ANT.

The day prior to surgery in a 19-year-old, right-handed woman with a 5-year history of epilepsy, MRI was performed on a 3-T Siemens Prisma scanner (Siemens AG, Healthcare Sector) using a 64-channel head and neck coil. As part of the imaging protocol, noncontrast magnetization-prepared rapid gradient echo (MP-RAGE) and diffusion tensor imaging (DTI) sequences were obtained for targeting purposes. The ANT was directly targeted using the FGATIR sequence, and bilateral Medtronic 3389 leads were placed. At the last follow-up (2 months), the patient reported an approximate 75% decrease in seizure frequency, as well as a decrease in seizure severity.

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R. Shane Tubbs, Marios Loukas, Mohammadali M. Shoja, Robert J. Spinner, Erik H. Middlebrooks, William R. Stetler Jr., Leslie Acakpo-Satchivi, John C. Wellons III, Jeffrey P. Blount and W. Jerry Oakes

Object

The suprascapular nerve may become entrapped as it travels deep to the suprascapular ligament, necessitating decompression. The present study was performed to verify the feasibility of a minimally invasive, endoscopically assisted technique for decompressing the suprascapular nerve in the supraspinous fossa.

Methods

The authors performed dissection and decompression of the suprascapular ligament using an endoscopically assisted technique via a 3-cm skin incision in 10 adult cadavers (20 sides). Measurements were also made of the depth from the skin to the suprascapular ligament.

Results

A mean depth of 4 cm was necessary to reach the suprascapular ligament from the skin surface. With the authors' approach, no obvious injury occurred to the suprascapular or other vicinal neurovascular structures (such as the spinal accessory nerve and suprascapular vessels).

Conclusions

The results of this cadaveric study demonstrate that access to the suprascapular nerve can be obtained endoscopically via a small suprascapular incision. This approach obviates a large incision, entry into the glenohumeral joint, and reduces the risk of spinal accessory nerve injury in the posterior cervical triangle, or atrophy of the trapezius or supraspinatus muscles from a standard larger dissection. To the authors' knowledge an endoscopically assisted approach to decompressing the suprascapular nerve as it courses deep to the suprascapular ligament has not been reported previously.