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Deciphering the frontostriatal circuitry through the fiber dissection technique: direct structural evidence on the morphology and axonal connectivity of the fronto-caudate tract

Spyridon Komaitis, Christos Koutsarnakis, Evgenia Lani, Theodosis Kalamatianos, Evangelos Drosos, Georgios P. Skandalakis, Faidon Liakos, Evangelia Liouta, Aristotelis V. Kalyvas, and George Stranjalis

OBJECTIVE

The authors sought to investigate the very existence and map the topography, morphology, and axonal connectivity of a thus far ill-defined subcortical pathway known as the fronto-caudate tract (FCT) since there is a paucity of direct structural evidence regarding this pathway in the relevant literature.

METHODS

Twenty normal adult cadaveric formalin-fixed cerebral hemispheres (10 left and 10 right) were explored through the fiber microdissection technique. Lateral to medial and medial to lateral dissections were carried out in a tandem manner in all hemispheres. Attention was focused on the prefrontal area and central core since previous diffusion tensor imaging studies have recorded the tract to reside in this territory.

RESULTS

In all cases, the authors readily identified the FCT as a fan-shaped pathway lying in the most medial layer of the corona radiata and traveling across the subependymal plane before terminating on the superolateral margin of the head and anterior part of the body of the caudate nucleus. The FCT could be adequately differentiated from adjacent fiber tracts and was consistently recorded to terminate in Brodmann areas 8, 9, 10, and 11 (anterior pre–supplementary motor area and the dorsolateral, frontopolar, and fronto-orbital prefrontal cortices). The authors were also able to divide the tract into a ventral and a dorsal segment according to the respective topography and connectivity observed. Hemispheric asymmetries were not observed, but instead the authors disclosed asymmetry within the FCT, with the ventral segment always being thicker and bulkier than the dorsal one.

CONCLUSIONS

By using the fiber microdissection technique, the authors provide sound structural evidence on the topography, morphology, and connectional anatomy of the FCT as a distinct part of a wider frontostriatal circuitry. The findings are in line with the tract’s putative functional implications in high-order motor and behavioral processes and can potentially inform current surgical practice in the fields of neuro-oncology and functional neurosurgery.

In Journal of Neurosurgery Publish Before Print

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Fine configuration of the dural fibrous network and the extradural neural axis compartment in the jugular foramen: an epoxy sheet plastination and confocal microscopy study

Jacob D. Bond, Zhaoyang Xu, and Ming Zhang

OBJECTIVE

The extradural neural axis compartment (EDNAC) is an adipovenous zone that is located between the meningeal (ML) and endosteal (EL) layers of the dura mater and has been minimally investigated in the jugular foramen (JF) region. In this study, the authors aimed to explore the fine architecture of the EDNAC within the JF and evaluate whether the EDNAC can be used as a component for JF compartmentalization.

METHODS

A total of 46 cadaveric heads (31 male, 15 female; age range 54–96 years) and 30 dry skulls were examined in this study. Twelve of 46 cadaveric heads were plastinated as a series of transverse (7 sets), coronal (3 sets), and sagittal (2 sets) slices and examined using stereomicroscopy and confocal microscopy. The dural entry points of the JF cranial nerves were recorded in 34 cadaveric skulls. The volumes of the JF, intraforaminal EDNAC, and internal jugular vein (IJV) were quantified.

RESULTS

Based on constant osseous landmarks, the JF was subdivided into preforaminal, intraforaminal, and subforaminal segments. The ML-derived fascial sheath along the anteromedial wall of the IJV demarcated the “venous portion” and the “EDNAC portion” of the bipartite JF. The EDNAC did not surround the intraforaminal IJV and comprised an ML-derived dural fibrous network and an adipose matrix. A fibrovenous curtain subdivided the intraforaminal EDNAC into a small anterior column containing cranial nerve (CN) IX and the anterior condylar venous plexus and a large posterior adipose column containing CNs X and XI. In the intraforaminal segment, the IJV occupied a slightly larger space in the foramen (57%; p < 0.01), whereas in the subforaminal segment it occupied a space of similar size to that of the EDNAC.

CONCLUSIONS

Excluding the IJV, the neurovascular structures in the JF traverse the dural fibrous network that is dominant in the foraminal EDNAC. The results of this study will contribute to anatomical knowledge of the obscure yet crucially important JF region, increase understanding of foraminal tumor growth and spread patterns, and facilitate the planning and execution of surgical interventions.

In Journal of Neurosurgery Volume 135: Issue 1 (Jul 2021)

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Comparative anatomical analysis between the minipterional and supraorbital approaches

Rafael Martínez-Pérez, Thiago Albonette-Felicio, Douglas A. Hardesty, and Daniel M. Prevedello

OBJECTIVE

Keyhole approaches, namely the minipterional approach (MPTa) and the supraorbital approach (SOa), are alternatives to the standard pterional approach to treat lesions located in the anterior and middle cranial fossae. Despite their increasing popularity and acceptance, the indications and limitations of these approaches require further assessment. The purpose of the present study was to determine the differences in the area of surgical exposure and surgical maneuverability provided by the MPTa and SOa.

METHODS

The areas of surgical exposure afforded by the MPTa and SOa were analyzed in 12 sides of cadaver heads by using a microscope and a neuronavigation system. The area of exposure of the region of interest and surgical freedom (maneuverability) of each approach were calculated.

RESULTS

The area of exposure was significantly larger in the MPTa than in the SOa (1250 ± 223 mm2 vs 939 ± 139 mm2, p = 0.002). The MPTa provided larger areas of exposure in the ipsilateral and midline compartments, whereas there was no significant difference in the area of exposure in the contralateral compartment. All targets in the anterior circulation had significantly larger areas of surgical freedom when treated via the MPTa versus the SOa.

CONCLUSIONS

The MPTa provides greater surgical exposure and better maneuverability than that offered by the SOa. The SOa may be advantageous as a direct corridor for treating lesions located in the contralateral side or in the anterior cranial fossa, but the surgical exposure provided in the midline region is inferior to that exposed by the MPTa.

In Journal of Neurosurgery Volume 134: Issue null (Apr 2021)

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Comparative anatomical analysis between the minipterional and supraorbital approaches

Rafael Martínez-Pérez, Thiago Albonette-Felicio, Douglas A. Hardesty, and Daniel M. Prevedello

OBJECTIVE

Keyhole approaches, namely the minipterional approach (MPTa) and the supraorbital approach (SOa), are alternatives to the standard pterional approach to treat lesions located in the anterior and middle cranial fossae. Despite their increasing popularity and acceptance, the indications and limitations of these approaches require further assessment. The purpose of the present study was to determine the differences in the area of surgical exposure and surgical maneuverability provided by the MPTa and SOa.

METHODS

The areas of surgical exposure afforded by the MPTa and SOa were analyzed in 12 sides of cadaver heads by using a microscope and a neuronavigation system. The area of exposure of the region of interest and surgical freedom (maneuverability) of each approach were calculated.

RESULTS

The area of exposure was significantly larger in the MPTa than in the SOa (1250 ± 223 mm2 vs 939 ± 139 mm2, p = 0.002). The MPTa provided larger areas of exposure in the ipsilateral and midline compartments, whereas there was no significant difference in the area of exposure in the contralateral compartment. All targets in the anterior circulation had significantly larger areas of surgical freedom when treated via the MPTa versus the SOa.

CONCLUSIONS

The MPTa provides greater surgical exposure and better maneuverability than that offered by the SOa. The SOa may be advantageous as a direct corridor for treating lesions located in the contralateral side or in the anterior cranial fossa, but the surgical exposure provided in the midline region is inferior to that exposed by the MPTa.

In Journal of Neurosurgery Publish Before Print

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Histology of the vertebral artery–dural junction: relevance to posterolateral approaches to the skull base

Robert C. Rennert, Martin P. Powers, Jeffrey A. Steinberg, Takanori Fukushima, John D. Day, Alexander A. Khalessi, and Michael L. Levy

OBJECTIVE

The far-lateral and extreme-lateral infrajugular transcondylar–transtubercular exposure (ELITE) and extreme-lateral transcondylar transodontoid (ELTO) approaches provide access to lesions of the foramen magnum, inferolateral to mid-clivus, and ventral pons and medulla. A subset of pathologies in this region require manipulation of the vertebral artery (VA)–dural interface. Although a cuff of dura is commonly left on the VA to avoid vessel injury during these approaches, there are varying descriptions of the degree of VA-dural separation that is safely achievable. In this paper the authors provide a detailed histological analysis of the VA-dural junction to guide microsurgical technique for posterolateral skull base approaches.

METHODS

An ELITE approach was performed on 6 preserved adult cadaveric specimens. The VA-dural entry site was resected, processed for histological analysis, and qualitatively assessed by a neuropathologist.

RESULTS

Histological analysis demonstrated a clear delineation between the intima and media of the VA in all specimens. No clear plane was identified between the connective tissue of the dura and the connective tissue of the VA adventitia.

CONCLUSIONS

The VA forms a contiguous plane with the connective tissue of the dura at its dural entry site. When performing posterolateral skull base approaches requiring manipulation of the VA-dural interface, maintenance of a dural cuff on the VA is critical to minimize the risk of vascular injury.

In Journal of Neurosurgery Volume 134: Issue null (Jan 2021)

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Spatial convergence of distant cortical regions during folding explains why arteries do not cross the sylvian fissure

Alan Bush, Maximiliano Nuñez, Alyssa K. Brisbin, Robert M. Friedlander, and Ezequiel Goldschmidt

OBJECTIVE

Cortical folding places regions that are separated by a large distance along the cortical surface in close proximity. This process is not homogeneous; regions such as the insular opercula have a much higher cortical surface distance (CSD) to euclidean distance (ED) than others. Here the authors explore the hypothesis that in the folded brain the CSD, and not the ED, determines regions of common irrigation, because this measure corresponds more closely with the distance along the prefolded brain, where the subarachnoid arterial vascular network starts forming.

METHODS

The authors defined a convergence index that compared the ED to the CSD and applied it to the cortical surface reconstruction of an average brain. They then compared cortical convergence to the irrigation patterns of major sulci and fissures of the brain, by assessing whether these structures were crossed or not crossed by arterial vessels in 20 fixed hemispheres.

RESULTS

The regions of highest convergence (top 1%) were clustered around the sylvian fissure, which is the only brain depression with high convergence values along its edges. Arterial crossings were commonly observed in every major sulcus of the brain, with the exception of the sylvian fissure, constituting a highly significant difference (p < 10−4).

CONCLUSIONS

Arteries do not cross regions of high convergence. In the adult brain the CSD, rather than the ED, predicts the regional irrigation pattern. The distant origin of the frontal and temporal lobes creates a region of high cortical convergence, which explains why arteries do not cross the sylvian fissure.

In Journal of Neurosurgery Volume 133: Issue null (Dec 2020)

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The frontal longitudinal system as revealed through the fiber microdissection technique: structural evidence underpinning the direct connectivity of the prefrontal-premotor circuitry

Spyridon Komaitis, Aristotelis V. Kalyvas, Georgios P. Skandalakis, Evangelos Drosos, Evgenia Lani, Evangelia Liouta, Faidon Liakos, Theodosis Kalamatianos, Maria Piagkou, John A. Emelifeonwu, George Stranjalis, and Christos Koutsarnakis

OBJECTIVE

The purpose of this study was to investigate the morphology, connectivity, and correlative anatomy of the longitudinal group of fibers residing in the frontal area, which resemble the anterior extension of the superior longitudinal fasciculus (SLF) and were previously described as the frontal longitudinal system (FLS).

METHODS

Fifteen normal adult formalin-fixed cerebral hemispheres collected from cadavers were studied using the Klingler microdissection technique. Lateral to medial dissections were performed in a stepwise fashion starting from the frontal area and extending to the temporoparietal regions.

RESULTS

The FLS was consistently identified as a fiber pathway residing just under the superficial U-fibers of the middle frontal gyrus or middle frontal sulcus (when present) and extending as far as the frontal pole. The authors were able to record two different configurations: one consisting of two distinct, parallel, longitudinal fiber chains (13% of cases), and the other consisting of a single stem of fibers (87% of cases). The fiber chains’ cortical terminations in the frontal and prefrontal area were also traced. More specifically, the FLS was always recorded to terminate in Brodmann areas 6, 46, 45, and 10 (premotor cortex, dorsolateral prefrontal cortex, pars triangularis, and frontal pole, respectively), whereas terminations in Brodmann areas 4 (primary motor cortex), 47 (pars orbitalis), and 9 were also encountered in some specimens. In relation to the SLF system, the FLS represented its anterior continuation in the majority of the hemispheres, whereas in a few cases it was recorded as a completely distinct tract. Interestingly, the FLS comprised shorter fibers that were recorded to interconnect exclusively frontal areas, thus exhibiting different fiber architecture when compared to the long fibers forming the SLF.

CONCLUSIONS

The current study provides consistent, focused, and robust evidence on the morphology, architecture, and correlative anatomy of the FLS. This fiber system participates in the axonal connectivity of the prefrontal-premotor cortices and allegedly subserves cognitive-motor functions. Based in the SLF hypersegmentation concept that has been advocated by previous authors, the FLS should be approached as a distinct frontal segment within the superior longitudinal system.

In Journal of Neurosurgery Volume 133: Issue 5 (Nov 2020)

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Neural and vascular architecture of the septum pellucidum: an anatomical study and considerations for safe endoscopic septum pellucidotomy

Laszlo Barany, Cintia Meszaros, Oliver Ganslandt, Michael Buchfelder, and Peter Kurucz

OBJECTIVE

The septum pellucidum is a bilateral thin membranous structure representing the border between the frontal horns of the lateral ventricles. Its most examined components are the septal veins due to their surgical importance during endoscopic septum pellucidotomy (ESP), which is a well-accepted method for surgical treatment of unilateral hydrocephalus. It is widely accepted that the septum pellucidum contains nerve fibers as well, but interestingly, no anatomical study has been addressed to its neural components before. The aim of the present study was to identify these elements as well as their relations to the septal veins and to define major landmarks within the ventricular system for neurosurgical use.

METHODS

Nine formalin-fixed human cadaveric brains (18 septa pellucida) were involved in this study. A central block containing both septa pellucida was removed and frozen at −30°C for 2 weeks in 7 cases. The fibers of the septum pellucidum and the adjacent areas including the venous elements were dissected under magnification by using homemade wooden spatulas and microsurgical instruments. In 2 cases a histological technique was used to validate the findings of the dissections. The blocks were sliced, embedded in paraffin, cut in 7-µm-thick slices, and then stained as follows: 1) with H & E, 2) with Luxol fast blue combined with cresyl violet, and 3) with Luxol fast blue combined with Sirius red.

RESULTS

The septum pellucidum and the subjacent septum verum form the medial wall of the frontal horn of the lateral ventricle. Both structures contain nerve fibers that were organized in 3 groups: 1) the precommissural fibers of the fornix; 2) the inferior fascicle; and 3) the superior fascicle of the septum pellucidum. The area directly rostral to the postcommissural column of the fornix consisted of macroscopically identifiable gray matter corresponding to the septal nuclei. The histological examinations validated the findings of the authors’ fiber dissections.

CONCLUSIONS

The nerve elements of the septum pellucidum as well as the subjacent septum verum were identified with fiber dissection and verified with histology for the first time. The septal nuclei located just anterior to the fornix and the precommissural fibers of the fornix should be preserved during ESP. Considering the venous anatomy as well as the neural architecture of the septum pellucidum, the fenestration should ideally be placed above the superior edge of the fornix and preferably dorsal to the interventricular foramen.

In Journal of Neurosurgery Volume 133: Issue 3 (Sep 2020)

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Quantitative analysis of ipsilateral and contralateral supracerebellar infratentorial and occipital transtentorial approaches to the cisternal pulvinar: laboratory anatomical investigation

Qing Sun, Xiaochun Zhao, Sirin Gandhi, Ali Tayebi Meybodi, Evgenii Belykh, Daniel Valli, Claudio Cavallo, Leandro Borba Moreira, Peter Nakaji, Michael T. Lawton, and Mark C. Preul

OBJECTIVE

The cisternal pulvinar is a challenging location for neurosurgery. Four approaches for reaching the pulvinar without cortical transgression are the ipsilateral supracerebellar infratentorial (iSCIT), contralateral supracerebellar infratentorial (cSCIT), ipsilateral occipital transtentorial (iOCTT), and contralateral occipital transtentorial/falcine (cOCTF) approaches. This study quantitatively compared these approaches in terms of surgical exposure and maneuverability.

METHODS

Each of the 4 approaches was performed in 4 cadaveric heads (8 specimens in total). A 6-sided anatomical polygonal region was configured over the cisternal pulvinar, defined by 6 reachable anatomical points in different vectors. Multiple polygons were subsequently formed to calculate the areas of exposure. The surgical freedom of each approach was calculated as the maximum allowable working area at the proximal end of a probe, with the distal end fixed at the posterior pole of the pulvinar. Areas of exposure, surgical freedom, and the working distance (surgical depth) of all approaches were compared.

RESULTS

No significant difference was found among the 4 different approaches with regard to the surgical depth, surgical freedom, or medial exposure area of the pulvinar. In the pairwise comparison, the cSCIT approach provided a significantly larger lateral exposure (39 ± 9.8 mm2) than iSCIT (19 ± 10.3 mm2, p < 0.01), iOCTT (19 ± 8.2 mm2, p < 0.01), and cOCTF (28 ± 7.3 mm2, p = 0.02) approaches. The total exposure area with a cSCIT approach (75 ± 23.1 mm2) was significantly larger than with iOCTT (43 ± 16.4 mm2, p < 0.01) and iSCIT (40 ± 20.2 mm2, p = 0.01) approaches (pairwise, p ≤ 0.01).

CONCLUSIONS

The cSCIT approach is preferable among the 4 compared approaches, demonstrating better exposure to the cisternal pulvinar than ipsilateral approaches and a larger lateral exposure than the cOCTF approach. Both contralateral approaches described (cSCIT and cOCTF) provided enhanced lateral exposure to the pulvinar, while the cOCTF provided a larger exposure to the lateral portion of the pulvinar than the iOCTT. Medial exposure and maneuverability did not differ among the approaches. A short tentorium may negatively impact an ipsilateral approach because the cingulate isthmus and parahippocampal gyrus tend to protrude, in which case they can obstruct access to the cisternal pulvinar ipsilaterally.

In Journal of Neurosurgery Volume 133: Issue 4 (Oct 2020)

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Surgical approaches for the lateral mesencephalic sulcus

Daniel Dutra Cavalcanti, Bárbara Albuquerque Morais, Eberval Gadelha Figueiredo, Robert F. Spetzler, and Mark C. Preul

OBJECTIVE

The brainstem is a compact, delicate structure. The surgeon must have good anatomical knowledge of the safe entry points to safely resect intrinsic lesions. Lesions located at the lateral midbrain surface are better approached through the lateral mesencephalic sulcus (LMS). The goal of this study was to compare the surgical exposure to the LMS provided by the subtemporal (ST) approach and the paramedian and extreme-lateral variants of the supracerebellar infratentorial (SCIT) approach.

METHODS

These 3 approaches were used in 10 cadaveric heads. The authors performed measurements of predetermined points by using a neuronavigation system. Areas of microsurgical exposure and angles of the approaches were determined. Statistical analysis was performed to identify significant differences in the respective exposures.

RESULTS

The surgical exposure was similar for the different approaches—369.8 ± 70.1 mm2 for the ST; 341.2 ± 71.2 mm2 for the SCIT paramedian variant; and 312.0 ± 79.3 mm2 for the SCIT extreme-lateral variant (p = 0.13). However, the vertical angular exposure was 16.3° ± 3.6° for the ST, 19.4° ± 3.4° for the SCIT paramedian variant, and 25.1° ± 3.3° for the SCIT extreme-lateral variant craniotomy (p < 0.001). The horizontal angular exposure was 45.2° ± 6.3° for the ST, 35.6° ± 2.9° for the SCIT paramedian variant, and 45.5° ± 6.6° for the SCIT extreme-lateral variant opening, presenting no difference between the ST and extreme-lateral variant (p = 0.92), but both were superior to the paramedian variant (p < 0.001). Data are expressed as the mean ± SD.

CONCLUSIONS

The extreme-lateral SCIT approach had the smaller area of surgical exposure; however, these differences were not statistically significant. The extreme-lateral SCIT approach presented a wider vertical and horizontal angle to the LMS compared to the other craniotomies. Also, it provides a 90° trajectory to the sulcus that facilitates the intraoperative microsurgical technique.

In Journal of Neurosurgery Volume 132: Issue 5 (May 2020)